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Telencephalon and geometric space in goldfish
European Journal of Neuroscience
Abstract
Neuroanatomical evidence indicates that the lateral pallium (LP) of ray-finned fishes could be homologous to the hippocampus of mammals and birds. Recent studies have found that hippocampus of mammals and birds is critical for learning geometric properties of space. In this work, we studied the effects of lesions to the lateral pallium of goldfish on the encoding of geometric spatial information. Goldfish with telencephalic lesions were trained to search for a goal in a rectangular-shaped arena containing one different wall that served as the only distinctive environmental feature. Although fish with lateral pallium lesions learned the task even faster than sham and medial pallium (MP)-lesioned animals, subsequent probe trials showed that they were insensitive to geometric information. Sham and medial pallium-lesioned animals could use both geometric and feature information to locate the goal. By contrast, fish with lateral palium lesions relied exclusively on the feature information provided by the wall of a different colour. These results indicate that lesions to the lateral pallium of goldfish, like hippocampal lesions in mammals and birds, selectively impair the encoding of geometric spatial information of environmental space. Thus, the forebrain structures of teleost fish that are neuroanatomically equivalent to the mammalian and avian hippocampus also share a central role in supporting spatial cognition. Present results suggest that the presence of a hippocampal-dependent memory system implicated in the processing of geometric spatial information is an ancient feature of the vertebrate forebrain that has been conserved during the divergent evolution of different vertebrate groups.
... Furthermore, the research team of Vargas [73] also found a place-cue learning dissociation during geometric navigation after damaging the lateral pallium of goldfish (the assumed homologue of the mammalian hippocampus). Fish with lateral pallium lesions, in contrast with those with medial pallium lesions and sham controls, were unable to use the arena's spatial geometry and, instead, just relied on the landmark. ...
... For instance, a study by Gómez and colleagues [99] revealed that map-like spatial representations in goldfish could be compromised by blocking hippocampal N-methyl-D-aspartate (NMDA) receptors. In goldfish, the recruitment of the dorsolateral telencephalon has been demonstrated multiple times in the use of geometry [73,100]. Following their initial study [73], Vargas and colleagues [100] went further into the investigation of specific telencephalic ablations on geometric navigation in the absence of other featural cues. ...
... In goldfish, the recruitment of the dorsolateral telencephalon has been demonstrated multiple times in the use of geometry [73,100]. Following their initial study [73], Vargas and colleagues [100] went further into the investigation of specific telencephalic ablations on geometric navigation in the absence of other featural cues. Differently from previous results, they noticed that lateral pallium lesions did not entirely impair the ability of goldfish to reorient by geometry when the goal position was unambiguous (two escape corners instead of one). ...
Simple Summary
Animals inhabit species-specific ecological environments and acquire knowledge about the surrounding space to adaptively behave and move within it. Spatial cognition is important for achieving basic survival actions such as detecting the position of a food site or a mate, going back home or hiding from a predator. As such, animals possess multiple mechanisms for spatial mapping, including the use of individual reference points or positional relationships among them. One such mechanism allows disoriented animals to navigate according to the distinctive geometry of the environment: within a rectangular enclosure, they can simply reorient by using “metrics” (e.g., longer/shorter, closer/farther) and “sense” (e.g., left, right) attributes. Navigation based on the environmental geometry has been widely investigated across the animal kingdom, including fishes. In particular, research on teleost fish has contributed to the general understanding of geometric representations through both visual and extra-visual modalities, even vertebrates phylogenetically remote from mammals.
Abstract
Fishes navigate through underwater environments with remarkable spatial precision and memory. Freshwater and seawater species make use of several orientation strategies for adaptative behavior that is on par with terrestrial organisms, and research on cognitive mapping and landmark use in fish have shown that relational and associative spatial learning guide goal-directed navigation not only in terrestrial but also in aquatic habitats. In the past thirty years, researchers explored spatial cognition in fishes in relation to the use of environmental geometry, perhaps because of the scientific value to compare them with land-dwelling animals. Geometric navigation involves the encoding of macrostructural characteristics of space, which are based on the Euclidean concepts of “points”, “surfaces”, and “boundaries”. The current review aims to inspect the extant literature on navigation by geometry in fishes, emphasizing both the recruitment of visual/extra-visual strategies and the nature of the behavioral task on orientation performance.
... These homologies led to the hypothesis that lesions of the DM or DL would have the same behavioral effects as lesions of the amygdala or hippocampus in mammals. Research generated primarily by researchers at the Universidad de Sevilla has largely supported this hypothesis (Portovella et al 2004a, b;Vargas et al. 2006;. ...
... ng goldfish and cichlid fish show place-related increases in the firing rate (Canfield and Mizumori 2004), and Uceda et al. (2015) observed spatial-learning-related increases in metabolic activity in the goldfish ventral DLv. Furthermore, a series of experiments from the Seville group indicate that lesions of the entire DL (e.g., Durán et al. 2010;J. Vargas et al. 2006), or just to the DLv (Bingman et al. 2017), impair allocentric spatial learning in goldfish. DM lesions, on the other hand, have no effect on allocentric spatial learning (Durán et al. 2010;J. Vargas et al. 2006). ...
... ventral DLv. Furthermore, a series of experiments from the Seville group indicate that lesions of the entire DL (e.g., Durán et al. 2010;J. Vargas et al. 2006), or just to the DLv (Bingman et al. 2017), impair allocentric spatial learning in goldfish. DM lesions, on the other hand, have no effect on allocentric spatial learning (Durán et al. 2010;J. Vargas et al. 2006). ...
... These homologies led to the hypothesis that lesions of the DM or DL would have the same behavioral effects as lesions of the amygdala or hippocampus in mammals. Research generated primarily by researchers at the Universidad de Sevilla has largely supported this hypothesis (Portovella et al 2004a, b;Vargas et al. 2006;2012). ...
... ng goldfish and cichlid fish show place-related increases in the firing rate (Canfield and Mizumori 2004), and Uceda et al. (2015) observed spatial-learning-related increases in metabolic activity in the goldfish ventral DLv. Furthermore, a series of experiments from the Seville group indicate that lesions of the entire DL (e.g., Durán et al. 2010;J. Vargas et al. 2006), or just to the DLv (Bingman et al. 2017), impair allocentric spatial learning in goldfish. DM lesions, on the other hand, have no effect on allocentric spatial learning (Durán et al. 2010;J. Vargas et al. 2006). ...
... ventral DLv. Furthermore, a series of experiments from the Seville group indicate that lesions of the entire DL (e.g., Durán et al. 2010;J. Vargas et al. 2006), or just to the DLv (Bingman et al. 2017), impair allocentric spatial learning in goldfish. DM lesions, on the other hand, have no effect on allocentric spatial learning (Durán et al. 2010;J. Vargas et al. 2006). ...
Ray-finned fish are often excluded from the group of non-human animals
considered to have phenomenal consciousness. This is generally done on the grounds that the
fish pallium lacks a sufficiently expansive gross parcellation, as well as even minimally
sufficient neuronal organization, intrinsic connectivity, and reciprocal extrinsic connections
with the thalamus to support the subjective experience of qualia. It is also argued that fish do
not exhibit the level of behavioral flexibility indicative of consciousness. A review of
neuroanatomical, neurophysiological and behavioral studies is presented which leads to the
conclusion that fish do have neurobiological correlates and behavioral flexibility of sufficient
complexity to support the hypothesis that they are capable of phenomenal consciousness.
... Since blenniid females do not establish territories and explore larger areas than males in search for mates, one can hypothesize the occurrence of sex differences in brain regions involved in spatial memory was biased towards females. Studies in goldfish revealed that the dorsolateral ventral region of the telencephalon (DLv) is involved in the processing of spatial learning and mem- ory [Vargas et al., 2000; Portavella et al., 2002; Rodríguez et al., 2002; Vargas et al., 2006] and considered homologous to the hippocampus of amniotes [Bradford, 1995; Wullimann and Mueller, 2004; Northcutt, 2006 Northcutt, , 2008. Thus, it is expected that sex differences in spatial behavior in blennies should be paralleled by sex differences in the size of the ventral area of the dorsolateral telencepha- lon. ...
... In L. pholis , the dispersal seems to be more restricted in both sexes when compared to the rockpool blenny, but the different methods used to estimate home range sizes in these two species prevent a direct comparison of the estimates. The DLv in fish seems to be involved in spatial learning and memory in a similar manner to the role of the hippocampus in birds and mammals [Vargas et al., 2000; Portavella et al., 2002; Vargas et al., 2006]. The size of the telencephalon of African cichlids is known to be correlated with the spatial complexity of the habitat [van Staaden et al., 1995] and to the species mating system [Pollen et al., 2007] . ...
... Moreover, telencephalon ablation impairs spatial learning [Salas et al., 1996; López et al., 2000; Durán et al., 2008] and short-term memory retention [Ohnishi, 1997] in goldfish. More specifically, lateral pallium ablations selectively impair the encoding of geometric spatial information of environmental space [Rodríguez et al., 2002; Vargas et al., 2006]. Finally, learning of a spatial task in goldfish induces protein synthesis in dorsolateral telencephalic neurons but not in other areas of the telencephalon [Vargas et al., 2000]. ...
Blenniid fish exhibit a polygynandric mating system with parental care restricted to males. Nest-holder males defend a breeding territory centered on their nest, usually a crevice or hole in a rocky substrate, to which they attract females to spawn. Females, on the other hand, must search for nests in order to spawn and usually are the choosy sex, producing several sequential egg batches and broods during the breeding season. Therefore, male blennies are more site-attached than females. This situation offers an opportunity to investigate potential neural correlates of intraspecific differences in selective pressures for different spatial abilities in these species. Since the dorsolateral telencephalon has been considered a teleost homologue of the mammalian hippocampus, we predicted that the spatial abilities required for females to locate and return accurately to nests of males may have produced a sex difference in the size of the telencephalic nuclei involved in spatial abilities, biased towards females. To test this hypothesis, we assessed the home ranges and measured the size of the dorsolateral telencephalon of both sexes during the breeding season in two blenniid species, the shanny (Lipophrys pholis) and the Azorean rock-pool blenny (Parablennius parvicornis). We chose these two species because they differ in the degree of chemical communication they use, and this could also lead to differences in telencephalic areas. As predicted, in both species females present considerably larger home ranges paralleled by larger dorsolateral ventral telencephalic nuclei (DLv) than males. Other telencephalic nuclei that were measured did not show any sex difference in size. These results suggest that the DLv is involved in spatial abilities in blenniid fish and that sexual selection may be promoting this divergence as already described for mammals and birds.
... Several functions and structures of the vertebrate brain, especially the forebrain, appear to have been largely conserved throughout the evolution of vertebrate taxa (Vargas et al., 2006;Xie & Dorsky, 2017). For example, the mammalian and avian hippocampus, along with the homologous pallial areas of the reptile and fish brain share a central role in supporting and encoding spatial information (Rodríguez et al. 2002;Portavella et al., 2002). ...
... For example, the mammalian and avian hippocampus, along with the homologous pallial areas of the reptile and fish brain share a central role in supporting and encoding spatial information (Rodríguez et al. 2002;Portavella et al., 2002). Vargas et al. (2006) demonstrated that lesions to the lateral pallium in goldfish (Carassius auratus) can impair the encoding of geometric spatial information, comparable to the effect of lesions on the hippocampus in mammals and birds. Likewise, patterns of sleep also appear similar across taxonomic groups, including in fishes, such as the observation of characteristic sleep behaviours (e.g. ...
Sleep is a ubiquitous process that has been conserved in animals. Yet, our understanding of the functions of sleep largely derives from a few species. Sleep is considered to play an important role in mental processes, including learning and memory consolidation, but how widespread this relationship is across taxa remains unclear. Here, we test the impact of sleep disruption on the ability of the cleaner fish ( Labroides dimidiatus ) to both learn and remember a novel cognitive task. Sleep was disrupted by exposing a subset of fish to light at set intervals during the night. We found a significant negative relationship between sleep disruption and the ability to learn a novel task. Specifically, we found that fish in the light‐disturbed sleep treatment took significantly longer and made more incorrect decisions to find a food reward, compared with the undisturbed sleep treatment. All fish were then allowed a normal sleep schedule and retested several days later to assess their ability to remember the task. In contrast to the learning phase, we observed no significant differences between the two treatment groups in remembering the food reward several days later. Our results demonstrate a negative impact of sleep disruption on performance in a cognitive challenging task that appeared to have the strongest effect when fish were first exposed to the challenge. Importantly, we show that the association between sleep and mental processes, such as learning, may be widespread across vertebrate taxa and potentially have an early origin in the evolutionary history of vertebrate animals.
... Additionally, Uceda et al. (2015) and Ocaña et al. (2017) have observed spatial-learning-related increases in metabolic activity in the goldfish ventral DLv. A second source of evidence comes from reports that lesions of the entire DL (DURÁN et al., 2010;VARGAS et al., 2006), or just to the DLv (BINGMAN et al., 2017), impair allocentric spatial learning in goldfish. DM lesions, on the other hand, have no effect on allocentric spatial learning (DURÁN et al., 2010;VARGAS et al., 2006). ...
... A second source of evidence comes from reports that lesions of the entire DL (DURÁN et al., 2010;VARGAS et al., 2006), or just to the DLv (BINGMAN et al., 2017), impair allocentric spatial learning in goldfish. DM lesions, on the other hand, have no effect on allocentric spatial learning (DURÁN et al., 2010;VARGAS et al., 2006). ...
In this paper I argue that Velmens' reflexive model of perceptual consciousness is useful for understanding the first-person perspective and sentience in animals. I then offer a defense of the proposal that ray-finned bony fish have a first-person perspective and sentience. This defense has two prongs. The first prong is presence of a substantial body of evidence that the neuroanatomy of the fish brain exhibits basic organizational principles associated with consciousness in mammals. These principles include a relationship between a second-order sensory relay, the preglomerular complex, and the fish pallium which bears a resemblance to the relationship between the mammalian thalamus and the neocortex, the existence of feedback/feedforward and reentrant circuitry in the pallium, and structural and functional differences among divisions of the fish pallium. The second prong is the existence of behaviors in fish that exhibit significant flexibility in the presence of environmental change and require relational learning among stimuli distributed in space, over time, or both. I conclude that, although they are instantiated differently, a first-person perspective and sentience are present in fish. key words: Sentience. Fish. Behavior. Pallium. Reflexive monism.
... Convergent evidence in mammals [19], birds [20], amphibians [21] and fish [22] suggests that the hippocampal formation plays a crucial role in geometry representation. There are of course also species differences. ...
... Accordingly, in these species of fishes, the region considered homologous to the hippocampus is located laterally rather than medially in the telencephalon. Consistent with that, it has been found that goldfish with telencephalic lesions in the lateral pallium (but not in the medial pallium) appeared to be insensitive to geometric information [22]. ...
Evidence is discussed about the use of geometric information for spatial orientation and the association between space and numbers in non-human animals. A variety of vertebrate species can reorient using simple Euclidian geometry of the environmental surface layout, i.e. in accord with metric and sense (right/left) relationships among extended surfaces. There seems to be a primacy of geometric over non-geometric information in spatial reorientation and, possibly, innate encoding of the sense of direction. The hippocampal formation plays a key role in geometry-based reorientation in mammals, birds, amphibians and fish. Although some invertebrate species show similar behaviours, it is unclear whether the underlying mechanisms are the same as in vertebrates. As to the links between space and number representations, a disposition to associate numerical magnitudes onto a left-to-right-oriented mental number line appears to exist independently of socio-cultural factors, and can be observed in animals with very little numerical experience, such as newborn chicks and human infants. Such evidence supports a nativistic foundation of number–space association. Some speculation about the possible underlying mechanisms is provided together with consideration on the difficulties inherent to any comparison among species of different taxonomic groups.
This article is part of a discussion meeting issue ‘The origins of numerical abilities'.
... In addition, it has been demonstrated that, as in mammals and birds, hippocampal pallium lesions in goldfish produce severe performance impairments in a variety of spatial learning tasks requiring allocentric, relational spatial memory strategies, but not when the task can be solved by means of nonrelational, egocentric strategies or nonspatial discriminations [Rodríguez et al., 2002;Broglio et al., 2010;Durán et al., 2010]. These studies show that the functional similarity between the teleost fish hippocampal pallium homologue and the hippocampus of tetrapods is striking, because it supports place learning, allocentric or worldcentered navigation [Rodríguez et al., 1994[Rodríguez et al., , 2002Durán et al., 2010], encoding of multiple allothetic spatial cues in an integrated relational memory representation [Rodríguez et al., 1994[Rodríguez et al., , 2002Salas et al., 1996b;López et al., 1999López et al., , 2000aDurán et al., 2010], conjoint encoding of the geometrical and featural properties of the environmental surfaces [Vargas et al., 2004[Vargas et al., , 2006, abilities for spatial pattern completion after partial cueing [Rodríguez et al., 1994;López et al., 1999López et al., , 2000aDurán et al., 2010], fast spatial reversal learning [Salas et al., 1996b;López et al., 2000b;Broglio et al., 2010], the capability to infer spatial relationships between elements that have never been experienced together and the flexible expression of spatial knowledge in novel situations (e.g., readily finding the shortest route to a location from a new starting place) [Salas et al., 1996a, b;Rodríguez et al., 2002] or in vector mapping [Durán et al., 2010], and even the capability of binding temporally separate events that compose sequential memories [Portavella et al., 2004;Rodríguez-Expósito et al., 2017]. ...
... Fur-thermore, lesion studies showed that damage of the Dlv, but not of the Dld, impairs the performance of goldfish trained in the spatial constancy task , indicating that the Dlv is a crucial structure for map-like spatial memory. In fact, severe learning and memory deficits have been reported consistently after Dlv lesions in a variety of spatial memory tasks [Rodríguez et al., 2002;Vargas et al., 2006;Broglio et al., 2010;Durán et al., 2010]. ...
The teleost fish hippocampal pallium, like the hippocampus of tetrapods, is essential for relational map-like spatial memories. In mammals, these relational memories involve the dynamic interactions among different hippocampal subregions and between the hippocampus-neocortex network, which performs specialized operations such as memory encoding and retrieval. However, how the teleost hippocampal homologue operates to achieve comparably sophisticated spatial cognition capabilities is largely unknown. In the present study, the progressive changes in the metabolic activity of the pallial regions that have been proposed as possible homologues of the mammalian hippocampus were monitored in goldfish. Quantitative cytochrome oxidase histochemistry was used to measure the level of activation along the rostrocaudal axis of the ventral (Dlv) and dorsal parts of the dorsolateral division (Dld) and in the dorsoposterior division (Dp) of the goldfish telencephalic pallium throughout the time course of the learning process of a spatial memory task. The results revealed a significant increase in spatial memory-related metabolic activity in the Dlv, but not in the Dld, suggesting that the Dlv, but not the Dld, is comparable to the amniote hippocampus. Regarding the Dlv, the level of activation of the precommissural Dlv significantly increased at training onset but progressively declined to finally return to the basal pretraining level when the animals mastered the spatial task. In contrast, the commissural Dlv activation persisted even when the acquisition phase was completed and the animal's performance reached an asymptotic level. These results suggest that, like the dentate gyrus of mammals, the goldfish precommissural Dlv seems to respond nonlinearly to increments of change in sensory input, performing pattern separation under highly dissimilar input patterns. In addition, like the CA3 of mammals, the commissural Dlv likely operates in a continuum between two modes, a pattern separation or storage operation mode at early acquisition when the change in the sensory input is high, probably driven by the precommissural Dlv output, and a pattern completion or recall operation mode when the animals have mastered the task and the change in sensory input is small. Finally, an unexpected result of the present study is the persistent activation of the area Dp throughout the complete spatial task training period, which suggests that the Dp could be an important component of the pallial network involved in spatial memory in goldfish, and supports the hypothesis proposing that the Dp is a specialized part of the hippocampal pallium network.
... The importance of geometry is also interesting from a neural coding perspective because hippocampal formation lesions can eliminate or interfere with geometric learning (rats, McGregor et al. 2004;pigeons, Bingman et al. 2006;Nardi and Bingman 2007;Vargas et al. 2004b) while keeping feature memory for goal locations intact. Indeed, lesions to a likely hippocampal homologue of teleost fish can disrupt navigation by geometry under some experimental conditions (Vargas et al. 2006(Vargas et al. , 2011, but not others (Vargas et al. 2011). ...
... Interesting in this context is that hippocampal formation lesions also eliminate or interfere with geometric learning in a variety of vertebrate species (rats, McGregor et al. 2004;pigeons, Bingman et al. 2006;Nardi and Bingman 2007;Vargas et al. 2004b) while keeping feature memory for goal locations intact. Indeed, lesions to the presumptive hippocampal homologue of teleost fish can also disrupt navigation by geometry (Vargas et al. 2006; but see Vargas et al. 2011). As such, one would expect that the toad medial pallium, the homologue of the mammalian hippocampus, would also be important for the geometric learning reported in the current study. ...
Although of crucial importance in vertebrate evolution, amphibians are rarely considered in studies of comparative cognition. Using water as reward, we studied whether the terrestrial toad, Rhinella arenarum, is also capable of encoding geometric and feature information to navigate to a goal location. Experimental toads, partially dehydrated, were trained in either a white rectangular box (Geometry-only, Experiment 1) or in the same box with a removable colored panel (Geometry-Feature, Experiment 2) covering one wall. Four water containers were used, but only one (Geometry-Feature), or two in geometrically equivalent corners (Geometry-only), had water accessible to the trained animals. After learning to successfully locate the water reward, probe trials were carried out by changing the shape of the arena or the location of the feature cue. Probe tests revealed that, under the experimental conditions used, toads can use both geometry and feature to locate a goal location, but geometry is more potent as a navigational cue. The results generally agree with findings from other vertebrates and support the idea that at the behavioral-level geometric orientation is a conserved feature shared by all vertebrates.
... The lateral pallium in the brain telencephalon (Chapter 2) seems to play a critical role in the ability of fish to form mental maps. For example, the rate of protein synthesis is higher in the lateral pallium of goldfish after they have learned a spatial task (Vargas et al. 2000(Vargas et al. , 2006 and the ability to use spatial maps, but not to use landmarks, is impaired if the lateral pallium is destroyed (Rodriguez et al. 2002;Broglio et al. 2003;Vargas et al. 2006). ...
... The lateral pallium in the brain telencephalon (Chapter 2) seems to play a critical role in the ability of fish to form mental maps. For example, the rate of protein synthesis is higher in the lateral pallium of goldfish after they have learned a spatial task (Vargas et al. 2000(Vargas et al. , 2006 and the ability to use spatial maps, but not to use landmarks, is impaired if the lateral pallium is destroyed (Rodriguez et al. 2002;Broglio et al. 2003;Vargas et al. 2006). ...
The ways in which fish use space in nature are described, distinguishing between movements within a home range, dispersal and directed migration, as are the mechanisms that determine how fish use space. The external stimuli to which fish respond, how they use these cues to find their way around and the role of hormones in migration are also covered. An account is then given of how movement and orientation change with age, the evidence for inherited differences in these aspects of behaviour and environmental effects on development of space use patterns. The benefits that accrue to fish from moving in particular ways are described, as are adverse consequences of such movements, in the form of energetic costs and exposure to predators and pathogens. The ways in which benefits and costs are balanced against each other are discussed, with special reference to diurnal vertical migration. Although cultured fish usually inhabit confined spaces, their natural patterns of orientation and movement can cause a number of problems in aquaculture and some of these are described. Such problems are amenable to biological solutions and these are considered in the final section of this chapter, which also looks at the potential for using what is known about how fish move about to improve the effectiveness of general husbandry practices.
... Lesion and electrophysiological studies suggest that an important function of the rat hippocampus is the encoding of geometric information of the environment [5,6,15]. Moreover, the hippocampal formation of the birds [27,32] and the dorsolateral telencephalon of the goldfish [29] have been shown to play an important role in the use of geometry. Nevertheless, recent studies have proposed that the encoding of geometric information in enclosures is primarily supported by proximal cues or local views near the target location [16,26,33]. ...
... Previous studies suggest that lesion to the lateral pallium in goldfish [29] and to the hippocampal formation in rats [7,22,23] and pigeons [1,32] disrupt the performance of a previously acquired spatial task based on geometric information These results have been interpreted as that the hippocampus is essential for processing distance information that would be crucial in defining geometric relations. In this sense, geometric relationships between environmental cues have been proposed as the basis of map-like or cartographic representations of the environment [see 13]. ...
Recent studies have found that hippocampus of mammals and birds and the lateral pallium of the fish telencephalon are critical for learning the geometric properties of space. Nevertheless, other studies suggest that navigation based on geometric information is primarily supported by proximal cues near the target location. According to this hypothesis, animals could use a taxon strategy to navigate an environment where only geometric cues are available and the results from lesion studies could be masking other effects related to the use of featural information. In the present study, we examined the effects of lesions to the lateral pallium of goldfish in the encoding of geometric spatial information. Goldfish with telencephalic lesions were trained to search for a goal in a rectangular-shaped arena with either one or two possible goals. Lateral pallium lesions do not interfere with goal location when the geometric information defined the goal unambiguously. Present results suggest that the geometric information is sensitive to be encoded in taxon strategies and therefore it could not depend directly on the correct functioning of the hippocampal system.
... How are the equally striking decreases in TeO size observed over a similar timeframe related to changing visual and nonvisual processing, visuomotor function, and behavioral output (e.g., see Thompson et al. 2016;Pietri et al. 2017)? More specifically, such a detailed analysis could uncover insights into modifications in sensory processing related to spatial navigation and memory in Danionella and other fish species and vertebrates in general (Rodríguez et al. 2002;Portavella and Vargas 2005;Vargas et al. 2006;Yamamoto et al. 2007;Nieuwenhuys 2011;Giassi et al. 2012;Costa et al. 2011;Rajan et al. 2022;Lee and Briggman 2023;Zada et al. 2024). ...
Animals integrate information from different sensory modalities as they mature and perform increasingly complex behaviors. This may parallel differential investment in specific brain regions depending on the changing demands of sensory inputs. To investigate developmental changes in the volume of canonical sensory regions, we used third harmonic generation imaging for morphometric analysis of forebrain and midbrain regions from larval through juvenile and adult stages in Danionella dracula , a transparent, miniature teleost fish whose brain is optically accessible throughout its lifespan. Relative to whole‐brain volume, increased volume or investment in the telencephalon, a higher order sensory integration center, shows the most dramatic increases between 30–60 days postfertilization (dpf) and again at 90 dpf as animals reach adulthood. The torus longitudinalis (TL), a midbrain visuomotor integration center, also significantly increases between 60 and 90 dpf. In contrast, investment in the midbrain optic tectum (TeO), a retinal‐recipient target, progressively decreases from 30 to 90 dpf, whereas investment is relatively consistent across all stages for the midbrain torus semicircularis (TS), a secondary auditory and mechanosensory lateral line center, and the olfactory bulb (OB), a direct target of the olfactory epithelium. In sum, increased investment in higher‐order integration centers (telencephalon, TL) occurs as juveniles reach adulthood (60–90 dpf) and exhibit more complex cognitive tasks, whereas investment in modality‐dominant regions occurs earlier (TeO) or is relatively consistent across development (TS, OB). Complete optical access throughout Danionella ’s lifespan provides a unique opportunity to investigate how changing brain structure over development correlates with changes in connectivity, microcircuitry, or behavior.
... Then it was shown that lesions to the lateral pallium, but not the medial pallium, result in impairment of spatial memory in the goldfish Durán et al., 2010;Rodrıǵuez et al., 2002). Additional studies showed that goldfish with lateral pallium lesions learned tasks faster than sham or medial pallium lesion groups, yet were insensitive to geometrical information (Vargas et al., 2006). ...
... The inferred control of boundary navigation by MP suggested by that earlier study is now more directly supported by the MP-lesion results. The results are consistent with other studies carried out in different vertebrate groups highlighting the importance of the MP/hippocampus for geometry-based navigation (rats [35]; pigeons [37]; fish [40,41]), suggesting a conserved evolutionary origin perhaps as old as the transition to land and perhaps as old as earlier fish ancestors [4]. ...
The medial pallium (MP) of amphibians is the homologue of the mammalian hippocampus, and previous research has implicated MP for locating a using the boundary geometry of an environment. MP-lesioned, sham-operated and intact control terrestrial toads, Rhinella arenarum, were trained to locate a goal in a rectangular arena with a visual feature cue placed on one of the short walls. Whereas the sham-operated and intact subjects successfully learned to locate the goal, the MP-lesioned toads showed no evidence of learning. The data support the hypothesis that the amphibian MP is involved when the boundary geometry of an environment is used to locate a goal, which is consistent with evidence from other vertebrate groups. Curious, however, is that the MP lesions also resulted in the toads’ inability to locate the goal based on the visual feature cue. This result supports previous research and suggests that, in contrast to the hippocampal homologue of amniotes, the amphibian medial pallium plays a broader role in spatial learning processes.
... En cuanto a los resultados obtenidos en los estudios de actividad cerebral asociada al aprendizaje espacial, haciendo la evaluación tanto por la técnica de AgNOR como mediante la técnica de c-Fos, se ha observado que el Pallium Medial (i.e., la Formación Hipocampal de los anfibios) es la principal área telencefálica comprometida en la navegación espacial (Daneri, Casanave & Muzio, Inédito;Sotelo, Daneri, Bingman & Muzio, 2016). Estos resultados no son sorprendentes, ya que coinciden con las evidencias obtenidas en los otros grupos de vertebrados estudiados como peces, aves y mamíferos, en los que la Formación Hipocampal es la región cerebral que procesa la mayor parte de la información relacionada con la cognición espacial Mayer et al., 2016;Tommasi, Gagliardo, Andrew & Vallortigara, 2003;Tommasi, Chiandetti, Pecchia, Sovrano & Vallortigara, 2012;Vargas, López, Salas & inus-Blanc, 2004, Vargas, Bingman, Portavella, & López, 2006. ...
Amphibians are a phylogenetically very old group that is characterized by being the representatives of the transition from the aquatic to terrestrial environment, with all the implications that this could have on the organization of its nervous system. The use of this animal model to study the evolution of spatial cognition, offers the additional advantage, by not having neocortex, of being able to inquire about the basic brain circuits that underlie this kind of behavior. This paper describes the several procedures and experimental devices that are used for the study of spatial navigational and orientation abilities in amphibians and its neural bases. Taking into account all the information accumulated so far in this experimental model, it is concluded that the properties of this cognitive ability have been largely conserved throughout evolution.
... Since homologies between the hippocampus of mammals and the lateral pallium of teleosts have been established [70,71], together with a common organization of the basal ganglia [72], it is plausible that three-dimensional frameworks and features may be differently implemented in the brain of vertebrates (hippocampus versus striatum), including fishes. Furthermore, evidence in chicks [73,74] and fish [75] have highlighted the preferential engagement of the right hemisphere in the encoding of extended layouts during geometry-driven navigation by providing additional contribution to such a functional dissociation. ...
Simple Summary
Geometric navigation allows animals to efficiently move towards essential life-spaces by taking advantage of macrostructural information such as distance, angular magnitude, and length, in relation to left-right positional sense. In natural contexts, these cues can be referred to extensive three-dimensional surfaces such as a slope or a riverbed, thus becoming crucial to orient and find useful supplies. In controlled contexts, it is possible to set apart these components by handling the global shape of the experimental space (rectangular or square) as well, with the aim to specially probe the impact of each of them on navigation behavior of animals, including fishes. The present study aimed at investigating whether a well-known vertebrate, the zebrafish, could learn to encode and retain in memory such metric information (in terms of distances, corners, and lengths) in association with left–right directions, to gain rewards. Our results showed that zebrafish learned to use all these geometric attributes when repeatedly exposed to them, over a period of training, thereby giving strength to the ecological relevance of environmental geometry as a source of spatial knowledge. Generally, the engagement of zebrafish may consent to assess computations underlying large-scale-based navigation, also by drawing targeted comparisons, due to its behavioral, cognitive, and even emotional similarities with mammals.
Abstract
Zebrafish spontaneously use distance and directional relationships among three-dimensional extended surfaces to reorient within a rectangular arena. However, they fail to take advantage of either an array of freestanding corners or an array of unequal-length surfaces to search for a no-longer-present goal under a spontaneous cued memory procedure, being unable to use the information supplied by corners and length without some kind of rewarded training. The present study aimed to tease apart the geometric components characterizing a rectangular enclosure under a procedure recruiting the reference memory, thus training zebrafish in fragmented layouts that provided differences in surface distance, corners, and length. Results showed that fish, besides the distance, easily learned to use both corners and length if subjected to a rewarded exit task over time, suggesting that they can represent all the geometrically informative parts of a rectangular arena when consistently exposed to them. Altogether, these findings highlight crucially important issues apropos the employment of different behavioral protocols (spontaneous choice versus training over time) to assess spatial abilities of zebrafish, further paving the way to deepen the role of visual and nonvisual encodings of isolated geometric components in relation to macrostructural boundaries.
... In conclusion, the study highlighted an increase in egr-1 expression in the telencephalon of C. auratus while exploring a novel environment and when learning a new task. As already demonstrated in several other studies (Burgess et al. 2001;Vargas et al. 2004Vargas et al. , 2006, goldfish can encode both nongeometric and geometric information and encode the goal location using geometrical clues (Bingman and Mench 1990;Salas et al. 1996a, b;Durán et al. 2008). In conclusion, fish needed to encode new geometric information due to the introduction of the modified third gate (Rajan et al. 2011). ...
Over the last few decades, it has been shown that fish, comprising the largest group of vertebrates and in many respects one of the least well studied, possess many cognitive abilities comparable to those of birds and mammals. Despite a plethora of behavioural studies assessing cognition abilities and an abundance of neuroanatomical studies, only few studies have aimed to or in fact identified the neural substrates involved in the processing of cognitive information. In this review, an overview of the currently available studies addressing the joint research topics of cognitive behaviour and neuroscience in teleosts (and elasmobranchs wherever possible) is provided, primarily focusing on two fundamentally different but complementary approaches, i.e. ablation studies and Immediate Early Gene (IEG) analyses. More recently, the latter technique has become one of the most promising methods to visualize neuronal populations activated in specific brain areas, both during a variety of cognitive as well as non-cognition-related tasks. While IEG studies may be more elegant and potentially easier to conduct, only lesion studies can help researchers find out what information animals can learn or recall prior to and following ablation of a particular brain area.
... Like vertebrates, goldfish (Carassius auratus) are able to use distal landmarks to navigate and solve a spatial task spontaneously by encoding its spatial relationships with its context and remember its location again (Broglio et al., 2003;Sovrano et al., 2007;Vargas et al., 2006). The evolutionary and cognitive studies in teleosts states that the anatomical substrate in brain is responsible for cognition is the forebrain in particular, the telencephalon (Yamamoto, 2009). ...
Social defeat (SD) has been implicated in different modulatory effects of physiology and behaviour including learning and memory. We designed an experiment to test the functional role of monoamine oxidase (MAO) in regulation of synaptic transmission, synaptic plasticity and memory in goldfish Carassius auratus. To test this, individuals were divided into three groups: (i) control; (ii) social defeat (SD) group (individuals were subjected to social defeat for 10 min by Pseudotropheus demasoni) and (iii) SD + MAO inhibitor pre-treated group. All experimental groups were subjected to spatial learning and then memory. Our results suggest that SD affects a spatial learning and memory, whereas SD exerts no influence on MAOI pre-treated group. In addition, we noted that the expression of monoamine oxidase-A (MAO-A) was up-regulated and level of serotonin (5-hydroxytryptamine; 5-HT), expression of serotonin transporter (SERT), synaptophysin (SYP), synaptotagmin −1 (SYT-1), N-methyl-D-asparate (NMDA) receptors subunits (NR2A and NR2B), postsynaptic density-95 (PSD-95) and brain-derived neurotrophic factor (BDNF) were reduced by SD, while MAOIs pretreatment protects the effect of SD. Taken together, our results suggest that MAO is an essential component in the serotonergic system that finely tunes the level of 5-HT, which further regulates the molecules involving in synaptic transmission, synaptic plasticity and memory.
... map-like strategies) [29][30][31][32][33], specifically by damaging the lateral region of the telencephalic pallium [34][35][36]. A study by Vargas and colleagues [37] has further shown that lesions to this region severely impaired the geometry-based reorientation behavior of goldfish in a rectangular-shaped arena, leaving unaffected the use of featural cues. More recently, Rajan and colleagues [38] have demonstrated that active spatial learning in a rectangular-shaped arena induced the expression of immediate-early gene (IEG) early growth response 1 (egr-1) in telencephalon of goldfish, a regulatory transcription factor involved in neural plasticity and memory formation in mammals [for a review : 39]. ...
Disoriented animals and humans use both the environmental geometry and visual landmarks to guide their spatial behavior. Although there is a broad consensus on the use of environmental geometry across various species of vertebrates, the nature of disoriented landmark-use has been greatly debated in the field. In particular, the discrepancy in performance under spontaneous choice conditions (sometimes called “working memory” task) and training over time (“reference memory” task) has raised questions about the task-dependent dissociability of mechanisms underlying the use of landmarks. Until now, this issue has not been directly addressed, due to the inclusion of environmental geometry in most disoriented navigation paradigms. In the present study, therefore, we placed our focus on landmark-based navigation in fish (Xenotoca eiseni), an animal model that has provided fruitful research in spatial reorientation. We began with a test of spontaneous navigation by geometry and landmarks (Experiment 1), showing a preference for the correct corner, even in the absence of reinforced training. We then proceeded to test landmarks without the influence of informative geometry through the use of square environments (Experiment 2–4), varying the numerosity of present landmarks, the distance of landmarks from the target corner, and the type of task (i.e., spontaneous cued memory or reference memory). We found marked differences in landmark-use in the absence of environmental geometry. In the spontaneous memory task, visual landmarks acquired perceptive salience (and attracted the fish) but without serving as a spatial cue to location when they were distal from the target. Across learning in the reference memory task, the fish overcame these effects and gradually improved in their performance, although they were still biased to learn visual landmarks near the target (i.e., as beacons). We discuss these results in relation to the existing literature on dissociable mechanisms of spatial learning.
... Similar to other teleost, the telencephalon hemispheres of grass carp were positioned at the posterior of the olfactory bulb, and the anterior of the optic tectum (Vargas et al., 2006;Lucini et al., 2018). In mammals, numerous and complicated sulcus were widely distributed on the surface of the telencephalon (Bjarkam et al., 2017). ...
... data]). The importance of the anuran HF for spatial cognition in toads is consistent with findings in other vertebrate classes/species (fish and reptiles [Vargas et al., 2006;Ocaña, et al., 2017]; pigeons [Vargas et al., 2004;Bingman et al., 2006]; chicks [Mayer et al., 2016;Mayer et al., 2018]; rats [Pearce et al., 2004]; humans [Doeller et al., 2017]), indicating conserved function of HF in spatial navigation throughout vertebrate evolution [Bingman and Muzio, 2017]. ...
Acoustic communication is essential for reproduction and predator avoidance in many anuran species. For example, mating calls are generally produced by males and represent a conspicuous communication signal employed during the breeding season. Although anuran mating calls have been largely studied to analyze content and phonotaxis toward choruses, they are rarely discussed as sources of information guiding spatial behavior in broader contexts. This is striking if we consider that previous studies have shown anurans to be impressive navigators. In the current study, we investigated whether terrestrial toad (Rhinella arenarum) males can use a mating call as a spatial cue to locate a water reward in a laboratory maze. Male toads could indeed learn the location of a reward guided by a mating call. This navigational ability, as indicated by c-Fos, was associated with greater neuronal activity in the telencephalic hippocampal formation (HF; also referred to in amphibians as medial pallium), the medial septum (MS), and the central amygdala (CeA). HF and MS are telencephalic structures associated with spatial navigation in mammals and other vertebrates. The CeA, by contrast, has been studied in the context of acoustic processing and communication in other amphibian species. The results are discussed in the framework of an evolutionary conserved, HF-septal spatial-cognitive network shared by amphibians and mammals.
... Although several C. auratus studies explored the remarkable parallelism between central nervous system morphology and functional organization of fishes, mammals, and birds (16)(17)(18)(19)(20)(21)(22)(23), none of them investigated potential influences of environmental changes on learning and memory performances, and on telencephalic cell changes, using unbiased stereological methods. The present research addressed this question controlling for all other sources of potential confounding factors, including water temperature, pH, O 2 concentration, day-night cycle, noise level, and sex and number of individuals per volume of water in the aquarium. ...
Carassius auratus is a teleost fish that has been largely used in behavioral studies. However, little is known about potential environmental influences on its performance of learning and memory tasks. Here, we investigated this question in C. auratus, and searched for potential correlation between exercise and visuospatial enrichment with the total number of telencephalic glia and neurons. To that end, males and females were housed for 183 days in either an enriched (EE) or impoverished environment (IE) aquarium. EE contained toys, natural plants, and a 12-hour/day water stream for voluntary exercise, whereas the IE had none of the above. A third plus-maze aquarium was used for spatial and object recognition tests. Different visual clues in 2 of its 4 arms were used to guide fish to reach the criteria to complete the task. The test consisted of 30 sessions and was concluded when each animal performed three consecutive correct choices or seven alternated, each ten trials. Learning rates revealed significant differences between EE and IE fish. The optical fractionator was used to estimate the total number of telencephalic cells that were stained with cresyl violet. On average, the total number of cells in the subjects from EE was higher than those from subjects maintained in IE (P=0.0202). We suggest that environmental enrichment significantly influenced goldfish spatial learning and memory abilities, and this may be associated with an increase in the total number of telencephalic cells.
... Of most relevance to the present discussion are those in which brain lesions were used to investigate the potential dependency of a form of learning, most frequently spatial learning, on telencephalic structures. A common outcome following various types of localized telencephalic lesions was that an effective lesion impaired but did not eliminate the type of learning in question and that specific spatial tasks were differentially affected by lesion location (L opez et al. 2000;Rodriguez et al. 2002;Portavella and Vargas 2005;Saito and Watanabe 2006;Vargas et al. 2006). It is especially noteworthy that in studies where total telencephalon ablation was performed, the result was either a deficit, with preserved capacity to learn one type of spatial task, while the ability to learn another was unimpaired (L opez et al. 2000;Rodriguez et al. 2002) or, in contrast, no deficit at all (Dur an et al. 2008). ...
... Lesion techniques have been also used to study the ultrastructure of specific areas of the brains, such as the olfactory epithelium (Hansen et al., 1999). In the recent past, studies using the ablation of different areas of the goldfish brain have demonstrated the specific involvement of the different areas in more behavioural aspects, such as taste aversion learning (Martín et al., 2011), memory (Broglio et al., 2010, spatial and temporal cognition and learning (Durán et al., 2010;Portavella et al., 2002;Saito and Watanabe, 2006;Vargas et al., 2006), emotional and motor response conditioning Rodríguez et al., 2005), and the shoaling behaviour (Shinozuka and Watanabe, 2004). ...
Goldfish has been used as an unconventional model organism to study a number of biological processes. For example, goldfish is a well-characterized and widely used model in comparative endocrinology, especially in neuroendocrinology. Several decades of research has established and validated a number of tools to study hormones in goldfish. The detailed brain atlas of goldfish, together with the stereotaxic apparatus is an invaluable tool for the neuroanatomic localization and central administration of endocrine factors. In vitro techniques, such as organ and primary cell cultures, have been developed using goldfish. In vivo approaches using goldfish were used to measure endogenous hormonal milieu, feeding, behaviour and stress. While there are many benefits in using goldfish as a model organism in research, there are also challenges associated with it. One example is its tetraploid genome that results in the existence of multiple isoforms of endocrine factors. The presence of extra endogenous forms of peptides and its receptors adds further complexity to the already redundant multifactorial endocrine milieu. This review will attempt to discuss the importance of goldfish as a model organism in comparative endocrinology. It will highlight some of the merits and challenges in employing goldfish as an animal model for hormone research in the post-genomic era.
... Hippocampal formation lesions can also eliminate or interfere with geometric learning [rats, McGregor et al., 2004;pigeons Vargas et al., 2004b;Bingman et al., 2006;Nardi and Bingman, 2007] while keeping other forms of spatial learning intact. Indeed, lesions to the likely hippocampal homologue of teleost fish can disrupt navigation by geometry under some experimental conditions [Vargas et al., 2006[Vargas et al., , 2011, but not others [Vargas et al., 2011]. ...
Amphibians are central to discussions of vertebrate evolution because they represent the transition from aquatic to terrestrial life, a transition with profound consequences for the selective pressures shaping brain evolution. Spatial navigation is one class of behavior that has attracted the interest of comparative neurobiologists because of the relevance of the medial pallium/hippocampus, yet, surprisingly, in this regard amphibians have been sparsely investigated. In the current study, we trained toads to locate a water goal relying on the boundary geometry of a test environment (Geometry-Only) or boundary geometry coupled with a prominent, visual feature cue (Geometry-Feature). Once learning had been achieved, the animals were given one last training session and their telencephali were processed for c-Fos activation. Compared to control toads exposed to the test environment for the first time, geometry-only toads were found to have increased neuronal labeling in the medial pallium, the presumptive hippocampal homologue, while geometry-feature toads were found to have increased neuronal labeling in the medial, dorsal, and lateral pallia. The data indicate medial pallial participation in guiding navigation by environmental geometry and lateral, and to a lesser extent dorsal, pallial participation in guiding navigation by a prominent visual feature. As such, participation of the medial pallium/hippocampus in spatial cognition appears to be a conserved feature of terrestrial vertebrates even if their life history is still tied to water, a brain-behavior feature seemingly at least as ancient as the evolutionary transition to life on land.
... In a comparative context, what remains indisputable is that in every vertebrate class studied (mammals, e.g., Morris et al., 1982;birds, e.g., Colombo and Broadbent, 2000; reptiles, e.g., Rodriguez et al., 2002), the hippocmapus or presumptive hippocampus (Teleost Fish, e.g., Vargas et al., 2006) has been found to play some role in spatial cognition. However, although not universally embraced, it is now generally accepted that the functional role of the mammalian hippocampus, while perhaps ancestrally grounded to representations of space, is more broadly involved in episodic memory processes (Eichenbaum and Cohen, 2014). ...
For more than thirty years, a growing number of researchers have been attracted to the challenge of understanding the neurobiological organization of the avian hippocampal formation (HF) and its relationship to the remarkable spatial cognitive abilities of birds. In this selective review, we highlight recent anatomical and developmental findings that reveal a HF design that defies any simple comparison to the mammalian hippocampus and leaves unanswered the seemingly enduring question of whether a dentate gyrus homologue is to be found in HF. From a functional perspective, we highlight recent discoveries that implicate HF in the use of space for memory pattern segregation and continued interest in the role HF neurogenesis may play in supporting memory function and its relationship to memory decline in aging birds. We also summarize data that nurture a fundamental re-interpretation of the role of HF in spatial cognition by suggesting HF involvement in spatial perception antecedent to any memory formation. Given the disproportionate adaptive significance of space for birds, which has led to the evolution of their exceptional navigational and memory abilities, there is little doubt that the avian HF will continue to provide important and unexpected insights into the neural basis of spatial cognition. This article is protected by copyright. All rights reserved.
© 2015 Wiley Periodicals, Inc.
... The use of simple animal models that allow scientists to perform controlled-rearing studies may open the door to research linking specific genes (Osborne, 2006) and elderly-related spatial detriments to reorientation impairment (Fellini, Schachner & Morellini, 2006). Comparative research investigating the role of the hippocampus as a crucial area for representing space is long established (O'Keefe & Nadel, 1978); however, hippocampal involvement in the geometric module paradigm remains controversial (Burgess, 2008;Vargas, Bingman, Portavella & Lopez, 2006;Vargas, Petruso & Bingman, 2004;Bingman, Erichsen, Anderson, Good & Pearce, 2006). Different families of cells strictly related to specific spatial demands have been discovered in the parahippocampal circuit (place cells: O'Keefe & Dostrovsky, 1971; head direction cells: Taube, Muller & Ranck, 1990;grid cells: Fyhn, Molden, Witter, Moser & Moser, 2004), but we are still far from comprehending their exact role in coordinating navigation and orientation; future investigation will be required before resolving this issue. ...
Studies on human infants, focused on the ontogenetic origins of knowledge, have provided evidence for a small set of separable systems of core knowledge dealing with the representation of objects, number, and space. We investigated core knowledge systems from a comparative perspective, making use of the domestic chick as a model system, and filial im - printing as a key to animal mind. Here, we discuss evidence showing precocious abilities in the chick for representing: (i) the cardinal and ordinal/sequential aspects of numerical cognition, and (ii) the distance, angle, and sense relations among extended surfaces in the surrounding layout. Some of the abilities associated with core knowledge systems of number and space were observed in the absence of (or with very reduced) visual experience, supporting a nativistic account of the ori- gins of knowledge.
... Of most relevance to the present discussion are those in which brain lesions were used to investigate the potential dependency of a form of learning, most frequently spatial learning, on telencephalic structures. A common outcome following various types of localized telencephalic lesions was that an effective lesion impaired but did not eliminate the type of learning in question and that specific spatial tasks were differentially affected by lesion location (L opez et al. 2000;Rodriguez et al. 2002;Portavella and Vargas 2005;Saito and Watanabe 2006;Vargas et al. 2006). It is especially noteworthy that in studies where total telencephalon ablation was performed, the result was either a deficit, with preserved capacity to learn one type of spatial task, while the ability to learn another was unimpaired (L opez et al. 2000;Rodriguez et al. 2002) or, in contrast, no deficit at all (Dur an et al. 2008). ...
We review studies claiming that fish feel pain and find deficiencies in the methods used for pain identification, particularly for distinguishing unconscious detection of injurious stimuli (nociception) from conscious pain. Results were also frequently mis-interpreted and not replicable, so claims that fish feel pain remain unsubstantiated. Comparable problems exist in studies of invertebrates. In contrast, an extensive litera-ture involving surgeries with fishes shows normal feeding and activity immediately or soon after surgery. C fiber nociceptors, the most prevalent type in mammals and responsible for excruciating pain in humans, are rare in teleosts and absent in elas-mobranchs studied to date. A-delta nociceptors, not yet found in elasmobranchs, but relatively common in teleosts, likely serve rapid, less noxious injury signaling, trigger-ing escape and avoidance responses. Clearly, fishes have survived well without the full range of nociception typical of humans or other mammals, a circumstance according well with the absence of the specialized cortical regions necessary for pain in humans. We evaluate recent claims for consciousness in fishes, but find these claims lack adequate supporting evidence, neurological feasibility, or the likelihood that consciousness would be adaptive. Even if fishes were conscious, it is unwar-ranted to assume that they possess a human-like capacity for pain. Overall, the behavioral and neurobiological evidence reviewed shows fish responses to nociceptive stimuli are limited and fishes are unlikely to experience pain.
... The demonstration that paralyzed larval zebrafish navigate similarly to freely swimming animals suggests that it is possible to use this system to study neural mechanisms underlying many behaviors, including associative learning (Aizenberg and Schuman, 2011), two-dimensional motor adaptation (Ahrens et al., 2012), and possibly place-preference learning (Ofstad et al., 2011). In addition, neural representations of spatial features or the location of the animal in space (Vargas et al., 2006) may exist in the brain of the larval zebrafish. It is now possible to search for these throughout the brain of the larval zebrafish without any a priori bias for specific brain regions or nuclei. ...
A full understanding of nervous system function requires recording from large populations of neurons during naturalistic behaviors. Here we enable paralyzed larval zebrafish to fictively navigate two-dimensional virtual environments while we record optically from many neurons with two-photon imaging. Electrical recordings from motor nerves in the tail are decoded into intended forward swims and turns, which are used to update a virtual environment displayed underneath the fish. Several behavioral features-such as turning responses to whole-field motion and dark avoidance-are well-replicated in this virtual setting. We readily observed neuronal populations in the hindbrain with laterally selective responses that correlated with right or left optomotor behavior. We also observed neurons in the habenula, pallium, and midbrain with response properties specific to environmental features. Beyond single-cell correlations, the classification of network activity in such virtual settings promises to reveal principles of brainwide neural dynamics during behavior.
... Comparative research investigating the role of hippocampus as a crucial area for representing space is long dated (O'Keefe & Nadel, 1978); however, the hippocampal involvement in the geometric module task is controversial (Bingman, Erichsen, Anderson, Good, & Pearce, 2006;Burgess, 2008;Vargas, Bingman, Portavella, & Lopez, 2006;Vargas, Petruso, & Bingman, 2004). In the chick brain, we found evidence for a role of the hippocampal formation in placefinding tasks in which birds were required to find the centre of an enclosure (Tommasi et al., 2003). ...
Studies on the ontogenetic origins of human knowledge provide evidence for a small set of separable systems of core knowledge dealing with the representation of inanimate and animate objects, number, and geometry. Because core knowledge systems are evolutionarily ancient, they can be investigated from a comparative perspective, making use of various animal models. In this review, I discuss evidence showing precocious abilities in nonhuman species to represent (a) objects that move partly or fully out of view and their basic mechanical properties such as solidity, (b) the cardinal and ordinal/sequential aspects of numerical cognition and rudimentary arithmetic with small numerosities, and (c) the geometrical relationships among extended surfaces in the surrounding layout. Controlled rearing studies suggest that the abilities associated with core knowledge systems of objects, number, and geometry are observed in animals in the absence (or with very reduced) experience, supporting a nativistic foundation of such cognitive mechanisms. Animal models also promise a fresh approach to the issue of the neurobiological and genetic mechanisms underlying the expression of core knowledge systems.
... Environmental geometry would be represented in geocentric coordinates [26] through the activation of specific neuronal circuitries, hippocampal-and parahippocampaldependent (mammals [27][28][29]; birds [30,31]; fish [32]). By contrast, freestanding objects arranged in arrays would be used as local beacons within a frame of reference defined by global geometric information provided by extended surfaces. ...
The macroscopic, three-dimensional surface layout geometry of an enclosure apparently provides a different contribution for spatial reorientation than the geometric cues associated with freestanding objects arranged in arrays with similar geometric shape. Here, we showed that a unitary spatial representation can account for the capability of animals to reorient both by extended surfaces and discrete objects in a small-scale spatial task. We trained domestic chicks to locate a food-reward from an opening on isolated cylinders arranged either in a geometrically uninformative (square-shaped) or informative (rectangular-shaped) arrays. The arrays were located centrally within a rectangular-shaped enclosure. Chicks trained to access the reward from a fixed position of openings proved able to reorient according to the geometric cues specified by the shape of the enclosure in all conditions. Chicks trained in a fixed position of opening with geometric cues provided both by the arena and the array proved able to reorient according to each shape separately. However, chicks trained to access the reward from a variable position of openings failed to reorient. The results suggest that the physical constrains associated with the presence of obstacles in a scene, rather than their apparent visual extension, are crucial for spatial reorientation.
... Early studies also emphasized the ''instinctual behavior'' of fish, while numerous newer studies have shown that some fish species can exhibit emotional (Carpenter and Summers, 2009) and spatial learning (Rodríguez et al., 1994;L opez et al., 1999) as well as learning to make remarkably complicated perceptual (Siebeck et al., 2009) and social (van Bergen et al., 2004;Bshary and Grutter, 2006;Grosenick et al., 2007) judgments. Recent studies have also demonstrated that different divisions of the teleost dorsal telencephalon (pallium) are required for even simple spatial and emotional learning (Portavella et al., 2002;Salas et al., 2003;Broglio et al., 2005;Portavella and Vargas, 2005;Vargas et al., 2006), indicating that there may well be deeper functional similarities between the pallium of teleosts and amniotes. ...
The present article examines the anatomical organization of the dorsal telencephalon of two gymnotiform fish: Gymnotus sp. and Apteronotus leptorhynchus. These electric fish use elaborate electrical displays for agonistic and sexual communication. Our study emphasizes mainly pallial divisions: dorsolateral (DL), dorsodorsal (DD), and dorsocentral (DC), previously implicated in social learning dependent on electric signals. We found that the pallial cytoarchitectonics of gymnotiformes are similar to those reported for the commonly studied goldfish, except that DC is larger and better differentiated in gymnotiformes. We identified a new telencephalic region (Dx), located between DL and DC, and describe the morphological and some biochemical properties of its neurons. Most neurons in DL, DD, and DC are glutamatergic with spiny dendrites. However, the size of these cells as well as the orientation and extent of their dendrites vary systematically across these regions. In addition, both DD and DL contained numerous small GABAergic interneurons as well as well-developed GABAergic plexuses. One important and novel observation is that the dendrites of the spiny neurons within all three regions remain confined to their respective territories. We confirm that DL and DC express very high levels of NMDA receptor subunits as well as CaMKIIα, a key downstream effector of this receptor. In contrast, this enzyme is nearly absent in DD, while NMDA receptors are robustly expressed, suggesting different rules for synaptic plasticity across these regions. Remarkably, GABAergic pallial neurons do not express CaMKIIα, in agreement with previously reported results in the cortex of rats.
... According to the neuroanatomical analysis and on the basis of the electrophysiological responses, the telencephalic pallium of teleost fish contains a functional homolog of the mammalian hippocampus and amygdala (Braford 1995;Nieuwenhuys 1963). The telencephalic pallium of goldfish was reported to be involved in spatial (Emmanuvel Rajan et al. 2011;Watanabe 2004, 2006;Salas et al. 1996;Vargas et al. 2006Vargas et al. , 2011 and emotional learning and memory (Portavella et al. 2002(Portavella et al. , 2004Xu et al. 2003). Nam et al. (2004) have demonstrated that treatment with a high concentration of KCl could stimulate NMDA receptor-dependent LTP in the zebrafish telencephalon. ...
N-Methyl-D-aspartate (NMDA) receptors are implicated in a wide range of complex behavioral functions, including cognitive activity. Numerous studies have shown that using the repetitive administration of a noncompetitive NMDA receptor antagonist, MK-801, induces amnesia in rodents. In this study, the effect of a subchronic MK-801 treatment on the cognitive function of zebrafish was evaluated using a novel inhibitory avoidance task. First, we established a new system to investigate the inhibitory avoidance learning of zebrafish where they were trained to refrain from swimming from a shallow compartment to a deep compartment in order to avoid electric shock. Second, we found that blocking NMDA receptors by MK-801 could significantly attenuate the inhibitory avoidance behavior of the zebrafish and alter the telencephalic extracellular signal-regulated kinase (ERK) phosphorylation level 90 min after the inhibitory avoidance training. These results suggest that the formation of long-term emotional memory is possibly mediated by ERK activation in the telencephalon of zebrafish.
... In rock hind, AVTr expression was observed in the lateral zone of the dorsal telencephalon, subdivision 1 (Dld1) and a previously undescribed region designated subdivision 2 (Dld2). In goldfish, lesions in this area abolish geometric spatial learning in controlled experiments (Vargas et al., 2006). Both male and female rock hind are very territorial and make use of even small visual landmarks to designate territories (Kline et al., 2011). ...
This article provides an update on strategies and neural basis of spatial learning, paying special attention to amphibians. Analysis of learning strategies has proved that amphibians, as many other groups, are capable of spatial orientation using either a turn strategy (own body reference) or a guide strategy (use of a visual cue or beacon) and that distance between this visual cue and the reinforcer has an effect on the learning rate. Use of two or more visual cues (landmarks) was also evaluated in relation with what was initially called a “cognitive map”. Concerning neural bases, the role of the amphibian medial pallium (homologue area of mammalian hippocampus) was determined to be crucial for spatial orientation, but their complete functional equivalence is being questioned.
Animals integrate information from different sensory modalities as they mature and perform increasingly complex behaviors. This may parallel differential investment in specific brain regions depending on the demands of changing sensory inputs. To investigate developmental changes in the volume of canonical sensory integration brain regions, we used third harmonic generation imaging for morphometric analysis of forebrain and midbrain regions from 5 to 90 days post fertilization (dpf) in Danionella dracula, a transparent, miniature teleost fish whose brain is optically accessible throughout its lifespan. Relative to whole brain volume, increased volume or investment in telencephalon, a higher order sensory integration center, and torus longitudinalis (TL), a midbrain visuomotor integration center, is relatively consistent from 5 to 30 dpf, until it increases at 60 dpf, followed by another increase at 90 dpf, as animals reach adulthood. In contrast, investment in midbrain optic tectum (TeO), a retinal-recipient target, progressively decreases from 30-90 dpf, whereas investment is relatively consistent across all stages for the midbrain torus semicircularis (TS), a secondary auditory and mechanosensory lateral line center, and the olfactory bulb (OB), a direct target of the olfactory epithelium. In sum, increased investment in higher order integration centers (telencephalon, TL) occurs as juveniles reach adulthood and exhibit more complex cognitive tasks, whereas investment in modality-dominant regions occurs in earlier stages (TeO) or is relatively consistent across development (TS, OB). Complete optical access throughout Danionella lifespan provides a unique opportunity to investigate how changing brain structure over development correlates with changes in connectivity, microcircuitry, or behavior.
The ability to navigate the world is a critical cognitive skill that most animals use to find food, shelter, and mates. Understanding the neural basis of navigation requires probing how the brain encodes spatial information through the study of the activity of single neurons and neuronal populations. Classically in vertebrates, studies have centered on the rodent hippocampal formation, which led to the discovery of place, grid, head direction and other cell types. However, since navigation skills are essential to almost all vertebrates, spatial cognition in different species also needs to be explored. In recent years, as a result of advances in technology, new data have emerged on the ways in which space is represented during navigation in the brains of vertebrates other than rodents, including teleost fish, birds, and other mammal species. Here, we review the state of the art on the neural representation of an animal’s position and motion across vertebrates at the level of single neurons. We argue that it is time to pool information across vertebrates to identify the underlying algorithms that lead to successful navigation. Although rodent-based data are important, findings in rodents are unlikely to cover the full spectrum of neural computations supporting navigation strategies in the vertebrate kingdom. Studying other species can shed light on length scales such as in large environments, and different scenarios such as naturalistic environments that are hard to carry out in rodents. In addition, a rodent-centric view may neglect the fact that different species are likely to represent positions in the world in ways that do not exist in mammals. Finally, we provide an outlook for the future which includes prediction about findings in unexplored species, and the opportunities for discoveries and understanding in this field.
The ability to navigate the world is a critical cognitive skill that most animals use to find food, shelter, and mates. Understanding the neural basis of navigation requires probing how the brain encodes spatial information through the study of the activity of single neurons and neuronal populations. Classically in vertebrates, studies have centered on the rodent hippocampal formation, which led to the discovery of place, grid, head direction and other cell types. However, since navigation skills are essential to almost all vertebrates, spatial cognition in different species also needs to be explored. In recent years, as a result of advances in technology, new data have emerged on the ways in which space is represented during navigation in the brains of vertebrates other than rodents, including teleost fish, birds, and other mammal species. Here, we review the state of the art on the neural representation of an animal’s position and motion across vertebrates at the level of single neurons. We argue that it is time to pool information across vertebrates to identify the underlying algorithms that lead to successful navigation. Although rodent-based data are important, findings in rodents are unlikely to cover the full spectrum of neural computations supporting navigation strategies in the vertebrate kingdom. Studying other species can shed light on length scales such as in large environments, and different scenarios such as naturalistic environments that are hard to carry out in rodents. In addition, a rodent-centric view may neglect the fact that different species are likely to represent positions in the world in ways that do not exist in mammals. Finally, we provide an outlook for the future which includes prediction about findings in unexplored species, and the opportunities for discoveries and understanding in this field.
Evolution of Learning and Memory Mechanisms is an exploration of laboratory and field research on the many ways that evolution has influenced learning and memory processes, such as associative learning, social learning, and spatial, working, and episodic memory systems. This volume features research by both outstanding early-career scientists as well as familiar luminaries in the field. Learning and memory in a broad range of animals are explored, including numerous species of invertebrates (insects, worms, sea hares), as well as fish, amphibians, birds, rodents, bears, and human and nonhuman primates. Contributors discuss how the behavioral, cognitive, and neural mechanisms underlying learning and memory have been influenced by evolutionary pressures. They also draw connections between learning and memory and the specific selective factors that shaped their evolution. Evolution of Learning and Memory Mechanisms should be a valuable resource for those working in the areas of experimental and comparative psychology, comparative cognition, brain–behavior evolution, and animal behavior.
Evolution of Learning and Memory Mechanisms is an exploration of laboratory and field research on the many ways that evolution has influenced learning and memory processes, such as associative learning, social learning, and spatial, working, and episodic memory systems. This volume features research by both outstanding early-career scientists as well as familiar luminaries in the field. Learning and memory in a broad range of animals are explored, including numerous species of invertebrates (insects, worms, sea hares), as well as fish, amphibians, birds, rodents, bears, and human and nonhuman primates. Contributors discuss how the behavioral, cognitive, and neural mechanisms underlying learning and memory have been influenced by evolutionary pressures. They also draw connections between learning and memory and the specific selective factors that shaped their evolution. Evolution of Learning and Memory Mechanisms should be a valuable resource for those working in the areas of experimental and comparative psychology, comparative cognition, brain–behavior evolution, and animal behavior.
Like most animals, the survival of fish depends on navigation in space. This capacity has been documented in behavioral studies that have revealed navigation strategies. However, little is known about how freely swimming fish represent space and locomotion in the brain to enable successful navigation. Using a wireless neural recording system, we measured the activity of single neurons in the goldfish lateral pallium, a brain region known to be involved in spatial memory and navigation, while the fish swam freely in a two-dimensional water tank. We found that cells in the lateral pallium of the goldfish encode the edges of the environment, the fish head direction, the fish swimming speed, and the fish swimming velocity-vector. This study sheds light on how information related to navigation is represented in the brain of fish and addresses the fundamental question of the neural basis of navigation in this group of vertebrates.
Fish use spatial cognition based on allocentric cues to navigate, but little is known about how environmental enrichment (EE) affects learning and memory in correlation with hematological changes or gene expression in the fish brain. Here we investigated these questions in Colossoma macropomum (Teleostei). Fish were housed for 192 days in either EE or in an impoverished environment (IE) aquarium. EE contained toys, natural plants, and a 12-h/day water stream for voluntary exercise, whereas IE had no toys, plants, or water stream. A third plus maze aquarium was used for spatial and object recognition tests. Compared with IE, the EE fish showed greater learning rates, body length, and body weight. After behavioral tests, whole brain tissue was taken, stored in RNA-later, and then homogenized for DNA sequencing after conversion of isolated RNA. To compare read mapping and gene expression profiles across libraries for neurotranscriptome differential expression, we mapped back RNA-seq reads to the C. macropomum de novo assembled transcriptome. The results showed significant differential behavior, cell counts and gene expression in EE and IE individuals. As compared with IE, we found a greater number of cells in the telencephalon of individuals maintained in EE but no significant difference in the tectum opticum, suggesting differential plasticity in these areas. A total of 107,669 transcripts were found that ultimately yielded 64 differentially expressed transcripts between IE and EE brains. Another group of adult fish growing in aquaculture conditions were either subjected to exercise using running water flow or maintained sedentary. Flow cytometry analysis of peripheral blood showed a significantly higher density of lymphocytes, and platelets but no significant differences in erythrocytes and granulocytes. Thus, under the influence of contrasting environments, our findings showed differential changes at the behavioral, cellular, and molecular levels. We propose that the differential expression of selected transcripts, number of telencephalic cell counts, learning and memory performance, and selective hematological cell changes may be part of Teleostei adaptive physiological responses triggered by EE visuospatial and somatomotor stimulation. Our findings suggest abundant differential gene expression changes depending on environment and provide a basis for exploring gene regulation mechanisms under EE in C. macropomum.
Cognitive Evolution provides an in-depth exploration of the history and development of cognition, from the beginning of life on Earth to present-day humans. Drawing together evolutionary and comparative research, this book presents a unique perspective on the evolution of human cognition. Adopting an information processing perspective – that is, from inputs to outputs – with all the mental processes in between, Boles provides a systematic overview of the evolutionary development of
cognition and of its sensation, movement, and perception components.
The book is supported by long-established evolutionary theories and backed up by a wealth of recent research from the growing field of cognitive evolution and cognitive neuroscience to provide a comprehensive text on the subject.
Cognitive Evolution is an essential read for advanced undergraduates and postgraduate students of cognitive and evolutionary psychology.
David B. Boles is Emeritus Professor of Psychology, University of Alabama, Tuscaloosa.
[For more information, or to order, please see https://www.routledge.com/Cognitive-Evolution-1st-Edition/Boles/p/book/9780367028558.
A Facebook page for the book is at https://www.facebook.com/DavidBBoles/?modal=admin_todo_tour.]
Ethanol is one of the most widely consumed drugs in the world, and the effects of ethanol during early development include morphological and cognitive problems. The regulation of adenosine levels is essential for the proper function of major neurotransmitter systems in the brain, particularly glutamate and dopamine; thus, the investigation of the relation of adenosine and memory after early ethanol exposure becomes relevant. Embryos of zebrafish were exposed to 1% ethanol during two distinct developmental stages: gastrula/segmentation or pharyngula. The evaluation of memory, morphology, and locomotor parameters was performed when fish were 3 months old. The effect of ecto-5'-nucleotidase and adenosine deaminase inhibition on the consequences of ethanol exposure with regard to memory formation was observed. Morphological evaluation showed decreases in body length and the relative telencephalic and cerebellar areas in ethanol exposed animals. The locomotor parameters evaluated were not affected by ethanol. In the inhibitory avoidance paradigm, ethanol exposure during the gastrula/segmentation and pharyngula stages decreased zebrafish memory retention. When ethanol was given in the pharyngula stage, the inhibition of ecto-5'-nucleotidase in the acquisition phase of memory tests was able to revert the effects of ethanol on the memory of adults. These findings suggest that the increased adenosine levels caused by ethanol could alter the neuromodulation of important components of memory formation, such as neurotransmitters. The adjustment of adenosine levels through ecto-5'-nucleotidase inhibition appears to be effective at restoring normal adenosine levels and the acquisition of memory in animals exposed to ethanol during the pharyngula stage.
The hippocampus (named after its resemblance to the seahorse, from the Greek ἱππόκαμπος, "seahorse" from ἵππος hippos, "horse" and κάμπος kampos, "sea monster") is a major component of the brains of humans and other vertebrates. Humans and other mammals have two hippocampi, one in each side of the brain. It belongs to the limbic system and plays important roles in the consolidation of information from short-term memory to long-term memory and spatial memory that enables navigation. The hippocampus is located under the cerebral cortex;(allocortical) and in primates it is located in the medial temporal lobe, underneath the cortical surface. It contains two main interlocking parts: the hippocampus proper (also called Ammon's horn) and the dentate gyrus.
In Alzheimer's disease (and other forms of dementia), the hippocampus is one of the first regions of the brain to suffer damage; short-term memory loss and disorientation are included among the early symptoms. Damage to the hippocampus can also result from oxygen starvation (hypoxia), encephalitis, or medial temporal lobe epilepsy. People with extensive, bilateral hippocampal damage may experience anterograde amnesia (the inability to form and retain new memories).
In rodents as model organisms, the hippocampus has been studied extensively as part of a brain system responsible for spatial memory and navigation. Many neurons in the rat and mouse hippocampus respond as place cells: that is, they fire bursts of action potentials when the animal passes through a specific part of its environment. Hippocampal place cells interact extensively with head direction cells, whose activity acts as an inertial compass, and conjecturally with grid cells in the neighboring entorhinal cortex.
Since different neuronal cell types are neatly organized into layers in the hippocampus, it has frequently been used as a model system for studying neurophysiology. The form of neural plasticity known as long-term potentiation (LTP) was first discovered to occur in the hippocampus and has often been studied in this structure. LTP is widely believed to be one of the main neural mechanisms by which memories are stored in the brain.
Located in the dorsomedial forebrain of amphibians, reptiles, and birds is a structure recognized as homologous to the mammalian hippocampus. Comparing the hippocampus among nonmammalian tetrapods enables a hypothetical evolutionary reconstruction, according to which the hippocampus transitions from a small and relatively unorganized amphibian-like hippocampus, which receives direct sensory inputs from the thalamus and olfactory bulbs, to a laminated (reptiles) or partially laminated (birds) hippocampus that receives sensory inputs after some processing has already taken place in the telencephalon. Further, a hippocampal homologue is identifiable also in teleost fish. Functionally, what binds all the variation in hippocampal organization together is a shared role in the maplike representation of space.
Adult neural stem cells (aNSCs) are defined by their self-Renewal and multipotency, which allow them to generate both neurons and glial cells in the adult brain. Contrary to mammals, the zebrafish brain maintains numerous neurogenic zones in the adult, among which the most characterized is the pallial ventricular zone. It is composed of radial glial cells serving as aNSCs. Which embryonic neural progenitors are at the origin of these aNSCs is still unknown. This work aims to determine the relative contributions of two embryonic neural progenitor populations, the «proneural clusters» (involved in embryonic neurogenesis) and the « progenitor pools » (characterized by a delayed neurogenesis), to the formation of aNSCs in the zebrafish pallium. First, using genetic lineage tracing techniques, we were able to identify the embryonic neural progenitor population at the origin of a subpopulation of aNSCs located in the dorso-Medial part of the pallium. The her4:ERT2CreERT2 transgenic driver line, combined with pharmacological treatments inhibiting the Notch signalling pathway, allowed showing that neural progenitors giving rise to dorso-Medial pallial aNSCs express the « Enhancer of split » her4 gene, specifically expressed in « proneural clusters » from very early stages of development. As a second step, clonal analyses as well as spatially controlled recombinations by laser highlighted that aNSCs of the zebrafish lateral pallium do not derive from her4-Positive embryonic progenitors maintained by the Notch pathway, but from a restricted population of neuroepithelial cells located in the embryonic telencephalic roof plate. These cells display « progenitor pool » specific features, as for instance the expression of non-Canonical her genes (independent of Notch signalling) such as her6 and her9, the expression of components of signalling pathways such as Wnt, BMP, FGF, and a late neurogenesis onset. These progenitors progressively generate, from juvenile stages, the vast majority of the aNSCs of the lateral pallium. Most interestingly, a small population of these neuroepithelial cells persists in the postero-Lateral pallium at adult stage and keeps generating de novo aNSCs of this brain region. In addition to identifying the origin of pallial aNSCs in the zebrafish, this study also delivers information on the progressive maturation steps that embryonic progenitors undergo to generate aNSCs, and highlights similarities and differencies existing between the dorso-Medial and lateral progenitors. Finally, this work also permits tracing the neurons generated by stem cells at different stages. This reveals for the first time the progressive formation of the different zebrafish pallial compartements, and allows appreciating their homologies with the mouse pallial regions.
Little is known on the embryonic origin and related heterogeneity of adult neural stem cells (aNSCs). We use conditional genetic tracing, activated in a global or mosaic fashion by cell type-specific promoters or focal laser uncaging, coupled with gene expression analyses and Notch invalidations, to address this issue in the zebrafish adult telencephalon. We report that the germinal zone of the adult pallium originates from two distinct subtypes of embryonic progenitors and integrates two modes of aNSC formation. Dorsomedial aNSCs derive from the amplification of actively neurogenic radial glia of the embryonic telencephalon. On the contrary, the lateral aNSC population is formed by stepwise addition at the pallial edge from a discrete neuroepithelial progenitor pool of the posterior telencephalic roof, activated at postembryonic stages and persisting lifelong. This dual origin of the pallial germinal zone allows the temporally organized building of pallial territories as a patchwork of juxtaposed compartments.
The goldfish (Carassius auratus) is a widely studied vertebrate model organism for studying cell proliferation in the adult brain, and provide the experimental advantage of growing their body and brain throughout their ∼30-year life time. Cell proliferation occurs in the teleost brain in widespread proliferation zones. Increased cell proliferation in the brain has been linked to the actions of certain antidepressants, including tranylcypromine (TCP), which is used in the treatment of depression. We hypothesized that proliferation zones in the adult goldfish brain can be used to determine the antidepressant effects on cellular proliferation. Here, we report that bromodeoxyuridine (BrdU) labeling over a 24-hr period can be used to rapidly identify the proliferation zones throughout the goldfish brain, including the telencephalon, diencephalon, optic tectal lobes, cerebellum, and facial and vagal lobes. In the first 24 hr of BrdU administration, TCP caused an approximate and significant doubling of labeled cells in the combined brain regions examined, as detected by BrdU immunohistochemistry. TCP caused the greatest increase in cell proliferation in the cerebellum. The normal migratory paths of the proliferating cells within the cerebellum were not affected by TCP treatment. These results indicate that the goldfish provide significant advantages as a vertebrate model for rapidly investigating the effects of antidepressant drugs on cellular proliferation and migration in the normal and injured brain. Anat Rec, 2014. © 2014 Wiley Periodicals, Inc.
A review of selected works on spatial memory in animals and humans is presented, and some ideas about the encoding of geometry and its role in evolution are presented, based on recently accumulated evidence from psychology, ethology and the neurosciences. It is argued that comparative analyses at the level of both spatial navigation behaviors and their underlying neural mechanisms may provide a solid foundation for the biological origins of organisms' spontaneous ability in dealing with geometric concepts. To this aim, the representations of space underlying memory tasks involving discrete (i.e., landmark arrays) or continuous elements (i.e., enclosed environments) are evaluated and compared as regards the impact of their geometric arrangement.
This study examined the spatial strategies used by goldfish (Carassius auratus) to find a goal in a 4-arm maze and the involvement of the telencephalon in this spatial learning. Intact and telencephalon-ablated goldfish were trained to find food in an arm placed in a constant room location and signaled by a local visual cue (mixed place–cue procedure). Both groups learned the task, but they used different learning strategies. Telencephalon-ablated goldfish learned the task more quickly and made fewer errors to criterion than controls. Probe trials revealed that intact goldfish could use either a place or a cue strategy, whereas telencephalon-ablated goldfish learned only a cue strategy. The results offer additional evidence that place and cue learning in fish are subserved by different neural substrates and that the telencephalon of the teleost fish, or some unspecified structure within it, is important for spatial learning and memory in a manner similar to the hippocampus of mammals and birds.
Rhesus monkeys (Macaca mulata) were subjected to a place finding task in a rectangular room perfectly homogeneous and without distinctive featural information. Results of Experiment 1 show that monkeys rely on the large-scale geometry of the room to retrieve a food reward. Experiments 2 and 3 indicate that subjects use also nongeometric information (colored wall) to reorient. Data of Experiments 4 and 5 suggest that monkeys do not use small angular cues but that they are sensitive to the size of the cues (Experiments 6, 7, and 8). Our findings strengthen the idea that a mechanism based on the geometry of the environment is at work in several mammalian species. In addition, the present data offer new perspectives on spatial cognition in animals that are phylogenetically close to humans. Specifically, the joint use of both geometric and landmark-based cues by rhesus monkeys tends to demonstrate that spatial processing became more flexible with evolution.
Pigeons (
Columba livia) searched for hidden food in a rectangular environment constructed to eliminate external orientation cues. A feature group was initially trained with distinct features in each corner. A geometric group was initially trained with no featural information. Tests revealed that both groups encoded the geometry of the apparatus. The geometric group was then retrained with features, and a series of tests was administered to both groups. Transformation tests revealed that the groups differed in reliance on features versus geometry. Pigeons in the feature group followed the positive feature even when it was placed in a geometrically incorrect corner, whereas pigeons in the geometric group showed shared control by features and geometry. Both groups were able to use features in corners distant to the goal to orient themselves, and both groups relied more on the color than on the shape of the features. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
The extraordinary navigational ability of homing pigeons provides a unique spatial cognitive system to investigate how the brain is able to represent past experiences as memory. In this paper, we first summarize a large body of lesion data in an attempt to characterize the role of the avian hippocampal formation (HF) in homing. What emerges from this analysis is the critical importance of HF for the learning of map-like, spatial representations of environmental stimuli used for navigation. We then explore some interesting properties of the homing pigeon HF, using for discussion the notion that the homing pigeon HF likely displays some anatomical or physiological specialization(s), compared to the laboratory rat, that account for its participation in homing and the representation of large-scale, environmental space. Discussed are the internal connectivity among HF subdivisions, the occurrence of neurogenesis, the presence of rhythmic theta activity and the electrophysiological profile of HF neurons. Comparing the characteristics of the homing pigeon HF with the hippocampus of the laboratory rat, two opposing perspectives can be supported. On the one hand, one could emphasize the subtle differences in the properties of the homing pigeon HF as possible departure points for exploring how the homing pigeon HF may be adapted for homing and the representation of large-scale space. Alternatively, one could emphasize the similarities with the rat hippocampus and suggest that, if homing pigeons represent space in a way different from rats, then the neural specializations that would account for the difference must lie outside HF. Only future research will determine which of these two perspectives offers a better approximation of the truth.
Hippocampal place cells in the rat are so named because they fire predominantly within circumscribed regions of the environment. This study describes the positional firing properties of cells afferent to hippocampal place cells, in superficial layers of medial entorhinal cortex (MEC). MEC cells in these layers project to the hippocampus via the perforant path and, along with lateral entorhinal cells, are the sole route by which cortical information reaches the hippocampus. MEC cells were recorded from rats while they retrieved pellets in simple geometric enclosures. The behavioral task as well as procedures for data collection and analysis were the same used in previous studies on hippocampal place cells (e.g., Muller et al., 1987) in order to facilitate the direct comparison between hippocampal and entorhinal cells. The firing patterns of MEC cells show pronounced locational variations reminiscent of hippocampal firing fields, but with a lower signal-to-noise ratio. While noisy, MEC firing patterns are stationary in time as evidenced by their reproducibility, and the improvement in spatial signal with long-duration recordings. Furthermore, MEC firing patterns are not due to variations in the rat's behavior. Taken together, these data show that the positional firing variations in MEC cells are due to the location-specificity of MEC cells. These and additional data lead us to conclude that location-specific information exists prior to the hippocampus. MEC cells are similar to hippocampal place cells in that their firing can be controlled by the rotation of a visual cue (a white card attached to the wall), but is not disrupted by removing the cue. An important difference between hippocampal and entorhinal cells was seen when the shape of the recording chamber was changed. In the transition from a cylinder to an equal-area square of similar appearance, MEC firing patterns topologically transformed (or "stretched") while those of hippocampal place cells changed to an unpredictable pattern. We conclude that the positional firing of MEC cells is more "sensory bound" than hippocampal cells, and that the ability to discriminate different environments, while present in the hippocampus, is not yet present in its input from MEC.
Using the techniques set out in the preceding paper (Muller et al., 1987), we investigated the response of place cells to changes in the animal's environment. The standard apparatus used was a cylinder, 76 cm in diameter, with walls 51 cm high. The interior was uniformly gray except for a white cue card that ran the full height of the wall and occupied 100 degrees of arc. The floor of the apparatus presented no obstacles to the animal's motions. Each of these major features of the apparatus was varied while the others were held constant. One set of manipulations involved the cue card. Rotating the cue card produced equal rotations of the firing fields of single cells. Changing the width of the card did not affect the size, shape, or radial position of firing fields, although sometimes the field rotated to a modest extent. Removing the cue card altogether also left the size, shape, and radial positions of firing fields unchanged, but caused fields to rotate to unpredictable angular positions. The second set of manipulations dealt with the size and shape of the apparatus wall. When the standard (small) cylinder was scaled up in diameter and height by a factor of 2, the firing fields of 36% of the cells observed in both cylinders also scaled, in the sense that the field stayed at the same angular position and at the same relative radial position. Of the cells recorded in both cylinders, 52% showed very different firing patterns in one cylinder than in the other. The remaining 12% of the cells were virtually silent in both cylinders. Similar results were obtained when individual cells were recorded in both a small and a large rectangular enclosure. By contrast, when the apparatus floor plan was changed from circular to rectangular, the firing pattern of a cell in an apparatus of one shape could not be predicted from a knowledge of the firing pattern in the other shape. The final manipulations involved placing vertical barriers into the otherwise unobstructed floor of the small cylinder. When an opaque barrier was set up to bisect a previously recorded firing field, in almost all cases the firing field was nearly abolished. This was true even though the barrier occupied only a small fraction of the firing field area. A transparent barrier was effective as the opaque barrier in attenuating firing fields. The lead base used to anchor the vertical barriers did not affect place cell firing.(ABSTRACT TRUNCATED AT 400 WORDS)
Disoriented rats and non-human primates reorient themselves using geometrical features of the environment. In rats tested in environments with distinctive geometry, this ability is impervious to non-geometric information (such as colours and odours) marking important locations and used in other spatial tasks. Here we show that adults use both geometric and non-geometric information to reorient themselves, whereas young children, like mature rats, use only geometric information. These findings provide evidence that: (1) humans reorient in accord with the shape of the environment; (2) the young child's reorientation system is impervious to all but geometric information, even when non-geometric information is available and is re-presented by the child--such information should improve performance and is used in similar tasks by the oriented child; and (3) the limits of this process are overcome during human development.
This article provides a hierarchical model of animal spatial cognitive maps. Such maps include both topological information, which affords loose, yet operational, representations of the connectivity of space and its overall arrangement, and metric information, which provides information about angles and distances. The model holds that maps can be initially described as a set of location-dependent reference frameworks providing directional information about other locations. The addition of an overall directional reference allows for the buildup of more complete (allocentric) representations. A survey of recent neurobiological data provides some hints about the brain structures involved in these processes and suggests that the hippocampal formation and the posterior parietal cortex would act differently by handling topological and metric information, respectively.
The human hippocampus has been implicated in memory, in particular episodic or declarative memory. In rats, hippocampal lesions cause selective spatial deficits, and hippocampal complex spike cells (place cells) exhibit spatially localized firing, suggesting a role in spatial memory, although broader functions have also been suggested. Here we report the identification of the environmental features controlling the location and shape of the receptive fields (place fields) of the place cells. This was done by recording from the same cell in four rectangular boxes that differed solely in the length of one or both sides. Most of our results are explained by a model in which the place field is formed by the summation of gaussian tuning curves, each oriented perpendicular to a box wall and peaked at a fixed distance from it.
Rhesus monkeys (Macaca mulata) were subjected to a place finding task in a rectangular room perfectly homogeneous and without distinctive featural information. Results of Experiment 1 show that monkeys rely on the large-scale geometry of the room to retrieve a food reward. Experiments 2 and 3 indicate that subjects use also nongeometric information (colored wall) to reorient. Data of Experiments 4 and 5 suggest that monkeys do not use small angular cues but that they are sensitive to the size of the cues (Experiments 6, 7, and 8). Our findings strengthen the idea that a mechanism based on the geometry of the environment is at work in several mammalian species. In addition, the present data offer new perspectives on spatial cognition in animals that are phylogenetically close to humans. Specifically, the joint use of both geometric and landmark-based cues by rhesus monkeys tends to demonstrate that spatial processing became more flexible with evolution.
The hippocampus is widely believed to be involved in the storage or consolidation of long-term memories. Several reports have shown short-term changes in single hippocampal unit activity during memory and plasticity experiments, but there has been no experimental demonstration of long-term persistent changes in neuronal activity in any region except primary cortical areas. Here we report that, in rats repeatedly exposed to two differently shaped environments, the hippocampal-place-cell representations of those environments gradually and incrementally diverge; this divergence is specific to environmental shape, occurs independently of explicit reward, persists for periods of at least one month, and transfers to new enclosures of the same shape. These results indicate that place cells may be a neural substrate for long-term incidental learning, and demonstrate the long-term stability of an experience-dependent firing pattern in the hippocampal formation.
The hippocampus of mammals and birds is critical for spatial memory. Neuroanatomical evidence indicates that the medial cortex (MC) of reptiles and the lateral pallium (LP) of ray-finned fishes could be homologous to the hippocampus of mammals and birds. In this work, we studied the effects of lesions to the MC of turtles and to the LP of goldfish in spatial memory. Lesioned animals were trained in place, and cue maze tasks and crucial probe and transfer tests were performed. In experiment 1, MC-lesioned turtles in the place task failed to locate the goal during trials in which new start positions were used, whereas sham animals navigated directly to the goal independently of start location. In contrast, no deficit was observed in cue learning. In experiment 2, LP lesion produced a dramatic impairment in goldfish trained in the place task, whereas medial and dorsal pallium lesions did not decrease accuracy. In addition, none of these pallial lesions produced deficits in cue learning. These results indicate that lesions to the MC of turtles and to the LP of goldfish, like hippocampal lesions in mammals and birds, selectively impair map-like memory representations of the environmental space. Thus, the forebrain structures of reptiles and teleost fish neuroanatomically equivalent to the mammalian and avian hippocampus also share a central role in spatial cognition. Present results suggest that the presence of a hippocampus-dependent spatial memory system is a primitive feature of the vertebrate forebrain that has been conserved through evolution.
Goldfish (Carassius auratus) were trained in different place-finding tasks as a means of analyzing their ability to encode the geometric and the featural properties of the environment. Results showed that goldfish could encode and use both geometric and featural information to navigate. Goldfish trained in a maplike, or relational, procedure encoded both types of information in a single representation. In contrast, fish trained in a directly cued procedure developed 2 independent and competing strategies. These results suggest that the geometric properties of the spatial arrangement and discrete landmarks are sensitive to encoding in a maplike or relational system, whereas different sources of spatial information are encoded in a single and flexible representation of the environment.
Geometric information provided by the walls of an environment has a strong influence over hippocampal unit activity. This suggests that the hippocampus forms part of a cognitive mapping system that encodes geometric relationships between environmental cues and the animal's location. Here, the authors show for the first time that excitotoxic lesions of the hippocampus disrupt the ability of rats to navigate to a goal using shape information provided by a solid-walled arena and an array of identical landmarks. These results are consistent with cognitive mapping theories of hippocampal function and extend previous research by showing that hippocampal cell loss impairs navigation with respect to shape information provided by both physical barriers and an array of landmarks.
The class of bony fishes or Osteichthyes is usually subdivided into two subclasses, the Actinopterygii or ray-finned fishes and the Sarcopterygii or lobe-finned fishes. The subclass last mentioned, the telencephalon of which will be treated in the next chapter, can further be subdivided into the Dipnoi or lungfishes and the Crossopterygii or tassel-finned fishes. The Actinopterygii constitute by far the most abundant group of recent vertebrates. They are usually subdivided into three superorders, the Chondrostei, Holostei, and Teleostei. Interestingly, these three superorders may be considered as representing three subsequent stages or gradations of actinopterygian evolution. The Chondrostei are considered as descendants of the Palaeoniscoidei, a primitive group of paleozoic fishes. During the early and middle Mesozoic times, the Chondrostei were supplanted by the Holostei, which in turn were largely replaced in the last phase of the Mesozoic era and the Cenozoic era by the expanding and now-abundant Teleostei.
The Osteichthyes comprise at least three groups of bony fishes which are generally believed to share a common ancestor: the Crossopterygii, the Dipnoi, and the Actinopterygii. The intergroup relationships have long been disputed by paleontologists, and there is no consensus at the present time. It is usually argued either that the Crossopterygii and the Dipnoi are more closely related to one another than either is to the Actinopterygii (Romer, 1966; Gardiner, 1973) or that the three have been distinct groups since their earliest appearance (Schaeffer, 1969; Miles in Moy-Thomas, 1971). Jarvik (1968), however, has favored a closer affinity between the Crossopterygii and the Actinopterygii than between either of these groups and the Dipnoi.
A morphotype of the forebrain of gnathostomes, i.e. those characters that must have been present in the forebrain of ancestral gnathostomes, was generated by using out-group analysis to identify the shared primitive characters present in the forebrains of extant gnathostomes. The nature of morphotypes and the steps in generating a morphotype are described. Because hypotheses of phylogenetic relationships profoundly affect the resulting morphotype, current hypotheses of gnathostome interrelationships are reviewed, and particular attention is paid to the problematic relationships of lobe-finned fishes. Ontogenetic studies provide the most common basis for how neural characters are grouped, and a review of the developmental literature indicates that gnathostome forebrains are segmented, with the diencephalon arising from a rostral parencephalic neuromere, which subsequently forms anterior and posterior divisions, and a more caudal synencephalic neuromere. Unfortunately, there is no agreement concerning the number of segments that form the secondary prosencephalon (telencephalon and hypothalamus). For this reason, the characters of the secondary prosencephalon must be analyzed in a topological manner. An out-group analysis of the characters of the diencephalon of extant gnathostomes reveals that the diencephalon of ancestral gnathostomes must have arisen from three segments: an anterior parencephalic segment, which gave rise to intermediate, ventrolateral and ventromedial thalamic nuclei; a posterior parencephalic segment, which gave rise to dorsal and ventral habenular nuclei, anterior, dorsal posterior, dorsal central, and, possibly, lateral posterior thalamic nuclei, and posterior tubercular nuclei; a synencephalic segment, which gave rise to pretectal nuclei, accessory optic nuclei and the nucleus of the medial longitudinal fascicle. The pretectal and posterior tubercular regions of ray-finned fishes appear to be highly derived, due to extensive cellular proliferations that give rise to numerous nuclei. The secondary prosencephalon of ancestral gnathostomes was probably divided rostrally into inverted and evaginated cerebral hemispheres, with paired olfactory bulbs arising directly from the hemispheres, and caudally into preoptic and hypothalamic areas. The cerebral hemispheres likely comprised a dorsally situated pallium divided into medial, dorsal and lateral pallial formations, as well as an intercalated pallial nucleus situated ventrolateral to the lateral pallium, and a ventrally situated subpallium divided medially into septal nuclei and a medial amygdalar nucleus and laterally into a corpus striatum. Both pallial and subpallial centers of ancestral gnathostomes probably received ascending thalamic and posterior tubercular inputs, with telencephalic efferent pathways terminating primarily in the hypothalamus, posterior tubercle and midbrain tegmentum. An out-group analysis further indicates that some taxa in each gnathostome radiation exhibit highly derived telencephalic characters due to the independent expansion of one or more pallial formations.
There is considerable evidence that the hippocampal system contributes both to (1) the temporary maintenance of memories and to (2) the processing of a particular type of memory representation. The findings on amnesia suggest that these two distinguishing features of hippocampal memory processing are orthogonal. Together with anatomical and physiological data, the neuropsychological findings support a model of cortico-hippocampal interactions in which the temporal and representational properties of hippocampal memory processing are mediated separately. We propose that neocortical association areas maintain shortterm memories for specific items and events prior to hippocampal processing as well as providing the final repositories of long-term memory. The parahippocampal region supports intermediate-term storage of individual items, and the hippocampal formation itself mediates an organization of memories according to relevant relationships among items. Hippocampal-cortical interactions produce (i) strong and persistent memories for events, including their constituent elements and the relationships among them, and (ii) a capacity to express memories flexibly across a wide range of circumstances.
There is a considerable amount of evidence that mammals and birds can use different spatial learning strategies based on
multiple learning and memory systems. Unfortunately, only a few studies have investigated spatial learning and memory mechanisms
in other vertebrates. This study aimed to identify the strategies used by goldfish to solve two different spatial tasks in
a series of three experiments. In experiment 1, two groups of goldfish (Carassius auratus) were trained either in a spatial constancy task (SC), in which visual cues signalled the goal indirectly, or in a directly
cued task (DC) in which similar cues signalled the goal directly. Transfer tests were conducted to study the effects of discrete
cue deletion on the performance in both tasks. In these transfer tests the performance of the animals trained in the DC task
dropped to chance level when the cue that signalled the goal directly was removed. In contrast, the removal of any single
cue did not disrupt SC performance. In experiment 2, fish trained in the SC or the DC task were trained with the goal reversed.
Goldfish in the SC group needed fewer sessions to master the reversal task than DC animals. Finally, experiment 3 investigated
the effects of a substantial modification of the geometrical features of the apparatus on the performance of animals trained
in the SC or in the DC condition. The performance of DC goldfish was not affected, whereas the same change disrupted performance
in the SC animals despite the presence of the visual cues. These results suggest that there are separate spatial learning
and memory systems in fish. Whereas the DC animals used a typical guidance strategy, relying only on the cue that signalled
the goal directly, SC fish relied on a strategy with the properties of an actual spatial mapping system. Thus, the comparative
approach points to the generality of these learning strategies among vertebrates.
Most contemporary theories of memory are based on the assumption that memory can be divided into multiple psychological systems that are subserved by different neural substrates and that contribute to performance in a relatively independent manner. Although the study of individual memory systems has proved to be enormously useful, recent data increasingly point towards complex interactions between memory systems during performance of any given memory task. Three basic classes of interactions between different memory systems (competition, synergism and independence) are presented that appear to be congruent with the findings of many behavioral studies. Consideration of interactions among multiple memory systems will enhance our current understanding of memory by encouraging the view that memory systems are dynamic interactive units, rather than independent modules that act in isolation.
Place units in the dorsal hippocampus of the freely-moving rat signal the animal's position in an environment (place field). In the present experiments, thirty four place units were recorded in two different environments: one, a small platform where the rat had received neither training nor reward; the other, an elevated T-maze inside a set of black curtains where the rat had been trained on a place discrimination. The places within the curtained enclosure were specified by four cues (a light, a card, a fan, and a buzzer) in addition to the food. Other cues were eliminated by rotating the maze and the four controlled cues relative to the external world from trial-to-trial.
Some units had place fields in both environments while others only had a place field in one. No relationship could be seen between the place fields of units with fields in both environments.
All twelve units tested extensively in the controlled enclosure had place fields related to the controlled cues. Probe experiments in which only some of the controlled cues were available showed that some of these units were being excited by one or two cues while others were influenced in a more complex way. The fields of these latter units were maintained by any two of the 4 cues and were due to inhibitory influences which suppressed the unit firing over the rest of the maze.
A stereotaxic apparatus and technique for electrode placement in forebrain nuclei of the goldfish is described. An atlas of forebrain nuclei is given. Some new nuclear regions are described and the nomenclature of several nuclei is discussed.
Single unit activity was recorded from complex spike cells in the hippocampus of the rat while the animal was performing a spatial memory task. The task required the animal to choose the correct arm of a 4 arm plus-shaped maze in order to obtain reward. The location of the goal arm was varied from trial to trial and was identified by 6 controlled spatial cues which were distributed around the enclosure and which were rotated in step with the goal. On some trials these spatial cues were present throughout the trial (spatial reference memory trials) while on other trials they were present during the first part of the trial but were removed before the rat was allowed to choose the goal (spatial working memory trials). On these latter trials the animal had to remember the location of the cues and/or goal during the delay in order to choose correctly. 55 units were recorded during sufficient reference memory trials for the relationship between their firing pattern and different spatial aspects of the environment to be determined. 33 units had fields with significant relations to the controlled cues while 16 had significant relations to the static background cues, those cues in the environment which did not change position from trial to trial. Of 43 units which could be tested for their relation to the shape of the maze arms themselves, 15 showed such a relationship. Therefore the place units can be influenced by different aspects of the spatial environment but those related to the task requirement appear to be more potent. Interaction effects between the different spatial factors also influenced the firing pattern of some units. Of particular interest was the interaction between the controlled cues and the static background cues found in some cells since this might shed some light on how the hippocampus enables the rat to solve the memory task. 30 units with place fields related to the controlled cues were recorded during successful performance on spatial working memory trials as well as during spatial reference memory trials. The place fields of 90% of these units were maintained during the retention phase of the memory trials. During the recording of some units, other types of trial were given as well. On control trials, the cues were removed before the rat was placed on the maze. These trials provided controls for the potential influence of information left behind by the controlled cues and for the influence of the animal's behaviour on the unit activity.(ABSTRACT TRUNCATED AT 400 WORDS)
The place behaviors of intact rats, and of those receiving fornix lesions, were examined in the radial-arm maze. A cue-restricted environment was constructed wherein the location of arms with food rewards were identifiable only by their position in relation to an intermittently rotated 4-cue set. Food obtainment was measured during a procedure in which either 1, 2 or 3 of the cues were removed during a block of test sessions. Control animals demonstrated place navigation abilities robust to the deletion of any 1 or 2 cues. The performance of lesioned rats declined in a manner consistent with the number of absent stimuli. The results indicate that the behavioral expressions of place knowledge relate to the responsiveness of hippocampal place cells.
The central projections of the olfactory bulb were studied in Polypterus using the Nauta and Fink-Heimer techniques. Two major target areas were identified in the subpallium: the lateral subpallial nucleus and the dorsal and ventral entopeduncular nuclei. The connections are predominantly, if not exclusively, ipsilateral. In the pallium a massive ipsilateral projection to the superficial third of the medial pallium was demonstrated while the remainder of the pallium was found to be free of degeneration. Thus it appears that the pallium of Polypterus is not uniform throughout, as has been suggested in the literature. This contention is also supported by an analysis of the pallial cytoarchitecture. Because the pallium of Polypterus is everted, rather than inverted and evaginated, the topographically medial pallium is in topological correspondence with the lateral pallium of tetrapods. On the basis of this topological correspondence and the similarity of afference from the olfactory bulb, it is argued that the “medial” pallium of Polypterus is homologous to the pyriform pallium of tetrapods. The findings of this study are compared to those of similar studies in teleosts, which also have an everted pallium. An apparent conflict appears and suggestions for resolving it are offered.
White and McDonald (1993, Behav Brain Res 55:269-281) previously reported that animals with amygdala lesions failed to acquire a conditioned-cue preference (CCP) based on spatial cues, but that animals with fornix lesions exhibited larger CCPs of this type than normal animals. The present experiments focused on the hippocampal interference with amygdala-based CCP learning inferred from this finding. In experiment 1 we tested the hypothesis that this interference was due to the acquisition of information about the maze and its environment during a 10 min period of free exploration of the maze before the start of CCP training, hitherto given to all animals in these experiments. Normal animals that were not preexposed to the maze and animals that were preexposed to a similar maze in a different room both exhibited larger CCPs than animals that were preexposed to the same maze in the same room as CCP training and testing. This suggests that normal animals acquire context-specific information during the preexposure period and that this may be the cause of the hippocampus-based interference with the amygdala-mediated CCP. In experiment 2 we attempted to determine if the information thought to be acquired by the hippocampal memory system interferes with acquisition or expression of the CCP. As previously demonstrated, animals that received fornix lesions before preexposure (i.e., before the start of the experiment) exhibited larger than normal CCPs. Animals that received fornix lesions after preexposure but before CCP training and animals that received fornix lesions after CCP training but before testing both exhibited normal CCPs.(ABSTRACT TRUNCATED AT 250 WORDS)
The large body of evidence that supports the hypothesis that the dorsal cortex and dorsal ventricular ridge of non-mammalian (non-synapsid) amniotes form the dorsal pallium and are homologous as a set of specified populations of cells to respective sets of cells in mammalian isocortex is reviewed. Several recently taken positions that oppose this hypothesis are examined and found to lack a solid foundation. A cladistic analysis of multiple features of the dorsal pallium in amniotes was carried out in order to obtain a morphotype for the common ancestral stock of all living amniotes, i.e., a captorhinomorph amniote. A previous cladistic analysis of the dorsal thalamus (Butler, A.B., The evolution of the dorsal thalamus of jawed vertebrates, including mammals: cladistic analysis and a new hypothesis, Brain Res. Rev., 19 (1994) 29-65; this issue, previous article) found that two fundamental divisions of the dorsal thalamus can be recognized--termed the lemnothalamus in reference to predominant lemniscal sensory input and the collothalamus in reference to predominant input from the midbrain roof. These two divisions are both elaborated in amniotes in that their volume is increased and their nuclei are laterally migrated in comparison with anamniotes. The present cladistic analysis found that two corresponding, fundamental divisions of the dorsal pallium were present in captorhinomorph amniotes and were expanded relative to their condition in anamniotes. Both the lemnothalamic medial pallial division and the collothalamic lateral pallial division were subsequently further markedly expanded in the synapsid line leading to mammals, along with correlated expansions of the lemnothalamus and collothalamus. Only the collothalamic lateral pallial division--along with the collothalamus--was subsequently further markedly expanded in the non-synapsid amniote line that gave rise to diapsid reptiles, birds and turtles. In the synapsid line leading to mammals, an increase in the degree of radial organization of both divisions of the dorsal pallium also occurred, resulting in an 'outside-in' migration pattern during development. The lemnothalamic medial division of the dorsal pallium has two parts. The medial part forms the subicular, cingulate, prefrontal, sensorimotor, and related cortices in mammals and the medial part of the dorsal cortex in non-synapsid amniotes. The lateral part forms striate cortex in mammals and the lateral part of dorsal cortex (or pallial thickening or visual Wulst) in non-synapsid amniotes. Specific fields within the collothalamic lateral division of the dorsal pallium form the extrastriate, auditory, secondary somatosensory, and related cortices in mammals and the visual, auditory, somatosensory, and related areas of the dorsal ventricular ridge in non-synapsid amniotes.
A morphotype of the forebrain of gnathostomes, i.e. those characters that must have been present in the forebrain of ancestral gnathostomes, was generated by using out-group analysis to identify the shared primitive characters present in the forebrains of extant gnathostomes. The nature of morphotypes and the steps in generating a morphotype are described. Because hypotheses of phylogenetic relationships profoundly affect the resulting morphotype, current hypotheses of gnathostome interrelationships are reviewed, and particular attention is paid to the problematic relationships of lobe-finned fishes. Ontogenetic studies provide the most common basis for how neural characters are grouped, and a review of the developmental literature indicates that gnathostome forebrains are segmented, with the diencephalon arising from a rostral parencephalic neuromere, which subsequently forms anterior and posterior divisions, and a more caudal synencephalic neuromere. Unfortunately, there is no agreement concerning the number of segments that form the secondary prosencephalon (telencephalon and hypothalamus). For this reason, the characters of the secondary prosencephalon must be analyzed in a topological manner. An out-group analysis of the characters of the diencephalon of extant gnathostomes reveals that the diencephalon of ancestral gnathostomes must have arisen from three segments: an anterior parencephalic segment, which gave rise to intermediate, ventrolateral and ventromedial thalamic nuclei; a posterior parencephalic segment, which gave rise to dorsal and ventral habenular nuclei, anterior, dorsal posterior, dorsal central, and, possibly, lateral posterior thalamic nuclei, and posterior tubercular nuclei; a synencephalic segment, which gave rise to pretectal nuclei, accessory optic nuclei and the nucleus of the medial longitudinal fascicle. The pretectal and posterior tubercular regions of ray-finned fishes appear to be highly derived, due to extensive cellular proliferations that give rise to numerous nuclei. The secondary prosencephalon of ancestral gnathostomes was probably divided rostrally into inverted and evaginated cerebral hemispheres, with paired olfactory bulbs arising directly from the hemispheres, and caudally into preoptic and hypothalamic areas. The cerebral hemispheres likely comprised a dorsally situated pallium divided into medial, dorsal and lateral pallial formations, as well as an intercalated pallial nucleus situated ventrolateral to the lateral pallium, and a ventrally situated subpallium divided medially into septal nuclei and a medial amygdalar nucleus and laterally into a corpus striatum. Both pallial and subpallial centers of ancestral gnathostomes probably received ascending thalamic and posterior tubercular inputs, with telencephalic efferent pathways terminating primarily in the hypothalamus, posterior tubercle and midbrain tegmentum. An out-group analysis further indicates that some taxa in each gnathostome radiation exhibit highly derived telencephalic characters due to the independent expansion of one or more pallial formations.
The comparative interpretation of forebrain organization of the ray-finned fishes presents a number of challenges. The telencephalon develops by an eversion process, and much of its surface is ventricular rather than pial. A topological map of the ventricular surface shows that the area ventralis (presumed subpallium) is bordered dorsally by the dorsomedial (DM) zone of the area dorsalis, which is, in turn, bordered by the olfactory-recipient dorsoposterior (DP) zone of the area dorsalis. Within the diencephalon small dorsal and ventral thalami and a large group of migrated nuclei assigned to the posterior tuberculum (but of uncertain status) are present. Both the dorsal thalamus and the migrated nuclei of the posterior tuberculum project to the telencephalon. A review of the known connections of the four major zones of the area dorsalis together with their topological positions leads to the following tentative interpretations. Zone DP is homologous to the primary olfactory cortex. There is not enough information concerning the dorsodorsal zone (DD) to speculate on its comparative relationships. Zone DM is a limbic-like area lying between the subpallium and the olfactory pallium and is possibly homologous to the pallial amygdala. The dorsolateral zone (DL) displays a pattern of connectivity with the cerebellum and the optic tectum suggesting a possible homology with non-olfactory, non-limbic pallial areas. Caveats are raised concerning the above interpretations of DM and DL. One or both of them may have evolved independently of the telencephalic zones in tetrapods and may thus represent examples of homoplasy.
Fimbria-fornix-lesioned (FF) rats (n = 10) and control rats (n = 10) were trained for the food-searching task in a rectangular box with four kinds of featural panels. In Experiment 1, food was placed at the fixed corner in front of the fixed panel so that both geometrical information (the shape of the rectangular box) and featural information (panels at the corners) were available for the rat. Control rats could find the food, but they sometimes searched at the diagonal corner of the food. Food location and its diagonal location were equivalent in relation to the longer and shorter sides of the box. FF rats could find food, only when the featural panel that showed the location of food was in front of them. From Experiments 2A and 2B which controlled geometrical information and featural information respectively, it is indicated that control rats could use geometrical information and featural information independently, but that FF rats could use only featural information. These results suggest that the hippocampus plays an important role in processing geometrical information, but not featural information.
In order to study the role of hippocampus in spatial learning, fimbria-fornix (FF) lesioned and control rats, eight each, were trained for a distance discrimination task in a rectangular test box (120 x 60 x 35 cm). A rat was placed in a start box at one of the corners of the test box, and then released to choose the bottle that contained food reward. Two bottles, at the distance of 50 cm, were placed along the walls, one short and the other long, on either side of the start box, and to find the reward the rat had to discriminate the distance, i.e., short vs. long wall of the test box. Results showed that control rats were able to make the discrimination, while FF rats were not. The finding suggests that hippocampus plays an important role in processing distance information in general, and distance discrimination in particular.
Spatial learning and memory related morphological changes in the argyrophilic nucleolar organizer region (AgNOR) of telencephalic neurons in goldfish were quantitatively evaluated by means of AgNOR neurohistochemical stain. The AgNORs and nuclei of nerve cells of two different telencephalic regions of goldfish trained in a spatial task or submitted to a similar non-contingent behavioral procedure (control group) were morphometrically evaluated. Results show that the area of AgNORs in goldfish dorsolateral telencephalic neurons increased significantly in the spatial learning group but not in control group. This effect seems to be highly specific as it did not appear in the dorsolateral area of the control group neither in the dorsomedial area of both groups. As the size of AgNORs in the nerve cell nuclei reflect the level of transcriptive activity, these morphological changes could be revealing increased protein synthesis in goldfish dorsolateral telencephalic neurons related with learning and memory. These findings could contribute to determining the subregions of the teleost telencephalon implicated in spatial learning and could indicate that the AgNOR staining technique would be a useful tool in assesing learning and memory related neuronal activity.
The effects of hippocampal lesions on the processing and retention of visual and spatial information in birds and mammals is reviewed. Both birds and mammals with damage to the hippocampus are severely impaired on a variety of spatial tasks, such as navigation, maze learning, and the retention of spatial information. In contrast, both birds and mammals with damage to the hippocampus are not impaired on a variety of visual tasks, such as delayed matching-to-sample, concurrent discrimination, or retention of a visual discrimination. In addition, both birds and mammals with hippocampal damage display impairments in the acquisition of an autoshaped response, as well as alterations in response suppression. These findings suggest that the avian hippocampus is a functional homologue of the mammalian hippocampus, and that in both birds and mammals the hippocampus is important for the processing and retention of spatial, rather than purely visual information.
This study examined the spatial strategies used by goldfish (Carassius auratus) to find a goal in a 4-arm maze and the involvement of the telencephalon in this spatial learning. Intact and telencephalon-ablated goldfish were trained to find food in an arm placed in a constant room location and signaled by a local visual cue (mixed place-cue procedure). Both groups learned the task, but they used different learning strategies. Telencephalon-ablated goldfish learned the task more quickly and made fewer errors to criterion than controls. Probe trials revealed that intact goldfish could use either a place or a cue strategy, whereas telencephalon-ablated goldfish learned only a cue strategy. The results offer additional evidence that place and cue learning in fish are subserved by different neural substrates and that the telencephalon of the teleost fish, or some unspecified structure within it, is important for spatial learning and memory in a manner similar to the hippocampus of mammals and birds.
Analysis of vasculature in the telencephalic pallium of a teleost allows the considerable depth of the sulcus externus, which lies at the lateral extent of the ependymal attachment, to be appreciated. The depth of this sulcus is compelling evidence for a simple eversion process (an outfolding of the pallial wall of each hemisphere) during telencephalic development in all ray-finned fishes that is not complicated in teleosts by secondary migration of pallial cell groups. A simple eversion process is known to occur in some ray-finned fishes with relatively simple telencephalic cytoarchitecture but has been disputed in teleosts based on the pattern of olfactory tract projections. A resolution to the conflicting hypotheses of pallial relationships across ray-finned fishes and in comparison with other craniate radiations is presented here, based on a re-examination of hodological and histochemical data mandated by this sulcal anatomy.
Eight experiments tested the abilities of 3-4-year-old children to reorient themselves and locate a hidden object in an open circular space furnished with three or four landmark objects. Reorientation was tested by hiding a target object inside one of the landmarks, disorienting the child, observing the child's search for the target, and comparing the child's performance to otherwise similar trials in which the child remained oriented. On oriented trials, children located the target successfully in every experiment. On disoriented trials, in contrast, children failed to locate the object when the landmarks were indistinguishable from one another but formed a distinctive geometric configuration (a triangle with sides of unequal length or a rectangle). This finding provides evidence that the children failed to use the geometric configuration of objects to reorient themselves. As in past research, children also did not appear to reorient themselves in accord with non-geometric properties of the layout. In contrast to these findings, children successfully located the object in relation to a geometric configuration of walls. Moreover, adults, who were tested in two further experiments, located the object by using both geometric and non-geometric information. Together, these ten experiments provide evidence that early-developing navigational abilities depend on a mechanism that is sensitive to the shape of the permanent, extended surface layout, but that is not sensitive to geometric or non-geometric properties of objects in the layout.
In mammals, the pallial amygdala is implicated in emotional learning and memory, whereas the hippocampus is involved in spatial, contextual, or relational memory. This review presents a set of experiments aimed to study the involvement of the dorsomedial and dorsolateral telencephalon of goldfish in spatial and active avoidance learning. Results showed that (1) medial lesions impaired both acquisition and retention of conditioned avoidance response in two-way active avoidance learning experiments with stimuli overlapping (emotional factor) and with an interstimuli gap (temporal and emotional factors), and (2) the medial lesion did not affect spatial learning (spatial, contextual, or relational factors). In contrast, lateral lesions did not impair conditioned avoidance response with stimuli overlapping, but affected conditioned avoidance response with an interstimuli gap and spatial learning. These results support the presence of two differentiated memory systems in teleost fish based on discrete pallial regions: emotional (dorsomedial telencephalon) and spatial/temporal or relational (dorsolateral telencephalon). Furthermore, these functional data support the homology between the medial pallium of the teleost and the pallial amygdala of land vertebrates, and between the teleost lateral pallium and the mammalian hippocampus.
When disoriented in environments with distinctive geometry, such as a closed rectangular arena, human infants and adult rats reorient in accord with the large-scale shape of the environment, but not in accord with nongeometric properties such as the colour of a wall. Human adults, however, conjoined geometric and nongeometric information to reorient themselves, which has led to the suggestion that spatial processing tends to become more flexible over development and evolution. We here show that fish tested in the same tasks perform like human adults and surpass rats and human infants. These findings suggest that the ability to make use of geometry for spatial reorientation is an ancient evolutionary tract and that flexibility and accessibility to multiple sources of information to reorient in space is more a matter of ecological adaptations than phylogenetic distance from humans.
Previous studies have shown that disoriented children use the geometric features of the environment to reorient, but the results have not consistently demonstrated whether children can combine such information with landmark information. Results indicating that they cannot suggest the existence of a geometric module for reorientation. However results indicating that children can use geometric information in combination with landmark information challenge the modularity interpretation. An uncontrolled variable in the studies yielding conflicting results has been the size of the experimental space. In the present studies, which tested young children in spaces of two different sizes, the size of the space affected their ability to use available landmark information. In the small space, the children did not use the landmark to reorient, but in the large space they did. The ability of children to use landmarks in combination with geometric information raises important questions about the existence of an encapsulated geometric module.
Many comparative pieces of research support the hypothesis that the medial cortex region of the reptilian forebrain could be homologous to hippocampal formation. Besides, there is some evidence involving this structure in complex spatial learning in a similar manner to hippocampus of mammals and birds. In this experiment we examined effects of medial cortex lesion in reversal learning. Turtles were trained in a spatial and a non-spatial maze procedure and the reversal of these tasks. Data revealed that sham and medial cortex lesioned turtles of both procedures performed well on the initial learning (acquisition). However, during the reversal phase, only the turtles with medial cortex lesion showed impaired performance in the spatial procedure. These results suggest that turtles possess different spatial learning and memory systems in close parallel to those described in other vertebrates, and that medial cortex plays a crucial role in complex place learning.
Domestic chicks bilaterally or unilaterally lesioned to the hippocampus were trained to search for food hidden beneath sawdust by ground-scratching in the centre of a large enclosure, the correct position of food being indicated by a local landmark in the absence of any extra-enclosure visual cues. At test, the landmark was removed or displaced at a distance from its original position. Results showed that sham-operated chicks and chicks with a lesion of the left hippocampus searched in the centre, relying on large-scale geometric information provided by the enclosure, whereas chicks with a lesion of either the right hippocampus or both hippocampi were completely disoriented (landmark removed) or searched close to the landmark shifted from the centre (landmark displaced). These results indicate that encoding of geometric features of an enclosure occurs in the right hippocampus even when local information provided by a landmark would suffice to localize the goal; encoding based on local information, in contrast, seems to occur outside the hippocampus. These findings provide evidence that the left and right avian hippocampi play different roles in spatial cognition, a phenomenon which had been documented previously only for the human hippocampus.
In mammals and birds, hippocampal processing is crucial for allocentric spatial learning. In these vertebrate groups, lesions to the hippocampal formation produce selective impairments in spatial tasks that require the encoding of relationships among environmental features, but not in tasks that require the approach to a single cue or simple non-spatial discriminations. In reptiles, a great deal of anatomical evidence indicates that the medial cortex (MC) could be homologous to the hippocampus of mammals and birds; however, few studies have examined the functional role of this structure in relation to learning and memory processes. The aim of this work was to study how the MC lesions affect spatial strategies. Results of Experiment 1 showed that the MC lesion impaired the performance in animals pre-operatively trained in a place task, and although these animals were able to learn the same task after surgery, probe test revealed that learning strategies used by MC lesioned turtles were different to that observed in sham animals. Experiment 2 showed that the MC lesion did not impair the retention of the pre-operatively learned task when a single intramaze visual cue identified the goal. These results suggest that the reptilian MC and hippocampus of mammals and birds function in quite similar ways, not only in relation to those spatial functions that are impaired, but also in relation to those learning processes that are not affected.
A monoclonal antibody specific to apolipoprotein E 4 (apoE4) was applied immunohistochemically to archival human brain tissue. The examined 30 cases comprised four epsilon/epsilon4, 10 epsilon3/epsilon4, one epsilon2/epsilon4, 10 epsilon3/epsilon3 and five epsilon2/epsilon3 genotypes. The anti apoE4 antibody visualized senile plaques, neurofibrillary tangles and reactive astrocytes, as well as serum in the blood vessels and vascular smooth muscle cells in the cases of epsilon4. Moreover, the staining intensity was stronger in the cases carrying the epsilon4 homozygosity than in those cases of epsilon4 heterozygosity. Specific immunoreactivity was not obtained in those cases not carrying the epsilon4 allele. This method will allow in situ detection of apoE epsilon4 and contribute to studies of the effect of epsilon4 on Alzheimer's disease.
The antiepileptic effects of the organic calcium channel blocker verapamil were tested in non-drug-induced epileptiform activities. Low Mg2+ epileptic field potentials (EFP) were elicited in hippocampal slices of guinea pigs. Verapamil reduced frequency of occurrence and amplitude of EFP until EFP failed. The EFP reappeared if verapamil was withdrawn from low Mg2+ solution. Elevating the KCl concentration from 4 to 8 mM resulted in shortening of the latency of EFP abolition by verapamil and prolongation of the depressive effects of verapamil following its withdrawal. The findings indicate that transmembraneous calcium fluxes play also an essential role in low Mg(2+)-induced epileptiform activities.
The geometric properties of bounded space have attracted considerable attention as a source of spatial information that can guide goal navigation. Although the use of geometric information to navigate has been observed in every species studied to date, the neural mechanisms that support the representation of geometric information are still debated. With the purpose of investigating this topic, we trained pigeons with lesion to the hippocampal formation to search for food in a rectangular-shaped arena containing one wall of a different color that served as the only distinctive environmental feature. Although lesioned pigeons learned the task even faster than control animals, probe trials showed that they were insensitive to geometric information. Control animals could encode and use both geometric and feature information to locate the goal. By contrast, lesioned pigeons relied exclusively on the feature information provided by the wall of a different color. The results indicate that the avian hippocampal formation is critical for learning the geometric properties of space in homing pigeons.