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Corpus Callosum Size in Delphinid Cetaceans
Abstract
The midsagittal surface area of the corpus callosum was determined by computer-assisted morphometry in juvenile and adult members of 13 species of the cetacean family Delphinidae. In 57 brains, absolute callosal areas ranged from 104 to 829 mm2. When compared to other mammal groups possessing a corpus callosum, callosal area in dolphins was smaller in relation to brain mass with a ratio range (mm2/g) of 0.08-0.31. The corpus callosum was decreased relative to brain mass in the larger-brained odontocetes, suggesting that increases in brain size were not necessarily allied with needs for equivalent increases in callosal linkage. One delphinid species, Tursiops truncatus, for which the largest single-species sample was available, was examined for sex differences in callosal size relative to brain mass. Among 10 males and 5 females the averaged ratio was not distinguishable between sexes.
... Furthermore, dolphins, which have a corpus callosum, albeit of a greatly diminished size (Ridgway, 1986;Tarpley & Ridgway, 1994;Lyamin et al., 2008), sleep unihemispherically and exhibit asymmetrical burst suppression under anesthesia (Howard et al., 2006). Taken together, these studies suggest that the absence, or evolutionary reduction, of the corpus callosum may allow the induction of asymmetrical burst suppression under anesthesia, whereas the ability to engage in unihemispheric sleep appears to be the result of further mechanistic or structural differences. ...
... Furthermore, dolphins, which have a greatly diminished corpus callosum (Ridgway, 1986;Tarpley & Ridgway, 1994), both sleep unihemispherically and exhibit asymmetric burst suppression patterns under anesthesia (Howard et al., 2006). ...
Sleep is an enigmatic state engaged in by all organisms studied to date. In spite of sleeps ubiquitous presence across the animal kingdom sleep manifests differently in different taxonomic groups. Interestingly, sleep in birds and mammals is composed of two distinct sub-states, slow wave sleep (SWS) and rapid eye movement (REM) sleep. Despite the presence of these similar states in birds and mammals, it has been unclear whether reptiles exhibit similar sleep states, raising the possibility that these states evolved independently in birds and mammals. In this thesis I examined various characteristics of sleep in birds and reptiles to gain a better understanding of the evolution of sleep states. Chapter 2 describes electrical signals under isoflurane anesthesia in crocodiles that are similar in some, but not all, respects to those occurring during SWS in birds. Chapter 3 demonstrates that SWS and REM sleep are present in tinamous, a member of an early evolutionary branch of birds.. Chapter 4 demonstrates that sleep responds similarly to predation risk in birds and mammals. In chapter 5, I show that, in birds, anesthetics induce brain activity in many, but not all, respects similar to SWS. These results further demonstrate that SWS and REM sleep in birds and mammals share similar regulatory mechanisms. I propose that the electrophysiological patterns observed in crocodiles reflect an ancestral form of SWS present in the common ancestor to reptiles, birds, and mammals, that was independently elaborated upon in mammals and birds.
... This hypothesis would explain why the hemisphere that passively receives imposed slow activity maintains its awake, conscious state, although the other hemisphere, where the slow activity originates, is fully anaesthetized. This situation may be reminiscent of that of dolphins and other whales, when they have slow-wave sleep in one hemisphere while the other is awake (Rattenborg et al., 2000) -although the corpus callosum is relatively small in some dolphin species (Tarpley & Ridgway, 1994). This concept may be called "cross-state unreceptiveness (CSUR)" (or "cross-state unresponsiveness/ refractoriness"). ...
Background
In the Wada test, one hemisphere is selectively anaesthetised by unilateral intracarotid injection of a fast-acting anaesthetic agent. This gives a unique opportunity to observe the functions and physiological activity of one hemisphere while anaesthetising the other, allowing direct comparisons between brain states and hemispheres that are not possible in any other setting.
Aim
To test whether potential measures of consciousness would be affected by selective anaesthesia of one hemisphere, and reliably distinguish the states of the anesthetised and non-anesthetised hemispheres.
Methods
We analysed EEG data from 7 patients undergoing Wada-tests in preparation for neurosurgery and computed several measures reported to correlate with the state of consciousness: power spectral density, functional connectivity, and measures of signal diversity. These measures were compared between conditions (normal rest vs. unilateral anaesthesia) and hemispheres (injected vs. non-injected), and used with a support vector machine to classify the state and site of injection objectively from individual patient's recordings.
Results
Although brain function, assessed behaviourally, appeared to be substantially altered only on the injected side, we found large bilateral changes in power spectral density for all frequency bands tested, and functional connectivity changed significantly both between and within both hemispheres. Surprisingly, we found no statistically significant differences in the measures of signal diversity between hemispheres or states, for the group of 7 patients, although 4 of the individual patients showed a significant decrease in signal diversity on the injected side. Nevertheless, including signal diversity measures improved the classification results, indicating that these measures carry at least some non-redundant information about the condition and injection site. We propose that several of these results may be explained by conduction of activity, via the corpus callosum, from the injected to the contralateral hemisphere and vice versa, without substantially affecting the function of the receiving hemisphere, thus reflecting what we call “cross-state unreceptiveness”.
... However, Balaena is an outlier having a lower index of folding and less cortex surface area relative to brain size (note differences in gyrencephaly apparent when we compare the brains shown in Fig. 17.2). The midsagittal surface area of the bowhead corpus callosum relative to brain mass (CCA:BM) is higher than what has been reported for other cetacean species Tarpley and Ridgway, 1994). In general, cetaceans possess smaller corpus callosum surface areas relative to terrestrial species. ...
Bowhead whales are one of the least encephalized mammals, possessing a small brain relative to their body size (e.g., a 3 kg brain in a 30,000 kg body). Features of the bowhead whale brain include a blunted temporal lobe and a gyrification index that is less than most cetaceans. Rather than having a cerebrum that is wider than long like odontocetes, the bowhead cerebrum is longer than it is wide. The hippocampus is very small and located within the lateral ventricle, which is ventral to the corpus callosum. The cytoarchitecture of the bowhead cerebral cortex is consistent with that of other cetaceans. The cortex is thin overall with a relatively thick, prominent layer I. As with other cetaceans, there is no granular layer IV. Notably, high numbers of von Economo neurons and fork neurons are found in all regions of the cortex. The highest numbers of these special neurons are observed at the apex of gyri.
... The missing layer, cortical layer 4, is essential for connecting distributed cortical regions in terrestrial mammals (Dantzker and Callaway, 2000), and its absence, in addition to the sparse cross-hemispheric connections in cetaceans, has been taken as evidence for generally low corticocortical connectivity in the whales and dolphins. Importantly, cross-hemispheric connectivity may be reduced in part to allow for unihemispheric sleep (Tarpley and Ridgway, 1994). More recent histological examination of whale and dolphin cortex has indicated unusual patterns of dense local connectivity (Hof et al., 2005). ...
Macphail’s comparative approach to intelligence focused on associative processes, an orientation inconsistent with more multifaceted lay and scientific understandings of the term. His ultimate emphasis on associative processes indicated few differences in intelligence among vertebrates. We explore options more attuned to common definitions by considering intelligence in terms of richness of representations of the world, the interconnectivity of those representations, the ability to flexibly change those connections, and knowledge. We focus on marine mammals, represented by the amphibious pinnipeds and the aquatic cetaceans and sirenians, as animals that transitioned from a terrestrial existence to an aquatic one, experiencing major changes in ecological pressures. They adapted with morphological transformations related to streamlining the body, physiological changes in respiration and thermoregulation, and sensory/perceptual changes, including echolocation capabilities and diminished olfaction in many cetaceans, both in-air and underwater visual focus, and enhanced senses of touch in pinnipeds and sirenians. Having a terrestrial foundation on which aquatic capacities were overlaid likely affected their cognitive abilities, especially as a new reliance on sound and touch, and the need to surface to breath changed their interactions with the world. Vocal and behavioral observational learning capabilities in the wild and in laboratory experiments suggest versatility in group coordination. Empirical reports on aspects of intelligent behavior like problem-solving, spatial learning, and concept learning by various species of cetaceans and pinnipeds suggest rich cognitive abilities. The high energy demands of the brain suggest that brain-intelligence relationships might be fruitful areas for study when specific hypotheses are considered, e.g., brain mapping indicates hypertrophy of specific sensory areas in marine mammals. Modern neuroimaging techniques provide ways to study neural connectivity, and the patterns of connections between sensory, motor, and other cortical regions provide a biological framework for exploring how animals represent and flexibly use information in navigating and learning about their environment. At this stage of marine mammal research, it would still be prudent to follow Macphail’s caution that it is premature to make strong comparative statements without more empirical evidence, but an approach that includes learning more about how animals flexibly link information across multiple representations could be a productive way of comparing species by allowing them to use their specific strengths within comparative tasks.
The majority of cetacean research suggests a right side/left cerebral hemisphere bias for processing visuospatial information and a left side/right cerebral hemisphere bias for processing social information. Beluga (Delphinapterus leucas) socio-sexual behavior involves motor skills coordination and is also hypothesized to serve a social function. The present study assessed whether 14 belugas in managed care displayed side bias in their lateral socio-sexual presentation behavior. No species-level bias was found, the majority of individuals did not display a side bias, and side use was not dependent on sex of the recipient, although some influence of swim direction was found. Only males had a statistically significant but small left side preference. Furthermore, there was a linear correlation with the left side being used increasingly more over Years 1-6 of life. This study suggests that belugas do not display consistent laterality of socio-sexual presentation behavior, which is in contrast to the laterality of mother-calf positions for belugas and the high levels of laterality that are reported for some behaviors of other cetacean species. Thus, it seems that beluga socio-sexual presentation behavior is flexible and may serve both motor skills practice and social functions, which likely involve both cerebral hemispheres as a cognitively engaging behavior.
CetaceanCetacea/cetaceans minds have been the topic of intense scientific interest for decades, and our continued study of them takes us on a complicated journey that requires us to regard cetacean brainsBrain and behavior as simultaneously very different and very familiar to us. Cetacean brains have undergone one of the most dramatic transformations during their evolutionEvolution from terrestrial animals to the highly acoustic and socially sophisticated animals we know today. Their brains are a challenging combination of highly conserved mammalian characteristics along with a unique neocortical organization that suggests that it processes information through alternative neural strategies to those of the primate brain. Their sensorium and perceptual capacities, especially in the realm of communicationCommunication, are unusual even for a fully aquatic mammal. Their cognitive and social capacities make it clear that there are striking convergences in psychology between cetaceansCetacea/cetaceans and many terrestrial carnivores as well as primates such as we are, including the reliance on strong social bondsSocial bonds and, in many cases, culturalCultural traditions.
Sensory laterality is influenced by the individual's attentional state. There are variations in the way different individuals of a same species attend to stimuli. When confronted to novelty, some individuals are more explorative than others. Curiosity is composed of sensation and knowledge seeking in humans. In the present study, we hypothesized that more curious animals, i.e., showing more sensory exploration would be less lateralized than quietly attentive individuals, performing instead more gazing behaviours. In order to test this hypothesis and its possible generality, we performed two studies using two animal models (dolphins and starlings) and two modalities (visual and auditory) of presentation of species-specific and non-species-specific stimuli. Both dolphins and starlings presented more gazes for the species-specific stimuli and more exploratory components for the non-species-specific stimuli. Moreover, in both cases, the non-species-specific stimuli involved more lateralized responses whereas there was no or less clear laterality for the species-specific stimuli. The more exploratory dolphins and starlings also showed a decreased laterality: the more "curious" individuals showed no laterality. Further studies are needed on characterization of curiosity in relation to attention structure. The present study suggests that individual variations in sensory laterality may help disentangle the subtle differences between curiosity, attention and boldness.
Rilling & Insel have argued that in primates, bigger brains have proportionally fewer anatomical interhemispheric connections, leading to reduced functional connectivity between the hemispheres (1). They based this on a comparison between surface areas of the corpus callosum and cortex rather than estimating connection counts, while leaving out other quantities also dependent on brain size such as callosal fiber density, neuron density, and number of functional areas.
We use data from the literature to directly estimate connection counts. First, we estimate callosal fiber density as a function of brain size. We validate this by comparing out-of-sample human data to our function’s estimate. We then mine the literature to obtain function estimates for all other quantities, and use them to estimate intra- and interhemispheric white matter connection counts as a function of brain size.
The results show a much larger decrease in the scaling of interhemispheric to intrahemispheric connections than previously estimated. However, we hypothesize that raw connection counts are the wrong quantity to be estimating when considering functional connectivity. Instead, we hypothesize that functional connectivity is related to connection counts relative to the number of cortical areas.
Accordingly, we estimate inter-area connection counts for intra- and interhemispheric connectivity and find no difference in how they scale with brain size. We find that, on average, an interhemispheric inter-area connection contains 3-8x more connections than an intrahemispheric inter-area connection, regardless of brain size. In doing so, we find that the fiber count of the human corpus callosum has been underestimated by 20%.
Significance Statement
There are arguments in the literature that larger brains have proportionally fewer interhemispheric connections. We find that the decrease is even larger than previously estimated. However, we argue that this quantity is the wrong thing to measure: Rather, we should measure functional connectivity between cortical areas. We show that the ratio of interhemispheric and intrahemispheric connectivity between cortical areas is constant across mammalian species. These findings are consistent with a growing literature that suggest interhemispheric connectivity is special across all primate species.
Sleep and wakefulness are opposite brain and body conditions that accomplish different but complementary functions. However, these opposing conditions have been combined in some animals by the adoption of a sleep/wake strategy that allows them to survive, while maintaining both an interaction with the environment at the same time as enabling brain and body recovery. They sleep with half of the brain while keeping the other half awake: a state known as unihemispheric sleep (US). Sleep of cetaceans is exclusively in the form of US; therefore, they experience neither bihemispheric sleep (BS) nor REM sleep. US episodes have also been recorded in eared seals and some species of birds. In those animals, US episodes are intermingled with episodes of BS and REM sleep. Studies have reported both a lateralized release of some neurotransmitters and a drop of brain temperature during US. The aims of this article are to formulate hypotheses about the neural mechanisms of unihemispheric sleep(US) based on findings regarding the neural mechanisms of the sleep/wake cycle of mammals. The neural mechanisms of the sleep/wake cycle are largely preserved across species, allowing to hypothesize about those triggering and regulating US.
The slow waves of NREM-sleep reflect experience-dependent plasticity and play a direct role in the restorative functions of sleep. Importantly, slow waves behave as traveling waves and their propagation is assumed to occur through cortico-cortical white matter connections. In this light, the corpus callosum (CC) may represent the main responsible for cross-hemispheric slow wave propagation. To verify this hypothesis, we performed overnight hd-EEG recordings in five patients who underwent total callosotomy due to drug-resistant epilepsy (CP; 2 females), in three non-callosotomized neurological patients (NP; 2 females), and in sample of 24 healthy adult subjects (HS; 13 females). In all CP slow waves displayed a significantly reduced probability of cross-hemispheric propagation and a stronger inter-hemispheric asymmetry. In both CP and HS, the incidence of large slow waves within individual NREM epochs tended to differ across hemispheres, with a relative overall predominance of the right over the left hemisphere. The absolute magnitude of this asymmetry was greater in CP relative to HS. However, the CC resection had no significant effects on the distribution of slow wave origin probability across hemispheres. Present results indicate that CC integrity is essential for the cross-hemispheric traveling of human sleep slow waves, in line with the assumption of a direct relationship between white matter integrity and slow wave propagation. Our findings also revealed a residual cross-hemispheric slow wave propagation that may rely on alternative pathways, including cortico-subcortico-cortical loops. Finally, this data indicate that the lack of the CC does not lead to differences in slow wave generation across brain hemispheres.
There is increasing interest in finding anatomical correlates in the brain for presumed gender-related differences in cognitive functioning. Recent attention has been drawn to reported sex differences in the human corpus callosum as reflecting sex differences in hemispheric lateralization of visuospatial functions. The question is whether or not existing knowledge of the corpus callosum permits interpretations that relate differing cognitive functions to variations in size and shape of the callosum. The striking variations in callosal size and shape among individuals regardless of gender, when viewed in the context of a growing body of experimental findings, suggest that postnatal maturational processes of the corpus callosum are significantly affected by experience.
Variable partial midline surgery on monkeys has revealed several characteristics of interhemispheric communication of visually learned pattern discriminations. The results show both that interhemispheric communication of visual information in the commissure-intact animal need not be immediate, and that when communication does occur transmission involves specific forebrain commissural components.RésuméDes interventions partielles et variables portant sur la ligne médiane chez des singes ont révelé plusieurs caractéristiques de communications interhémisphériques de discrimination des modèles optiquement appris. Les résultats montrent à la fois que la communication interhémisphérique de l'information visuelle chez l'animal avec commissures intactes n'a pas besoin d'être immédiate et que lorsque cette communication survient la transmission implique des composantes commissurales spécifiques du télencéphale.ZusammenfassungIn Affenversuchen wurden an verschiedenen Stellen mittelliniennahe Hemisphärenverbindungen partiell operativ unterbrochen. Es zeigte sich dabei, dass mehrere Arten interhemisphärischer Wechselbeziehungen für die Unterscheidungsfähigkeit optisch erlernter Handlungsmodelle bestehen. Aus den Ergebnissen liessen sich zweierlei Folgerungen ziehen: einmal, dass Versuchstiere mit intakten kommissuralen Verbindungen bei Weitergabe optischer Informationen an beide Hemisphären keinen direkten Zugangsweg benötigten, und dann, dass eine kommunikative Wechselbeziehung, die auf diese Weise zustande kam, für die interhemisphärische Verbindung spezifischer Vorderhirnkommissuren bedurfte.
The number, types, and distribution of distinct classes of axons and glia in four cerebral commissures of the adult rhesus monkey (Macaca mulatta) were determined using electron microscopic and immunocytochemical methods. The two neocortical commissures, the corpus callosum, and the anterior commissure contain small but cytologically distinct archicortical components: the hippocampal commissure, which lies ventral to the splenium of the corpus callosum, and the basal telencephalic commissure, which forms a small crescent at the anterior margin of the anterior commissure. Each archicortical pathway is delineated from the adjacent neocortical commissure by a glial capsule. The glia cells that form this border are immunoreactive with antisera directed against glial fibrillary acidic protein (GFAP) and issue long processes that form numerous desmosomal junctions with one another. Braids of these glial processes envelop axonal fascicles within the archicortical commissures. In contrast, the GFAP-positive cells of the corpus callosum and anterior commissure are randomly distributed cells with relatively short stellate processes that do not form boundaries around axon fascicles.
Quantitative anatomical investigations provide the basis for functional models. In this study the density of neurons and synapses was measured in three different areas (8, 6, and 17) of the neocortex of the mouse. Both kinds of measurements were made on the same material, embedded in Epon/Araldit. In order to determine the synaptic density per mm3, the proportion of synaptic neuropil was also measured; it was found to be 84%. The cortical volume occupied by cell bodies of neurons and glia cells amounted to 12%, that by blood vessels to 4%.
The total average was 9.2 × 104 neurons/mm3 and 7.2 × 108 synapses/mm3. About 11% of the synapses were of type II. The density of neurons increased with decreasing cortical thickness; thus the number of neurons under a given surface area was about constant. The synaptic density, on the other hand, was almost constant in the three areas, the number of synapses under a given cortical surface area tended, therefore, to increase with cortical thickness. The average number of synapses per neuron was 8,200, with a tendency to increase with increasing cortical thickness.
Shrinkage of the tissue was also measured for various staining techniques. No shrinkage occurred during perfusion with 3.7% formaldehyde or with a solution of buffered paraformaldehyde and glutaraldehyde and during fixation in situ. Electron microscopical material showed almost no shrinkage, whereas Nissl-preparations on paraffin-embedded material had only 43% of their original volume. After Nissl stain on frozen sections the volume had shrunken to 68% and after Golgi impregnation and embedding in celloidin to 70%. The total volume of the neocortex was 112 mm3 (both hemispheres together). The total number of neurons was thus 1.0 × 107 and the total number of synapses 8.1 × 1010.
There is much disagreement in the literature about whether or not certain parts of the corpus callosum show a sexual dimorphism. Amidst this debate, a rather surprising area of agreement is neglected: Even though there are dramatic overall sex differences in brain size (brain size being quite directly related to body surface), the corpus callosum of males and females shows no such drastic size difference. The significance of this lack of allometry is discussed in terms of putative functions of the corpus callosum. At present, there is no reason to assume that whatever can or cannot be said about sex differences in corpus callosum parameters cannot also be said more generally about large and small brains.
Variations in the size of the human corpus callosum were examined as a possible morphological substrate of functional asymmetries of the cerebral hemispheres, such as cerebral speech dominance. The midsagittal surface area of the corpus callosum, obtained by magnetic resonance imaging, was measured in 50 patients with epilepsy and 50 neurologically normal control subjects. The mean callosal area did not differ significantly between patients and control subjects, between left-handed and right-handed subjects, or between men and women. When measurements were compared among 44 patients, whose cerebral speech dominance had been determined by the intracarotid injection of sodium amytal, the area of the corpus callosum was significantly greater in patients with right-hemisphere cerebral speech dominance. The mean callosal area was greater by 109 to 159 square millimeters (18-28%) when compared to that of patients with either left-hemisphere speech dominance or bilateral speech representation. This difference in midsagittal surface area could represent as many as 37 to 54 million additional callosal axons in subjects with right-hemisphere cerebral speech dominance.
The relationships between brain weight, sex and various callosal parameters including cross-sectional surface area and maximum splenial width in nonhuman primates are delineated. Overall, brain weight is a good predictor of quantitative aspects of the corpus callosum. However, both pongids and strepsirhines evince sex differences on certain callosal measures. No sex differences were found for either the ceboids or cercopithecoids. We speculate that one aspect of primate brain evolution has involved the modulation of interhemispheric connectivity along the lines of sex.
Neuronal and glial numerical densities were measured in the lateral gyrus of the cerebral hemisphere of dolphins (Tursiops truncatus) from the neonatal period to adulthood. The cortex studied is the area known to be visually excitable in evoked potential studies. Two distinct parts of the adult lateral gyrus are identifiable, one relatively anterior, in which neuronal density is 23,000/mm3, the other more posterior, with' almost double this density. In a neonate, the neuronal density in the anterior lateral gyrus was found to be more than double that of the adult. No samples from the immature posterior area were available.
Glial density varies much less than neuronal density, both with age and between areas. Soon after birth the glia/neuron ratio is 1.6 in anterior lateral gyrus, rising to around 3 in the adult anterior lateral area, and rather less in the posterior region, where neuronal density is high.
We speculate that the existence of a high numerical density of neurons in the posterior part of the dolphin visual cortex could perhaps indicate a specialized area corresponding to the primate primary visual cortex, also known to have high neuronal density.