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Page 436. CHAPTER 22 Reinventing Primate Neuroscience for the Twenty-First Century Todd M. Preuss The manner in which an organism perceives and responds to features of its environment reflects the state of the neural systems that make up... more
Page 436. CHAPTER 22 Reinventing Primate Neuroscience for the Twenty-First Century Todd M. Preuss The manner in which an organism perceives and responds to features of its environment reflects the state of the neural systems that make up its brain. ...
Subdivisions of the prefrontal cortex (PFC) evolved at different times. Agranular parts of the PFC emerged in early mammals, and rodents, primates, and other modern mammals share them by inheritance. These are limbic areas and include the... more
Subdivisions of the prefrontal cortex (PFC) evolved at different times. Agranular parts of the PFC emerged in early mammals, and rodents, primates, and other modern mammals share them by inheritance. These are limbic areas and include the agranular orbital cortex and agranular medial frontal cortex (areas 24, 32, and 25). Rodent research provides valuable insights into the structure, functions, and development of these shared areas, but it contributes less to parts of the PFC that are specific to primates, namely, the granular, isocortical PFC that dominates the frontal lobe in humans. The first granular PFC areas evolved either in early primates or in the last common ancestor of primates and tree shrews. Additional granular PFC areas emerged in the primate stem lineage, as represented by modern strepsirrhines. Other granular PFC areas evolved in simians, the group that includes apes, humans, and monkeys. In general, PFC accreted new areas along a roughly posterior to anterior trajectory during primate evolution. A major expansion of the granular PFC occurred in humans in concert with other association areas, with modifications of corticocortical connectivity and gene expression, although current evidence does not support the addition of a large number of new, human-specific PFC areas.
Modern studies of granular frontal cortex (GFC) in large-brained, anthropoid primates, such as Macaca, indicate that this region is comprised of many areal subdivisions. These areas vary in their architectonic appearance and each has a... more
Modern studies of granular frontal cortex (GFC) in large-brained, anthropoid primates, such as Macaca, indicate that this region is comprised of many areal subdivisions. These areas vary in their architectonic appearance and each has a distinctive, diverse set of corticocortical connections. The great extent of the GFC region in anthropoids, and its high degree of areal parcellation, suggest that some GFC areas may be specializations of anthropoids, not found in other mammals. To investigate this possibility, we studied the corticocortical connections of GFC in the relatively small-brained, strepsirhine primate Galago, with a series of eight tracer injections in the frontal cortex, and an additional eight injections of parietal and temporal cortex. Tracers used were wheat-germ agglutinin conjugated to horseradish peroxidase and tritiated amino acids. Our results indicate that Galago GFC has strong, reciprocal connections with the parietal area-7 complex and with higher-order temporal areas; there are additional connections with extrastriate visual cortex, parahippocampal, and cingulate areas, and frontal cortex. Thus GFC has an extremely diverse array of cortical connections in Galago, as in Macaca. However, we also found that the pattern of parietofrontal connections is simpler in Galago than in Macaca. Specifically, parietal areas project to fewer discrete zones within the GFC of Galago, consistent with the view that these animals have fewer GFC areas than Macaca. In addition, Galago GFC possesses connections that specifically resemble those of Macaca arcuate cortex, but lacks connectional patterns that are characteristic of principalis cortex. These results are in accord with our previous architectonic studies, which indicated that Galago does not possess homologues of principalis areas. We conclude that the arcuate areas are common elements of primate GFC organization, while the areas located within and adjacent to the principal sulcus are anthropoid specializations.
We have conducted a systematic comparison of the ipsilateral (uncrossed) and contralateral (crossed) thalamic connections of prefrontal cortex in macaque monkeys, using cortical implants of horseradish peroxidase pellets and tetramethyl... more
We have conducted a systematic comparison of the ipsilateral (uncrossed) and contralateral (crossed) thalamic connections of prefrontal cortex in macaque monkeys, using cortical implants of horseradish peroxidase pellets and tetramethyl benzidine histochemistry to demonstrate anterograde and retrograde thalamic labeling. Contrary to the prevailing belief that thalamocortical projections are entirely uncrossed, our findings indicate that a modest crossed projection to prefrontal cortex arises from the mesial thalamus, principally the anteromedial and midline nuclei. Also, while confirming that corticothalamic projections are bilateral, we found that the pattern of crossed projections differs from that of uncrossed projections. Projections to mesial thalamic nuclei, specifically to the anteromedial nucleus, the midline nuclei, and the magnocellular part of the mediodorsal nucleus are bilateral, the contralateral projection being nearly as dense as the ipsilateral projection. Projections to the parvicellular part of the mediodorsal and ventral anterior nuclei are also bilateral, but the contralateral projection is much weaker than the ipsilateral projection. Prefrontal projections to the reticular nucleus, medial pulvinar, suprageniculate nucleus, and limitans nucleus appear to be exclusively ipsilateral.These results indicate that prefrontal cortex has prominent bilateral and reciprocal connections with the nuclei of the mesial thalamic region. As this region of the diencephalon has been implicated by anatomical and behavioral studies in memory functions, our findings suggest that prefrontal cortex, through its connections with this region, may be involved in the bilateral integration of mnemonic systems.
In macaque monkeys with injections of tritiated amino acids or horseradish peroxidase in the ventrolateral granular frontal cortex, we observed extensive anterograde and retrograde labeling of the premotor and somatosensory cortex in and... more
In macaque monkeys with injections of tritiated amino acids or horseradish peroxidase in the ventrolateral granular frontal cortex, we observed extensive anterograde and retrograde labeling of the premotor and somatosensory cortex in and around the lateral sulcus. Comparable labeling was not present with large and small control injections of the dorsal granular cortex. Cytoarchitectonic evaluation of the perisylvian cortex in the three cases examined in detail indicated that labeled areas included the ventral premotor cortex (area 6V); the precentral opercular and orbitofrontal opercular areas (PrCO and OFO); the second somatosensory area (S-II); the opercular cortex immediately anterior to S-II, possibly corresponding to area 2 of the S-I complex; and the central part of the insular cortex, including portions of the granular and dysgranular insular fields (Ig, Idg). Labeling was particularly dense and extensive in areas 6V, S-II, and OFO. Lighter labeling was also present in the rostral inferior parietal lobule (areas 7b and POa). The distribution of label within perisylvian areas was not uniform: certain parts were heavily labeled, while other parts were lightly labeled or unlabeled. Comparison of label distribution with published accounts of the somatotopy of these areas indicates that forelimb and orofacial representations were selectively labeled. Further, our results, taken together with other recent anatomical findings (e.g., Matelli et al.: Journal of Comparative Neurology 251:281-298, 1987; Barbas and Pandya: Journal of Comparative Neurology 256:211-228, 1987) suggest strongly that there is a network of interconnected forelimb and orofacial representations in macaque cortex, involving the ventral granular frontal cortex, area 6V, OFO, opercular area 2, S-II, the central insula, and area 7b. Each injection of frontal cortex which labeled the perisylvian somatic cortex involved the cortex of the ventral rim of the principal sulcus (PSvr). The cortex surrounding the PSvr does not stand out as a distinct area in Nissl-stained material. However, examination of myelin-stained sections prepared from uninjected hemispheres with the Gallyas technique revealed the existence of a distinct zone centered on the PSvr. This myeloarchitectonic area, which we term area 46vr, is more heavily myelinated than the ventral bank and fundus of the principal sulcus (area 46v) but is less heavily myelinated than the ventral (inferior) convexity (area 12). Involvement of area 46vr in our injections was probably responsible for the strong labeling observed in perisylvian somatic areas.(ABSTRACT TRUNCATED AT 400 WORDS)
Our understanding of human brain evolution has advanced enormously over the past decade, owing to contributions of scientists from many different branches of the life sciences. This chapter reviews some of the concepts and findings from... more
Our understanding of human brain evolution has advanced enormously over the past decade, owing to contributions of scientists from many different branches of the life sciences. This chapter reviews some of the concepts and findings from evolutionary biology and neuroscience central to human brain evolutionary studies, surveys some major recent findings, and identifies issues for future research.
This chapters defines subdivisions of the somatosensory cortex in mammals, with a focus on the anterior parietal cortex, especially in primates. Most mammals have at least five areas of the somatosensory cortex, with the primary... more
This chapters defines subdivisions of the somatosensory cortex in mammals, with a focus on the anterior parietal cortex, especially in primates. Most mammals have at least five areas of the somatosensory cortex, with the primary somatosensory cortex (S1) being the most architectonically distinct. S1 of many mammals is not uniform in histological appearance, but is instead divided into modules or patches of granular cortex that express high levels of myelin and cytochrome oxidase (CO) while being separated by septal regions that are dysgranular, poorly myelinated, and have little CO. The modules represent distinct parts of the body (digits, whiskers, etc.). Other modules in S1 of monkeys and probably other primates contain neurons that are activated by either slowly or rapidly adapting cutaneous receptors. Anthropoid primates have more areas of the anterior parietal cortex (areas 3a, 3b, 1, and 2), and more subdivisions of the lateral and the posterior parietal cortex than most mammals, although many of these areas are not architectonically distinct and well defined.
There is evidence for enlargement of association cortex in humans compared to other primate species. Expansion of temporal association cortex appears to have displaced extrastriate cortex posteriorly and inferiorly in humans compared to... more
There is evidence for enlargement of association cortex in humans compared to other primate species. Expansion of temporal association cortex appears to have displaced extrastriate cortex posteriorly and inferiorly in humans compared to macaques. However, the details of the organization of these recently expanded areas are still being uncovered. Here, we used diffusion tractography to examine the organization of extrastriate and temporal association cortex in chimpanzees, humans, and macaques. Our goal was to characterize the organization of visual and auditory association areas with respect to their corresponding primary areas (primary visual cortex and auditory core) in humans and chimpanzees. We report three results: (1) Humans, chimpanzees, and macaques show expected retinotopic organization of primary visual cortex (V1) connectivity to V2 and to areas immediately anterior to V2; (2) In contrast to macaques, chimpanzee and human V1 shows apparent connectivity with lateral, inferior, and anterior temporal regions, beyond the retinotopically organized extrastriate areas; (3) Also in contrast to macaques, chimpanzee and human auditory core shows apparent connectivity with temporal association areas, with some important differences between humans and chimpanzees. Diffusion tractography reconstructs diffusion patterns that reflect white matter organization, but does not definitively represent direct anatomical connectivity. Therefore, it is important to recognize that our findings are suggestive of species differences in long-distance white matter organization rather than demonstrations of direct connections. Our data support the conclusion that expansion of temporal association cortex, and the resulting posterior displacement of extrastriate cortex, occurred in the human lineage after its separation from the chimpanzee lineage. It is possible, however, that some expansion of the temporal lobe occurred prior to the separation of humans and chimpanzees, reflected in the reorganization of long white matter tracts in the temporal lobe that connect occipital areas to the fusiform gyrus, middle temporal gyrus, and anterior temporal lobe.
Brains come in many shapes and sizes. Nature has endowed big-brained primate species like humans with a proportionally large cerebral cortex. White matter connectivity – the brain’s infrastructure for long-range communication – might not... more
Brains come in many shapes and sizes. Nature has endowed big-brained primate species like humans with a proportionally large cerebral cortex. White matter connectivity – the brain’s infrastructure for long-range communication – might not always scale at the same pace as the cortex. We investigated the consequences of this allometric scaling for white matter brain network connectivity. Structural T1 and diffusion MRI data were collated across fourteen primate species, describing a comprehensive 350-fold range in brain volume. We report volumetric scaling relationships that point towards a restriction in macroscale connectivity in larger brains. Building on previous findings, we show cortical surface to outpace white matter volume and the corpus callosum, suggesting the emergence of a white matter ‘bottleneck’ of lower levels of connectedness through the corpus callosum in larger brains. At the network level, we find a potential consequence of this bottleneck in shaping connectivity p...
Tau pathology in Alzheimer's disease (AD) preferentially afflicts the limbic and recently enlarged association cortices, causing a progression of mnemonic and cognitive deficits. Although genetic mouse models have helped reveal... more
Tau pathology in Alzheimer's disease (AD) preferentially afflicts the limbic and recently enlarged association cortices, causing a progression of mnemonic and cognitive deficits. Although genetic mouse models have helped reveal mechanisms underlying the rare, autosomal‐dominant forms of AD, the etiology of the more common, sporadic form of AD remains unknown, and is challenging to study in mice due to their limited association cortex and lifespan. It is also difficult to study in human brains, as early‐stage tau phosphorylation can degrade postmortem. In contrast, rhesus monkeys have extensive association cortices, are long‐lived, and can undergo perfusion fixation to capture early‐stage tau phosphorylation in situ. Most importantly, rhesus monkeys naturally develop amyloid plaques, neurofibrillary tangles comprised of hyperphosphorylated tau, synaptic loss, and cognitive deficits with advancing age, and thus can be used to identify the early molecular events that initiate and p...
Behavioral traits like aggression, anxiety, and trainability differ significantly across dog breeds and are highly heritable. However, the neural bases of these differences are unknown. Here we analyzed structural MRI scans of 62 dogs in... more
Behavioral traits like aggression, anxiety, and trainability differ significantly across dog breeds and are highly heritable. However, the neural bases of these differences are unknown. Here we analyzed structural MRI scans of 62 dogs in relation to breed-average scores for the 14 major dimensions in the Canine Behavioral Assessment and Research Questionnaire, a well-validated measure of canine temperament. Several behavior categories showed significant relationships with morphologically covarying gray matter networks and regional volume changes. Networks involved in social processing and the flight-or-fight response were associated with stranger-directed fear and aggression, putatively the main behaviors under selection pressure during wolf-to-dog domestication. Trainability was significantly associated with expansion in broad regions of cortex, while fear, aggression, and other "problem" behaviors were associated with expansion in distributed subcortical regions. These results closely overlapped with regional volume changes with total brain size, in striking correspondence with models of developmental constraint on brain evolution. This suggests that the established link between dog body size and behavior is due at least in part to disproportionate enlargement of later-developing regions in larger brained dogs. We discuss how this may explain the known correlation of increasing reactivity with decreasing body size in dogs.
The development of complex cognitive functions during human evolution coincides with pronounced encephalization and expansion of white matter, the brain’s infrastructure for region-to-region communication. We investigated adaptations of... more
The development of complex cognitive functions during human evolution coincides with pronounced encephalization and expansion of white matter, the brain’s infrastructure for region-to-region communication. We investigated adaptations of the human macroscale brain network by comparing human brain wiring with that of the chimpanzee, one of our closest living primate relatives. White matter connectivity networks were reconstructed using diffusion-weighted MRI in humans ( n = 57) and chimpanzees ( n = 20) and then analyzed using network neuroscience tools. We demonstrate higher network centrality of connections linking multimodal association areas in humans compared with chimpanzees, together with a more pronounced modular topology of the human connectome. Furthermore, connections observed in humans but not in chimpanzees particularly link multimodal areas of the temporal, lateral parietal, and inferior frontal cortices, including tracts important for language processing. Network analys...
See Vértes and Seidlitz (doi:10.1093/brain/awz353) for a scientific commentary on this article.Is schizophrenia a by-product of human brain evolution? By comparing the human and chimpanzee connectomes, van den Heuvel et al. demonstrate... more
See Vértes and Seidlitz (doi:10.1093/brain/awz353) for a scientific commentary on this article.Is schizophrenia a by-product of human brain evolution? By comparing the human and chimpanzee connectomes, van den Heuvel et al. demonstrate that connections unique to the human brain show greater involvement in schizophrenia pathology. Modifications in service of higher-order brain functions may have rendered the brain more vulnerable to dysfunction.
Significance A longstanding controversy in neuroscience pertains to differences in human prefrontal cortex (PFC) compared with other primate species; specifically, is human PFC disproportionately large? Distinctively human behavioral... more
Significance A longstanding controversy in neuroscience pertains to differences in human prefrontal cortex (PFC) compared with other primate species; specifically, is human PFC disproportionately large? Distinctively human behavioral capacities related to higher cognition and affect presumably arose from evolutionary modifications since humans and great apes diverged from a common ancestor about 6–8 Mya. Accurate determination of regional differences in the amount of cortical gray and subcortical white matter content in humans, great apes, and Old World monkeys can further our understanding of the link between structure and function of the human brain. Using tissue volume analyses, we show a disproportionately large amount of gray and white matter corresponding to PFC in humans compared with nonhuman primates.
Subdivisions of the prefrontal cortex (PFC) evolved at different times. Agranular parts of the PFC emerged in early mammals, and rodents, primates, and other modern mammals share them by inheritance. These are limbic areas and include the... more
Subdivisions of the prefrontal cortex (PFC) evolved at different times. Agranular parts of the PFC emerged in early mammals, and rodents, primates, and other modern mammals share them by inheritance. These are limbic areas and include the agranular orbital cortex and agranular medial frontal cortex (areas 24, 32, and 25). Rodent research provides valuable insights into the structure, functions, and development of these shared areas, but it contributes less to parts of the PFC that are specific to primates, namely, the granular, isocortical PFC that dominates the frontal lobe in humans. The first granular PFC areas evolved either in early primates or in the last common ancestor of primates and tree shrews. Additional granular PFC areas emerged in the primate stem lineage, as represented by modern strepsirrhines. Other granular PFC areas evolved in simians, the group that includes apes, humans, and monkeys. In general, PFC accreted new areas along a roughly posterior to anterior trajectory during primate evolution. A major expansion of the granular PFC occurred in humans in concert with other association areas, with modifications of corticocortical connectivity and gene expression, although current evidence does not support the addition of a large number of new, human-specific PFC areas.
DNA methylation is a critical regulatory mechanism implicated in development, learning, memory, and disease in the human brain. Here we have elucidated DNA methylation changes during recent human brain evolution. We demonstrate dynamic... more
DNA methylation is a critical regulatory mechanism implicated in development, learning, memory, and disease in the human brain. Here we have elucidated DNA methylation changes during recent human brain evolution. We demonstrate dynamic evolutionary trajectories of DNA methylation in cell-type and cytosine-context specific manner. Specifically, DNA methylation in non-CG context, namely CH methylation, has increased (hypermethylation) in neuronal gene bodies during human brain evolution, contributing to human-specific down-regulation of genes and co-expression modules. The effects of CH hypermethylation is particularly pronounced in early development and neuronal subtypes. In contrast, DNA methylation in CG context shows pronounced reduction (hypomethylation) in human brains, notably in cis-regulatory regions, leading to upregulation of downstream genes. We show that the majority of differential CG methylation between neurons and oligodendrocytes originated before the divergence of ho...
Despite our close genetic relationship with chimpanzees, there are notable differences between chimpanzee and human social behavior. Oxytocin and vasopressin are neuropeptides involved in regulating social behavior across vertebrate taxa,... more
Despite our close genetic relationship with chimpanzees, there are notable differences between chimpanzee and human social behavior. Oxytocin and vasopressin are neuropeptides involved in regulating social behavior across vertebrate taxa, including pair bonding, social communication, and aggression, yet little is known about the neuroanatomy of these systems in primates, particularly in great apes. Here, we used receptor autoradiography to localize oxytocin and vasopressin V1a receptors, OXTR and AVPR1a respectively, in seven chimpanzee brains. OXTR binding was detected in the lateral septum, hypothalamus, medial amygdala, and substantia nigra. AVPR1a binding was observed in the cortex, lateral septum, hypothalamus, mammillary body, entire amygdala, hilus of the dentate gyrus, and substantia nigra. Chimpanzee OXTR/AVPR1a receptor distribution is compared to previous studies in several other primate species. One notable difference is the lack of OXTR in reward regions such as the ventral pallidum and nucleus accumbens in chimpanzees, whereas OXTR is found in these regions in humans. Our results suggest that in chimpanzees, like in most other anthropoid primates studied to date, OXTR has a more restricted distribution than AVPR1a, while in humans the reverse pattern has been reported. Altogether, our study provides a neuroanatomical basis for understanding the function of the oxytocin and vasopressin systems in chimpanzees.

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Understanding how human brain organization differs from that of other species is essential for understanding the neural bases of human cognitive and behavioral specializations. Nevertheless, neuroscientists have largely ignored this... more
Understanding how human brain organization differs from that of other species is essential for understanding the neural bases of human cognitive and behavioral specializations.  Nevertheless, neuroscientists have largely ignored this subject. A review of the small body of available evidence indicates that the human brain heume enormously enlarged following the divergence of humans from African apes, with association cortex expanding disproportionately. There is,
however, no evidence that humans evolved new cortical areas; indeed, a reasonable Ulie can be made that classical language areas have homologs in nonhuman primates. Humans possess morphological characteristics (sylvian-fissure asymmetries) and features of cortical histology that monkeys lack, although apes are more similar to humans in these respects. We can improve our understanding of human brain specializations by directly comparing humans. apes, and oilier nonhuman primates using the wide array of available morphological and histological techniques that do not require invasive or terminal procedures.
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"Primates are unique among mammals in possessing a region of dorsolateral prefrontal cortex with a well-developed internal gr.anular layer. This region is commonly implicated in higher cognitive functions. Despite the histological... more
"Primates are unique among mammals in possessing a region
of dorsolateral prefrontal cortex with a well-developed internal
gr.anular layer. This region is commonly implicated in higher
cognitive functions. Despite the histological distinctiveness of
primate dorsolateral prefrontal cortex, the work of Rose, Woolsey, and Akert produced a broad consensus among neuroscientists that homologues of primate granular frontal cortex exist in nonprimates and can be recognized by their dense innervation from the mediodorsal thalamic nucleus (MD). Additional characteristics have come to be identified with dorsolateral prefrontal cortex, including rich dopaminergic innervation and involvement in spatial delayed-reaction tasks.  However, recent studies reveal that these characteristics are not distinctive of the dorsolateral prefrontal region in primates: MD and dopaminergic projections are widespread in the frontal lobe, and medial and orbital frontal areas may play a role in delay tasks. A reevaluation of idt frontal cortex suggests that the medial frontal cortex, usually considered to be homologous to the dorsolateral prefrontal cortex of primates, actually consists of cortex homologous to primate premotor and anterior cingulate cortex. The lateral MD-projection cortex of rats resembles portions of primate orbital cortex. If prefrontal cortex is construed broadly enough to include orbital and cingulate cortex, rats can be said to have prefrontal cortex. However, they evidently lack homologues of the dorsolateral prefrontal areas of primates. This assessment suggests that rats probably do not provide useful models of human dorsolateral frontal lobe function and dysfunction, although they might prove valuable for understanding other regions of frontal cortex."
Most cognitive neuroscience research to date has focused on brain mechanisms. We can gain additional insights into the neural basis of cognition and action by considering how this finely tuned organ came to be, both from an evolutionary... more
Most cognitive neuroscience research to date has focused on brain mechanisms. We can gain additional insights into the neural basis of cognition and action by considering how this finely tuned organ came to be, both from an evolutionary and a developmental perspective. This article focuses primarily on developmental and evolutionary changes in higher cognitive functions, in particular the ability to reason about the world and about others’ mental states. These functions are supported by neural circuits involving prefrontal cortex, a part of the brain that has expanded over evolution and that develops slowly over childhood and adolescence in humans.
Research Interests:
Cortical neuroscience is founded on studies of a very few model organisms, mainly rats, cats, and macaque monkeys. The concentration of effort on such a few species would be defensible if cortical organization were basically uniform... more
Cortical neuroscience is founded on studies of a very few model organisms, mainly rats, cats, and macaque monkeys. The concentration of effort on such a few species would be defensible if cortical organization were basically uniform across mammals, as is commonly believed. Although there is little reason to doubt that some features of cortical organization are indeed widespread among mammals, phyletic variation in cortical organization is far more extensive than has generally been appreciated or acknowledged. Rats, for example, differ from other mammals in the genetics and chemistry of their cortical neurons, in connectivity and areal organization, and in the functions of specific cortical regions. Likewise, macaque monkeys, although widely used as models of the human visual system, lack a number of features found in human visual cortex. Given the variability of cortical organization, how should neuroscientists approach the study of nonhuman species, and what can we reasonably expect to learn from them? First, by examining a wider range of species than are currently employed, and by using modern techniques of phyletic analysis, neuroscientists can more rigorously identify those features of cortical organization that are, in fact, widely shared among mammals or among particular mammalian subgroups. Second, by taking account of variations, neuroscientists can abstract more reliable and general principles of structure-function relationships in the nervous system. Finally, freed from the doctrine of basic uniformity, neuroscientists can pursue the study of human cortical specializations, and so advance our understanding of what distinguishes humans as a biological species.
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Neuroscientists make inferences about the human brain by studying nonhuman species, an enterprise that depends on assumptions about the nature of evolution. Traditionally, many neuroscientists have supposed that all mammals possess... more
Neuroscientists make inferences about the human brain by studying nonhuman species, an enterprise that depends on assumptions about the nature of evolution.  Traditionally, many neuroscientists have supposed that all mammals possess variants of the same brain which differ only in size and degree of elaboration. Under this model, the brains of nonhuman species can be treated as simplified versions or models of the human brain. However, there is evidence thai mammalian cerebral organization is much more variable than is commonly acknowledged. The diversity of mammalian brain organization implies that neuroscientists can make better inferences about human brain organization by comparing multiple species chosen based on their evolutionary relationships to humans, than by studying individual "model" or "representative" species. The existence of neural diversity also suggests that nonhuman species have evolved cognitive specializations that are absent in humans."
Research Interests:
Research Interests:
Research Interests:
Understanding how humans differ from other animals, as well as how we are like them, requires comparative investigations. For the purpose of documenting the distinctive features of humans, the most informative research involves comparing... more
Understanding how humans differ from other animals, as well as how we are like them, requires comparative investigations. For the purpose of documenting the distinctive features of humans, the most informative research involves comparing humans to our closest relatives–the chimpanzees and other great apes. Psychology and anthropology have maintained a tradition of empirical comparative research on human specializations of cognition. The neurosciences, by contrast, have been dominated by the model-animal research paradigm, which presupposes the commonality of "basic" features of brain organization across species and discourages serious treatment of species differences. As a result, the neurosciences have made little progress in understanding human brain specializations. Recent developments in neuroimaging, genomics, and other non-invasive techniques make it possible to directly compare humans and nonhuman species at levels of organization that were previously inaccessible, offering the hope of gaining a better understanding of the species-specific features of the human brain. This hope will be dashed, however, if chimpanzees and other great ape species become unavailable for even non-invasive research.
Page 1. What's Human about the Human Brain By Todd M. Preuss From “Cognitive Neuroscience” (Gazzaniga Editor) Page 2. Outline • Homo sapiens: The undiscovered primate • Identifying human brain specializations • Continuity versus... more
Page 1. What's Human about the Human Brain By Todd M. Preuss From “Cognitive Neuroscience” (Gazzaniga Editor) Page 2. Outline • Homo sapiens: The undiscovered primate • Identifying human brain specializations • Continuity versus diversity in cerebral evolution ...
The temporal lobe is a morphological specialization of primates resulting from an expansion of higher-order visual cortex that is a hallmark of the primate brain. Among primates, humans possess a temporal lobe that has significantly... more
The temporal lobe is a morphological specialization of primates resulting from an expansion of higher-order visual cortex that is a hallmark of the primate brain. Among primates, humans possess a temporal lobe that has significantly expanded. Several uniquely human cognitive abilities, including language comprehension, semantic memory, and aspects of conceptual processing, are represented in the temporal lobe. Understanding how the temporal lobe has been modified and reorganized in the human lineage is crucial to understanding how it supports human cognitive specializations. Identifying these structural modifications requires a direct comparison with other primates, with special attention to our closest relatives, the chimpanzees. Comparative examination of data from architectonics, tract tracing, and newer imaging methodologies suggests modifications to external morphology (gyri and sulci), preferential expansion of association areas, and elaboration of white matter fasciculi, distinguishing the human temporal lobe from those of Old World monkeys. Chimpanzees and humans share some of these features of cortical expansion, although more research is needed in order to elucidate whether humans possess simply a large hominoid temporal lobe or whether important reorganization has happened since our divergence from chimpanzees.
The evolution of the human brain can be inferred from the endocasts of the skulls of extinct ancestors, which reveal the sizes and shapes of brains, and the results of comparative studies of brain organization in present-day mammals.... more
The evolution of the human brain can be inferred from the endocasts of the skulls of extinct ancestors, which reveal the sizes and shapes of brains, and the results of comparative studies of brain organization in present-day mammals. Early mammals had small brains with little neocortex and few cortical areas. The brains of early primates were different in that the visual system was greatly expanded and reorganized, and posterior parietal cortex was a large part of the brain guiding motor behaviors via an expanded motor system. Early monkeys had larger brains specialized for diurnal vision, mediated in part by an expanded temporal cortex. Early hominins had brains the size of those of great apes that became three times larger with modern humans. This large size, together with specializations of the two hemispheres and an increase in number of cortical areas, provided brain systems for language, tool use, and human cognition.
If behavior is the leading edge of evolution, and if the brain is the principal organ of behavior, one might expect the neurosciences to occupy a central place in evolutionary biology. Obviously, this is not the case—at present. Yet the... more
If behavior is the leading edge of evolution, and if the brain is the principal organ of behavior, one might expect the neurosciences to occupy a central place in evolutionary biology. Obviously, this is not the case—at present. Yet the founders of modern physical anthropology and primatology included several individuals who also made significant contributions to neuroanatomy, particularly Grafton Elliot Smith, Wilfred E. Le Gros Clark, and Raymond Dart. (Examples of these contributions include Elliot Smith, 1897, 1910, 1919; Le Gros Clark, 1932, 1941, 1956; Dart, 1934). Such a confluence of professional interests was no accident: these individuals regarded the understanding of brain evolution as crucial for understanding primate phylogeny. As Elliot Smith (1924, p. 21) put it, the facts of brain evolution are “the cement to unite into one comprehensive story the accumulations of knowledge concerning the essential facts of Man’s pedigree.” In the works of Elliot Smith and Le Gros Clark, it was the increasing complexity of the brain, a result of life in the trees, that enabled primates to become behaviorally flexible or adaptable, and so escape the narrowing adaptations that beset terrestrial mammals (see especially Elliot Smith, 1924; Le Gros Clark, 1959).
Primates are distinguished from other mammals by a number of anatomical features, including convergent, close-set orbits; enlarged eyes; digits tipped with nails rather than claws; opposable hallux; and elongated calcaneus (Cartmill,... more
Primates are distinguished from other mammals by a number of anatomical features, including convergent, close-set orbits; enlarged eyes; digits tipped with nails rather than claws; opposable hallux; and elongated calcaneus (Cartmill, 1992; Martin, 1990; Szalay et al., 1987). These shared, derived characters (synapomorphies) are generally thought to have arisen as adaptations in ancestral (stem) primates for nocturnal activity in the fine, terminal branches of trees (Martin, 1990). The behaviors that drove the evolution of primate anatomical synapomorphies remain at issue, with proposals including visually guided predation on insects and small vertebrates (Allman, 1977; Cartmill, 1972, 1974), foraging on fruits and flowers, in addition to predation (Rasmussen, 1990; Sussman, 1991), and a hindlimb-dominated “graspleaping” locomotor pattern (Szalay and Dagosto, 1988). If evolutionary history left its imprint on the primate body, what mark did it leave on the brain? Traditionally, studies of primate brain evolution have focused on changes in brain size and external morphology. Size and external morphology give little indication of evolutionary changes in internal brain organization, however, and, if modern neuroscience teaches us anything, it is
Page 436. CHAPTER 22 Reinventing Primate Neuroscience for the Twenty-First Century Todd M. Preuss The manner in which an organism perceives and responds to features of its environment reflects the state of the neural systems that make up... more
Page 436. CHAPTER 22 Reinventing Primate Neuroscience for the Twenty-First Century Todd M. Preuss The manner in which an organism perceives and responds to features of its environment reflects the state of the neural systems that make up its brain. ...
The order Primates is the group of mammals that includes the hominoids (apes and humans), Old World monkeys, New World monkeys, tarsiers, lemurs, lorises, and bush babies. Enormous progress has been made over the past three decades in... more
The order Primates is the group of mammals that includes the hominoids (apes and humans), Old World monkeys, New World monkeys, tarsiers, lemurs, lorises, and bush babies. Enormous progress has been made over the past three decades in understanding the relationships of primates to other mammals, the relationships among primate groups, and the adaptive origins of primates and of primate subgroups. Several lines of evidence indicate that primates belong to a higher-order grouping of mammals, the Archonta, that includes at least tree shrews and flying lemurs. Primates probably originated as a group of small, nocturnally active animals, evolving grasping extremities and close-set, forward-facing eyes to locomote and feed in the fine terminal branches of tree. The origin of anthropoid primates (New World monkeys, Old World monkeys, and hominoids) was marked by a shift to diurnality and the evolution of a retinal fovea for enhanced visual acuity, followed by increased body size and the advent of more complex forms of social organization Primate brain evolution was marked by changes at many levels of structural organization. Brain size increased early in primate evolution, with expansion of the neocortex and the addition of numerous new cortical sensory areas and new systems of interconnections between areas. Also, primates evolved new areas in higher-order cortical regions such as posterior parietal, superior temporal sulcal, and dorsolateral prefrontal cortex, and a new thalamic nucleus, the dorsal (medial) pulvinar, which has extensive connections with the higher-order cortex. The evolution of anthropoid primates was accompanied by further increases in brain size, and the appearance of new areas, especially in higher-order and limbic regions, although it is not clear that the addition of new areas accounts for the increased encephalization of anthropoids. Evolutionary changes in primate brain organization were by no means limited to changes in the complement of areas and extrinsic connectivity: numerous changes in the internal laminar and modular organization of cortical areas have been documented, and there is increasing evidence of changes in the morphological and biochemical phenotypes of brain cells.
Abstract The human brain enlarged enormously in evolution, especially after our genus, Homo, diverged from the australopithecines. With the development of noninvasive neuroimaging and molecular biological techniques we can for the first... more
Abstract The human brain enlarged enormously in evolution, especially after our genus, Homo, diverged from the australopithecines. With the development of noninvasive neuroimaging and molecular biological techniques we can for the first time compare the internal organization of human brains to those of other primates, including our closest relatives, the chimpanzees. These studies reveal that most of the enlargement of the human brain was due to the expansion of the association cortex, the critical substrate for higher-order cognition. Association cortex enlargement was accompanied by extensive modification of the connections linking cortical areas into functional networks, as shown in investigations of the language and tool-manipulation systems. Surprisingly, there is no clear evidence to support the popular view that the human brain contains a large number of new cortical areas. Perhaps even more surprising is the evidence that humans possess extensive specializations at finer levels of brain organization, including cell morphology, biochemistry, and physiology.
This chapters defines subdivisions of the somatosensory cortex in mammals, with a focus on the anterior parietal cortex, especially in primates. Most mammals have at least five areas of the somatosensory cortex, with the primary... more
This chapters defines subdivisions of the somatosensory cortex in mammals, with a focus on the anterior parietal cortex, especially in primates. Most mammals have at least five areas of the somatosensory cortex, with the primary somatosensory cortex (S1) being the most architectonically distinct. S1 of many mammals is not uniform in histological appearance, but is instead divided into modules or patches of granular cortex that express high levels of myelin and cytochrome oxidase (CO) while being separated by septal regions that are dysgranular, poorly myelinated, and have little CO. The modules represent distinct parts of the body (digits, whiskers, etc.). Other modules in S1 of monkeys and probably other primates contain neurons that are activated by either slowly or rapidly adapting cutaneous receptors. Anthropoid primates have more areas of the anterior parietal cortex (areas 3a, 3b, 1, and 2), and more subdivisions of the lateral and the posterior parietal cortex than most mammals, although many of these areas are not architectonically distinct and well defined.