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Abstract

Untrained Octopus vulgaris (observers) were allowed to watch conditioned Octopus(demonstrators) perform the task of selecting one of two objects that were presented simultaneously and differed only in color. After being placed in isolation, the observers, in a similar test, consistently selected the same object as did the demonstrators. This learning by observation occurred irrespective of the object chosen by the demonstrators as the positive choice and was more rapid than the learning that occurred during the conditioning of animals. The task was performed correctly without significant errors and further conditioning for 5 days. These results show that observational learning can occur in invertebrates.
... Following from such compelling anecdotal accounts, experimental trials have provided proof of such sophisticated capabilities in cephalopods. Among the most notable findings are: the recognition of human faces and individuals (Boal, 2006;Tricarico et al., 2011Tricarico et al., , 2014, play (Mather and Anderson, 1999;Kuba et al., 2003Kuba et al., , 2006, 'personality' (Mather and Anderson, 1993;Borrelli, 2007;Borrelli and Fiorito, 2008;Sinn et al., 2008Sinn et al., , 2010Borrelli et al., 2020;O'Brien et al., 2021), social learning (Fiorito and Scotto, 1992;Fiorito, 1993;Fiorito and Chichery, 1995;Amodio and Fiorito, 2013;Huang and Chiao, 2013;Tomita and Aoki, 2014), episodic memory (e.g., Pronk et al., 2010;Jozet-Alves et al., 2013;Schnell et al., 2021b), and deliberate and projective tool use within a specific octopus population (Finn et al., 2009), among others. ...
... Nevertheless, most species of cephalopods have historically been considered asocial animals in the sense that they don't establish or maintain familial relationships and are relatively short-lived (in contrast to the social mammals). Still, this overarching generalization has often been contradicted by both observation and experimental studies (Fiorito and Scotto, 1992;Fiorito, 1993;Huang and Chiao, 2013;Tomita and Aoki, 2014) as well as recent accounts (e.g., Godfrey-Smith and Lawrence, 2012;Amodio and Fiorito, 2013;Guerra et al., 2014;Scheel et al., 2016). ...
... The foregoing prompts some important questions. As a largely asocial animal, why would the octopus have developed the capacity to learn from conspecifics (Fiorito and Scotto, 1992)? Why would a specific population of octopuses travel a fairly significant distance in order to procure coconuts to use as nests (Finn et al., 2009)? ...
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It is only in recent decades that subjective experience - or consciousness - has become a legitimate object of scientific inquiry. As such, it represents perhaps the greatest challenge facing neuroscience today. Subsumed within this challenge is the study of subjective experience in non-human animals: a particularly difficult endeavor that becomes even more so, as one crosses the great evolutionary divide between vertebrate and invertebrate phyla. Here, we explore the possibility of consciousness in one group of invertebrates: cephalopod molluscs. We believe such a review is timely, particularly considering cephalopods' impressive learning and memory abilities, rich behavioral repertoire, and the relative complexity of their nervous systems and sensory capabilities. Indeed, in some cephalopods, these abilities are so sophisticated that they are comparable to those of some higher vertebrates. Following the criteria and framework outlined for the identification of hallmarks of consciousness in non-mammalian species, here we propose that cephalopods - particularly the octopus - provide a unique test case among invertebrates for examining the properties and conditions that, at the very least, afford a basal faculty of consciousness. These include, among others: (i) discriminatory and anticipatory behaviors indicating a strong link between perception and memory recall; (ii) the presence of neural substrates representing functional analogs of thalamus and cortex; (iii) the neurophysiological dynamics resembling the functional signatures of conscious states in mammals. We highlight the current lack of evidence as well as potentially informative areas that warrant further investigation to support the view expressed here. Finally, we identify future research directions for the study of consciousness in these tantalizing animals.
... (Roth, 2015). As with bees, there is debate as to whether squids have a "mental map" (Roth, 2015) and the extent to which they are capable of "learning by observation" (Fiorito & Chichery, 1995;Fiorito & Scotto, 1992;Roth, 2015). ...
... As in Table 1 One property of vertebrate brains is that they can grow new neurons, even in adulthood (Lindsey and Tropepe, 2006;Lemaire et al., 2012). Among the invertebrates, the cephalopod mollusks, specifically octopi and cuttlefish appear to be the most intelligent (Fiorito and Scotto, 1992;Godfrey-Smith, 2013). The cognitive abilities of cephalopods resemble those of vertebrates, as reviewed by Schnell and Clayton (2021). ...
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Microtubules, are formed of the protein tubulin, which is a heterodimer of α- and β-tubulin subunits. Both α- and β-tubulin exist as numerous isotypes, differing in amino acid sequence and tissue distribution. Among the vertebrate β isotypes, βIII has a very narrow distribution, being found primarily in neurons and in advanced cancers. The places in the amino acid sequence where βIII differs from the other β isotypes are highly conserved in evolution. βIII appears to be highly resistant to reactive oxygen species and it forms highly dynamic microtubules. The first property would be very useful in neurons, which have high concentrations of free radicals, and the high dynamicity would aid neurite outgrowth. The same properties make βIII useful in cancers. Examination of the amino acid sequences indicates a cysteine cluster at positions 124–129 in βIII (CXXCXC). This occurs in all βIII isotypes but not in βI, βII, or βIV. βIII also lacks the easily oxidized C239. Both features could play roles in free radical resistance. Many aggressive tumors over-express βIII. However, a recent study of breast cancer patients showed that many of them mutated their βI, βII, and βIV at particular places to change the residues to those found at the corresponding sites in βIII; these are all sites that are highly conserved in vertebrate βIII. It is possible that these residues are important, not only in the resistance to free radicals, but also in the high dynamicity of βIII. The cephalopod mollusks are well known to be highly intelligent and can remodel their own brains. Interestingly, several cephalopods contain the cysteine cluster as well as up to 7 of the 17 residues that are highly conserved in vertebrate βIII, but are not found in βI, βII, or βIV. In short, it is possible that we are looking at a case of convergent evolution, that a βIII-like isotype may be required for neuronal growth and function and that a structure-function study of the particular residues conserved between vertebrate βIII and cephalopod tubulin isotypes could greatly increase our understanding of the role of the various tubulin isotypes in neuronal growth and function and could aid in the development of novel anti-tumor drugs.
... Cephalopods are critical reference species in neuroscience, with multiple examples of genomic and neuronal innovations and convergent evolution (Albertin et al., 2012;Striedter et al., 2014;Yoshida et al., 2015;Nesher et al., 2020;Turchetti-Maia et al., 2017;Albertin et al., 2015: Liscovitch-Brauer et al., 2017. Octopuses are known for their highly flexible behavior, which relies on various forms of associative learning, including observational learning Amodio & Fiorito, 2013;Boal, 1996;Boycott, 1954;Fiorito & Scotto, 1992;Hanlon & Messenger, 2018;Mackintosh, 1965;Maldonado, 1963;Maldonado, 1965;Moriyama & Gunji, 1997;Papini & Bitterman, 1991;Sutherland, 1959;Wells, 1978). Their behavioral flexibility also includes solving the problems of complex motor tasks through learning strategy (Fiorito et al., 1990;Gutnick et al., 2011;Gutnick et al., 2020;Richter et al., 2015;Richter et al., 2016see review Nesher et al., 2020 Behavioral lesion and stimulation studies have implicated the vertical lobe (VL, Figure 1) as a major part of the octopus learning system (Boycott, 1961;Boycott & Young, 1958;Fiorito & Chichery, 1995;Graindorge et al., 2006;Shomrat et al., 2008). ...
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The vertical lobe (VL) in the octopus brain plays an essential role in its sophisticated learning and memory. Early anatomical studies suggested that the VL is organized in a "fan-out fan-in" connectivity matrix comprising only three morphologically identified neuron types; input axons from the median superior frontal lobe (MSFL) innervating en passant millions of small amacrine interneurons (AMs), which converge sharply onto large VL output neurons (LNs). Recent physiological studies confirmed the feedforward excitatory connectivity; a glutamatergic synapse at the first MSFL-to-AM synaptic layer and a cholinergic AM-to-LNs synapse. MSFL-to-AMs synapses show a robust hippocampal-like activity-dependent long-term potentiation (LTP) of transmitter release. 5-HT, octopamine, dopamine and nitric oxide modulate short- and long-term VL synaptic plasticity. Here, we present a comprehensive histolabeling study to better characterize the neural elements in the VL. We generally confirmed glutamatergic MSFLs and cholinergic AMs. Intense labeling for NOS activity in the AMs neurites were in-line with the NO-dependent presynaptic LTP mechanism at the MSFL-to-AM synapse. New discoveries here reveal more heterogeneity of the VL neurons than previously thought. GABAergic AMs suggest a subpopulation of inhibitory interneurons in the first input layer. Clear GABA labeling in the cell bodies of LNs supported an inhibitory VL output, yet the LNs co-expressed FMRFamide-like neuropeptides, suggesting an additional neuromodulatory role of the VL output. Furthermore, a group of LNs was glutamatergic. A new cluster of cells organized as a "deep nucleus" showed rich catecholaminergic labeling and may play a role in intrinsic neuromodulation. In-situ hybridization and immunolabeling allowed characterization and localization of a rich array of neuropeptides and neuromodulators, likely involved in reward/punishment signals. This analysis of the fast transmission system, together with the newly found cellular elements, help integrate behavioral, physiological, pharmacological and connectome findings into a more comprehensive understanding of an efficient learning and memory network.
... Right after the training phase octopuses choose the correct ball in 85% of all trails. The result remains approximately the same (81%) even 5 days after training [16], [18]. ...
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Octopus is an invertebrate belonging to the class of Cephalopoda. The body of an Octopus lacks any morphological joints and rigid parts. Their arms, skin and the complex nervous system are investigated by a several researchers all over the world. Octopuses are the object of inspiration for my scientists in different areas, including AI. Soft- and hardware are developed based on octopus features. Soft-robotics octopus-inspired arms are the most common type of developments. There are a lot of different variants of this solution, each of them is different from the other. In this paper, we describe the most remarkable octopus features, show solutions inspired by octopus and provide new ideas for further work and investigations in combination of AI and bioinspired soft-robotics areas.
... In contrast, modern deep learning systems, such as GPT-3, have over 100 billion synapses [28] and yet fail at similar forms of sophisticated associative learning. Even in the mollusca phylum, octopuses have been found to perform observational learning, with single shot accuracy at selecting novel objects by simply watching another octopus perform the task [29]. This rapid form of (continual) learning allows the animal to effectively use an object it has never seen before in new situations (constraints and causality), simply by choosing to play with it (curiosity). ...
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Research on both natural intelligence (NI) and artificial intelligence (AI) generally assumes that the future resembles the past: intelligent agents or systems (what we call 'intelligence') observe and act on the world, then use this experience to act on future experiences of the same kind. We call this 'retrospective learning'. For example, an intelligence may see a set of pictures of objects, along with their names, and learn to name them. A retrospective learning intelligence would merely be able to name more pictures of the same objects. We argue that this is not what true intelligence is about. In many real world problems, both NIs and AIs will have to learn for an uncertain future. Both must update their internal models to be useful for future tasks, such as naming fundamentally new objects and using these objects effectively in a new context or to achieve previously unencountered goals. This ability to learn for the future we call 'prospective learning'. We articulate four relevant factors that jointly define prospective learning. Continual learning enables intelligences to remember those aspects of the past which it believes will be most useful in the future. Prospective constraints (including biases and priors) facilitate the intelligence finding general solutions that will be applicable to future problems. Curiosity motivates taking actions that inform future decision making, including in previously unmet situations. Causal estimation enables learning the structure of relations that guide choosing actions for specific outcomes, even when the specific action-outcome contingencies have never been observed before. We argue that a paradigm shift from retrospective to prospective learning will enable the communities that study intelligence to unite and overcome existing bottlenecks to more effectively explain, augment, and engineer intelligences.
... There are also studies demonstrating future-oriented tool use and at least a minimal degree of planning in octopuses (Finn, Tregenza, and Norman 2009). Even more remarkably, Fiorito and Scotto (1992) report a case of domain-general observational learning (although this finding has not yet been replicated). Similarly, rodents and primates have shown the ability to successfully perform a variety of higher-order cognitive tasks. ...
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Predictive processing framework (PP) has found wide applications in cognitive science and philosophy. It is an attractive candidate for a unified account of the mind in which perception, action, and cognition fit together in a single model. However, PP cannot claim this role if it fails to accommodate an essential part of cognition-conceptual thought. Recently, Daniel Williams (2018) argued that PP struggles to address at least two of thought's core properties-generality and rich compositionality. In this paper, I show that neither necessarily presents a problem for PP. In particular, I argue that because we do not have access to cognitive processes but only to their conscious manifestations, compositionality may be a manifest property of thought, rather than a feature of the thinking process, and result from the interplay of thinking and language. Pace Williams, both of these capacities, constituting parts of a complex and multifarious cognitive system, may be fully based on the architectural principles of PP. Under the assumption that language presents a subsystem separate from conceptual thought, I sketch out one possible way for PP to accommodate both generality and rich compositionality.
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Octopuses are mollusks that have evolved intricate neural systems comparable with vertebrates in terms of cell number, complexity and size. The cell types within the octopus brain that control their amazingly rich behavioral repertoire are still unknown. Here we profile cell diversity of the paralarval Octopus vulgaris brain to build a comprehensive cell type atlas that comprises mostly neural cells, as well as multiple glial subtypes, endothelial cells and fibroblasts. Moreover, we spatially map cell types within the octopus brain, including vertical and optic lobe cell types. Investigation of cell type conservation reveals a shared gene signature between glial cells of mice, fly and octopus. Genes related to learning and memory are enriched in vertical lobe cells, which show molecular similarities with Kenyon cells in Drosophila . Taken together, our data sheds light on cell type diversity and evolution of the complex octopus brain. Highlights & Key findings Characterization of different cell types present in the early paralarval brain Cross-species comparisons reveal a conserved glial gene expression signature Vertical lobe amacrine cells in octopus have molecular similarities to fly Kenyon cells Homeobox genes are defining transcription factors for cell type identity Recently expanded gene families may underlie cellular diversification
Chapter
Learning is a change in behavior that results from experience. Although genetic change allows populations to adapt to their environments across generations, behavioral change allows individual animals to adapt to their environments within a lifetime; learning plays a strong role in this individual adaptation, especially for animals that have long lives and therefore the time to learn. Learning occurs as a result of many types of interactions between animals and their environments. Animals must learn to filter out stimuli that have no important consequences (habituation), while enhancing their responses to highly relevant, often dangerous, stimuli (sensitization). They must learn what behaviors are likely to produce desirable and undesirable consequences (operant conditioning) and what stimuli might be associated with certain conditions or events (classical conditioning). Learning can support very practical activities, such as finding stored food, migrating, and recognizing suitable mates. In social settings, behavioral change can spread throughout a group as a result of observational learning much more quickly than it can as a result of natural selection. Finally, when animals play, they may be engaging in the most far-flung and intriguing type of learning.
Chapter
Imitation is so often an untractable phenomenon for comparative psychologists that some have declared the task of defining it hopeless. Yet commonalities in examples of imitation suggest that imitation is a coherent concept. To evaluate its meaning and significance, I examine the conception of imitation in accounts by four authors who have systematically investigated imitation: James Mark Baldwin, Conwy Lloyd Morgan, Paul Guillaume, and Jean Piaget. Each of these authors elucidates different stages or levels in the development of imitation which indicate significantly different psychological capacities in the production of imitation. The similarities between these developmental frameworks are remarkable (though differences are apparent), but the conceptions of imitation provided by these authors show some distinct differences. To offer a coherent account of imitation, I analyze it conceptually and offer necessary and sufficient criteria for its occurrence. I claim that imitation occurs when something C (the copy) is produced by an organism and/or machine, where: C is similar to something else M (the model); registration of M is necessary for the production of C; and C is designed to be similar to M. This definition offers formal criteria for imitation per se, but does not differentiate qualitatively different types of imitation. Thus, using and developing the accounts of Baldwin, Morgan, Guillaume, and Piaget, I depict five nested levels of imitation, such that imitation at each level is produced by a program which incorporates control over programs in preceding levels. I provide examples of imitation by humans and non-humans at each of these levels. These five levels of imitation are distinguished by the processes which bring about the imitation: first-level imitations are based on evolution, selection, and morphogenesis; second-level, on perception and action; third-level, on learning; fourth-level, on self-awareness; and fifth-level, on planning and the awareness of another’s awareness. Imitation, then, is a conceptually coherent phenomenon with various manifestations, which result from processes at different but hierarchically related levels.
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The red squirrel is a food opportunist, exploiting the seed resources in many types of forest and possessing the capacity for learning new feeding techniques. Two groups of naive, individually isolated squirrels were presented with hickory nuts for the first time. One group could observe an experienced squirrel (Model) feeding. Comparisons of the metabolic cost of feeding. times, and techniques after 6 wk showed that the group with the Model expended half the time and energy used by other group while feeding and approached the Model in time and technique. The improved performance persisted after removal of the Model. While feeding techniques may develop by trial and error, observational learning (for example, from a parent or other conspecific) is more efficient in terms of energy and time and may be crucial to the safe and rapid exploitation of new foods and habitats.
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The memory mechanisms of cephalopods consist of a series of matrices of intersecting axes, which find associations between the signals of input events and their consequences. The tactile memory is distributed among eight such matrices, and there is also some suboe-sophageal learning capacity. The visual memory lies in the optic lobe and four matrices, with some re-exciting pathways. In both systems, damage to any part reduces proportionally the effectiveness of the whole memory. These matrices are somewhat like those in mammals, for instance those in the hippocampus. The first matrix in both visual and tactile systems re-ceives signals of vision and taste, and its output serves to increase the tendency to attack or to take with the arms. The second matrix provides for the correlation of groups of signals on its neurons, which pass signals to the third matrix. Here large cells find clusters in the sets of signals. Their output re-excites those of the first lobe, unless pain occurs. In that case, this set of cells provides a record that ensures retreat. There is experimental evidence that these distributed memory systems allow for the identification of categories of visual and tactile inputs, for generalization, and for decision on appropriate behavior in the light of experience. The evidence suggests that learning in cephalopods is not localized to certain layers or "grandmother cells" but is distributed with high redundance in serial networks, with recurrent circuits.
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juvenile Dicentrarchus labrax having achieved good or poor performance in a task involving pushing a lever to obtain food served as demonstrators for conspecifics naive to the task. The results show that fish exposed to good demonstrators were subsequently more likely to engage in the same operant act than same-aged fish that observed poor demonstrators. Thus the development of traditions is shown to be possible in small groups of fish of the same age, originating in the appearance of a novel, adaptive behaviour by certain innovative individuals.
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Evidence is presented for the ability of Indian Ocean bottlenose dolphins (Tursiops aduncus) to learn complex behavioural sequences by observation and to imitate a wide variety of previously unfamiliar motor patterns and sounds, without any apparent external reinforcement apart from the performance of the activity itself, both in the presence and in the absence of the stimulus which originally evoked the imitative behaviour. The reproduction in fine detail by a dolphin of the comfort and sleeping movements of a Cape Fur Seal (Arctocephalus pusillus), leading to behavioural interactions between the two forms with attempts at copulation, and culminating in aggression is described. Further instances of observational learning are cited, including the imitation by dolphins of the activities and sounds of human divers during maintenance operations in the pool which resulted in elementary tool-using behaviour by the dolphins. Interactions between dolphins and seals occurred not only in captivity but also under free-ranging conditions. The significance of imitation in delphinids for comparative assessments of animal intelligence is discussed and the possible function under normal conditions of the delphinid faculty to imitate is considered. It is proposed that the tendency to imitate may be genetically programmed in delphinids to operate in the selection of compatible sexual partners, in the reinforcement of social bonds and in the strengthening of group cohesiveness.
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Pairs of individually recognizable male Octopus vulgaris were observed in a large seawater tank containing two suitable homes (brick pots or plastic buckets). None of the animals established exclusive occupancy of one home and for much of the time both animals were associated together at the same site. Usually one of the two homes was preferred and its occupant was most likely to be the larger animal, or the earlier resident if they were of equal size. Large animals were observed to take food forcefully from smaller octopus. An arm alignment interaction is described which, it is suggested, may be a means by which two octopuses establish their relative sizes.
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Operant conditioning was studied in six specimens of Octopus cyaneus Gray. An “arm-out-of-water” operant, in which the octopus inserted an arm up a feeding-tube breaking the water surface, proved susceptible to reinforcement schedules. An apparatus was developed that provided automated reinforcement and recording. Performance was studied under continuous reinforcement, fixed-ratio and variable-ratio schedules, and extinction conditions.
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The vertical lobe system in Octopus is concerned in the regulation of the tendency to attack. It receives impulses from the optic lobes, from touch and chemoreceptors and from pain receptors. The visual part of the system is organized into lower and upper loops. The lower loop leads from the optic lobes, through two centres and back to the optic lobes. The upper loop also consists of two centres, superposed in parallel above the lower ones. Each of the two loops thus contains two centres in series and it is suggested that the first centre of each pair tends to promote attack and the second to restrain or prevent it. The net effect of the two centres of each pair together is to increase the probability of attack, unless pain intervenes. After any interruption of the lower loop an octopus does not launch out to attack a crab moving in its visual field, although it still puts out an arm to take a crab that is within reach. The impulses set up in the visual system cannot release an attack without the 'amplification' produced by the centres of the lower loop. After interruption of the upper loop the octopus is still able to attack but the animals make errors both in failure to attack when rewarded with food and in continuing to attack in spite of shocks. Individual untrained octopuses were found to show consistent differences, in tendency to attack crabs, and these differences survived anaesthesia and dummy operation. However, any interruption of the upper loop tended to reverse the previous attack tendency. When the tendency to attack was high it was decreased by removal of the median superior frontal but not by removal of the vertical lobes. Removal of the median superior frontal after the vertical leads to a reduction in attacks, but removing the vertical after the superior frontal was followed by an increase. This evidence that the median superior frontal increases the tendency to attack and the vertical lobe reduces it was confirmed at longer periods after operation. Attacks at crabs in spite of shocks continued longer after removal of either lobe than in controls, but more attacks were made by animals without vertical than without median superior frontal lobes. The main output of the superior frontal is through the vertical and thus any injury affects both functions. However, severing the tract between them or removing both of them produced effects different from removing either alone. Each therefore has some effect when acting in isolation, though they normally operate together to influence the attack behaviour. There was greatly increased variability between individuals and within the performance of each individual after any interference with the vertical lobe system. This upper loop thus serves to produce stable and consistently adaptive behaviour, in addition to other effects that it may have in the process of learning.
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In the greenfinch, Chloris chloris, single birds can learn a food discrimination task more rapidly than pairs of birds, though fewer of the latter are fearful of approaching the discriminanda. This behaviour can fail to be maladaptive only in species with relatively conservative food habits, or of a solitary nature. In the more inquisitive and exploitative great tit, on the other hand, the birds suffered no disadvantage when trained in pairs. Thus, additional evidence is provided to support the view that species characteristic behaviour may be determined by imitative processes and the establishment of traditions, as well as by innate differences in structure and behaviour.