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1.  Biochemical specificity of von Economo neurons in hominoids 
Von Economo neurons (VENs) are defined by their thin, elongated cell body and long dendrites projecting from apical and basal ends. These distinctive neurons are mostly present in anterior cingulate (ACC) and fronto-insular (FI) cortex, with particularly high densities in cetaceans, elephants, and hominoid primates (i.e., humans and apes). This distribution suggests that VENs contribute to specializations of neural circuits in species that share both large brain size and complex social cognition, possibly representing an adaptation to rapidly relay socially-relevant information over long distances across the brain. Recent evidence indicates that unique patterns of protein expression may also characterize VENs, particularly involving molecules that are known to regulate gut and immune function. In this study, we used quantitative stereologic methods to examine the expression of three such proteins that are localized in VENs – activating-transcription factor 3 (ATF3), interleukin 4 receptor (IL4Rα) and neuromedin B (NMB). We quantified immunoreactivity against these proteins in different morphological classes of ACC layer V neurons of hominoids. Among the different neuron types analyzed (pyramidal, VEN, fork, enveloping, and other multipolar), VENs showed the greatest percentage that displayed immunostaining. Additionally, a higher proportion of VENs in humans were immunoreactive to ATF3, IL4Rα, and NMB than in other apes. No other ACC layer V neuron type displayed a significant species difference in the percentage of immunoreactive neurons. These findings demonstrate that phylogenetic variation exists in the protein expression profile of VENs, suggesting that humans might have evolved biochemical specializations for enhanced interoceptive sensitivity.
PMCID: PMC3004764  PMID: 21140465
brain; evolution; ape; human; neuron
2.  Broca's Area Homologue in Chimpanzees (Pan troglodytes): Probabilistic Mapping, Asymmetry, and Comparison to Humans 
Cerebral Cortex (New York, NY)  2009;20(3):730-742.
Neural changes that occurred during human evolution to support language are poorly understood. As a basis of comparison to humans, we used design-based stereological methods to estimate volumes, total neuron numbers, and neuron densities in Brodmann's areas 44 and 45 in both cerebral hemispheres of 12 chimpanzees (Pan troglodytes), one of our species’ closest living relatives. We found that the degree of interindividual variation in the topographic location and quantitative cytoarchitecture of areas 44 and 45 in chimpanzees was comparable to that seen in humans from previous studies. However, in contrast to the documented asymmetries in humans, we did not find significant population-level hemispheric asymmetry for any measures of areas 44 and 45 in chimpanzees. Furthermore, there was no relationship between asymmetries of stereological data and magnetic resonance imaging–based measures of inferior frontal gyrus morphology or hand preference on 2 different behavioral tasks. These findings suggest that Broca's area in the left hemisphere expanded in relative size during human evolution, possibly as an adaptation for our species’ language abilities.
PMCID: PMC2820707  PMID: 19620620
cytoarchitecture; evolution; great ape; handedness; stereology
3.  Histological Asymmetries of Primary Motor Cortex Predict Handedness in Chimpanzees (Pan troglodytes) 
Like humans, chimpanzees display robust and consistent hand preferences during the performance of certain tasks. Although correlations have been demonstrated between gross anatomic measures of primary motor cortex asymmetry and handedness in captive chimpanzees, the relationship between histological architecture and behavioral lateralization has not yet been investigated. Therefore, we examined interhemispheric asymmetry of several different microstructural characteristics of the primary motor cortex in the region of hand representation from 18 chimpanzees tested on a coordinated bimanual task before death. At the population level our data showed leftward bias for higher layer II/III neuron density. Of note, however, there was no population-level asymmetry in the areal fraction of Nissl-stained cell bodies, a finding that differs from previous studies of this cortical region in humans. Nonetheless, we found that asymmetry in the density of layer II/III parvalbumin-immunoreactive interneurons was the best predictor of individual hand preference. These results suggest that histological asymmetries are related to handedness in chimpanzees, while overall patterns of asymmetry at the population level might differ from humans.
PMCID: PMC2680156  PMID: 17534947
primary motor cortex; handedness; interneuron; parvalbumin; brain evolution
4.  Modular structure facilitates mosaic evolution of the brain in chimpanzees and humans 
Nature communications  2014;5:4469.
Different brain components can evolve in a coordinated fashion or they can show divergent evolutionary trajectories according to a mosaic pattern of variation. Understanding the relationship between these brain evolutionary patterns, which are not mutually exclusive, can be informed by the examination of intraspecific variation. Our study evaluates patterns of brain anatomical covariation in chimpanzees and humans to infer their influence on brain evolution in the hominin clade. We show that chimpanzee and human brains have a modular structure that may have facilitated mosaic evolution from their last common ancestor. Spatially adjacent regions covary with one another to the strongest degree and separated regions are more independent from each other, which might be related to a predominance of local association connectivity. Despite the undoubted importance of developmental and functional factors in determining brain morphology, we find that these constraints are subordinate to the primary effect of local spatial interactions.
PMCID: PMC4144426  PMID: 25047085
5.  Developmental changes in the spatial organization of neurons in the neocortex of humans and common chimpanzees 
The Journal of comparative neurology  2013;521(18):4249-4259.
In adult humans, the prefrontal cortex possesses wider minicolumns and more neuropil space than other cortical regions. These aspects of prefrontal cortex architecture, furthermore, are increased in comparison to chimpanzees and other great apes. In order to determine the developmental appearance of this human cortical specialization, we examined the spatial organization of neurons in four cortical regions (frontal pole [Brodmann’s area 10], primary motor [area 4], primary somatosensory [area 3b], and prestriate visual cortex [area 18]) in chimpanzees and humans from birth to approximately the time of adolescence (11 years of age). Horizontal spacing distance (HSD) and gray level ratio (GLR) of layer III neurons were measured in Nissl-stained sections. In both human and chimpanzee area 10, HSD was significantly higher in the post-weaning specimens compared to the pre-weaning ones. No significant age-related differences were seen in the other regions in either species. In concert with other recent studies, the current findings suggest that there is a relatively slower maturation of area 10 in both humans and chimpanzees as compared to other cortical regions, and that further refinement of the spatial organization of neurons within this prefrontal area in humans takes place after the post-weaning periods included here.
PMCID: PMC4041080  PMID: 23839595
minicolumn; evolution; comparative neuroanatomy; biological anthropology
6.  Dendritic Morphology of Pyramidal Neurons in the Chimpanzee Neocortex: Regional Specializations and Comparison to Humans 
Cerebral Cortex (New York, NY)  2012;23(10):2429-2436.
The primate cerebral cortex is characterized by regional variation in the structure of pyramidal neurons, with more complex dendritic arbors and greater spine density observed in prefrontal compared with sensory and motor cortices. Although there are several investigations in humans and other primates, virtually nothing is known about regional variation in the morphology of pyramidal neurons in the cerebral cortex of great apes, humans' closest living relatives. The current study uses the rapid Golgi stain to quantify the dendritic structure of layer III pyramidal neurons in 4 areas of the chimpanzee cerebral cortex: Primary somatosensory (area 3b), primary motor (area 4), prestriate visual (area 18), and prefrontal (area 10) cortex. Consistent with previous studies in humans and macaque monkeys, pyramidal neurons in the prefrontal cortex of chimpanzees exhibit greater dendritic complexity than those in other cortical regions, suggesting that prefrontal cortical evolution in primates is characterized by increased potential for integrative connectivity. Compared with chimpanzees, the pyramidal neurons of humans had significantly longer and more branched dendritic arbors in all cortical regions.
PMCID: PMC3767963  PMID: 22875862
area 10; dendrites; evolution; Golgi; primate cerebral cortex
7.  Increased morphological asymmetry, evolvability and plasticity in human brain evolution 
The study of hominin brain evolution relies mostly on evaluation of the endocranial morphology of fossil skulls. However, only some general features of external brain morphology are evident from endocasts, and many anatomical details can be difficult or impossible to examine. In this study, we use geometric morphometric techniques to evaluate inter- and intraspecific differences in cerebral morphology in a sample of in vivo magnetic resonance imaging scans of chimpanzees and humans, with special emphasis on the study of asymmetric variation. Our study reveals that chimpanzee–human differences in cerebral morphology are mainly symmetric; by contrast, there is continuity in asymmetric variation between species, with humans showing an increased range of variation. Moreover, asymmetric variation does not appear to be the result of allometric scaling at intraspecific levels, whereas symmetric changes exhibit very slight allometric effects within each species. Our results emphasize two key properties of brain evolution in the hominine clade: first, evolution of chimpanzee and human brains (and probably their last common ancestor and related species) is not strongly morphologically constrained, thus making their brains highly evolvable and responsive to selective pressures; second, chimpanzee and, especially, human brains show high levels of fluctuating asymmetry indicative of pronounced developmental plasticity. We infer that these two characteristics can have a role in human cognitive evolution.
PMCID: PMC3652445  PMID: 23615289
chimpanzee; hominin; EvoDevo; geometric morphometrics; neuroanatomy
8.  Exceptional Evolutionary Divergence of Human Muscle and Brain Metabolomes Parallels Human Cognitive and Physical Uniqueness 
PLoS Biology  2014;12(5):e1001871.
Accelerated evolution of the human brain and muscle metabolomes reflects our unique cognitive and physical capacities.
Metabolite concentrations reflect the physiological states of tissues and cells. However, the role of metabolic changes in species evolution is currently unknown. Here, we present a study of metabolome evolution conducted in three brain regions and two non-neural tissues from humans, chimpanzees, macaque monkeys, and mice based on over 10,000 hydrophilic compounds. While chimpanzee, macaque, and mouse metabolomes diverge following the genetic distances among species, we detect remarkable acceleration of metabolome evolution in human prefrontal cortex and skeletal muscle affecting neural and energy metabolism pathways. These metabolic changes could not be attributed to environmental conditions and were confirmed against the expression of their corresponding enzymes. We further conducted muscle strength tests in humans, chimpanzees, and macaques. The results suggest that, while humans are characterized by superior cognition, their muscular performance might be markedly inferior to that of chimpanzees and macaque monkeys.
Author Summary
Physiological processes that maintain our tissues' functionality involve the generation of multiple products and intermediates known as metabolites—small molecules with a weight of less than 1,500 Daltons. Changes in concentrations of these metabolites are thought to be closely related to changes in phenotype. Here, we assessed concentrations of more than 10,000 metabolites in three brain regions and two non-neural tissues (skeletal muscle and kidney) of humans, chimpanzees, macaque monkeys, and mice using mass spectrometry-based approaches. We found that the evolution of the metabolome largely reflects genetic divergence between species and is not greatly affected by environmental factors. In the human lineage, however, we observed an exceptional acceleration of metabolome evolution in the prefrontal cortical region of the brain and in skeletal muscle. Based on additional behavioral tests, we further show that metabolic changes in human muscle seem to be paralleled by a drastic reduction in muscle strength. The observed rapid metabolic changes in brain and muscle, together with the unique human cognitive skills and low muscle performance, might reflect parallel mechanisms in human evolution.
PMCID: PMC4035273  PMID: 24866127
9.  NSF Workshop Report: Discovering General Principles of Nervous System Organization by Comparing Brain Maps across Species 
Efforts to understand nervous system structure and function have received new impetus from the federal Brain Research through Advancing Innovative Neurotechnologies (BRAIN) Initiative. Comparative analyses can contribute to this effort by leading to the discovery of general principles of neural circuit design, information processing, and gene-structure-function relationships that are not apparent from studies on single species. We here propose to extend the comparative approach to nervous system ‘maps’ comprising molecular, anatomical, and physiological data. This research will identify which neural features are likely to generalize across species, and which are unlikely to be broadly conserved. It will also suggest causal relationships between genes, development, adult anatomy, physiology, and, ultimately, behavior. These causal hypotheses can then be tested experimentally. Finally, insights from comparative research can inspire and guide technological development. To promote this research agenda, we recommend that teams of investigators coalesce around specific research questions and select a set of ‘reference species’ to anchor their comparative analyses. These reference species should be chosen not just for practical advantages, but also with regard for their phylogenetic position, behavioral repertoire, well-annotated genome, or other strategic reasons. We envision that the nervous systems of these reference species will be mapped in more detail than those of other species. The collected data may range from the molecular to the behavioral, depending on the research question. To integrate across levels of analysis and across species, standards for data collection, annotation, archiving, and distribution must be developed and respected. To that end, it will help to form networks or consortia of researchers and centers for science, technology, and education that focus on organized data collection, distribution, and training. These activities could be supported, at least in part, through existing mechanisms at NSF, NIH, and other agencies. It will also be important to develop new integrated software and database systems for cross-species data analyses. Multidisciplinary efforts to develop such analytical tools should be supported financially. Finally, training opportunities should be created to stimulate multidisciplinary, integrative research into brain structure, function, and evolution.
PMCID: PMC4028317  PMID: 24603302
10.  Neuropeptide Y-immunoreactive neurons in the cerebral cortex of humans and other haplorrhine primates 
American journal of primatology  2012;75(5):415-424.
We examined the distribution of neurons immunoreactive for neuropeptide Y (NPY) in the posterior part of the superior temporal cortex (Brodmann's area 22 or area Tpt) of humans and nonhuman haplorrhine primates. NPY has been implicated in learning and memory and the density of NPY-expressing cortical neurons and axons is reduced in depression, bipolar disorder, schizophrenia, and Alzheimer's disease. Due to the role that NPY plays in both cognition and neurodegenerative diseases, we tested the hypothesis that the density of cortical and interstitial neurons expressing NPY was increased in humans relative to other primate species. The study sample included great apes (chimpanzee and gorilla), Old World monkeys (pigtailed macaque, moor macaque, and baboon) and New World monkeys (squirrel monkey and capuchin). Stereologic methods were used to estimate the density of NPY-immunoreactive (-ir) neurons in layers I-VI of area Tpt and the subjacent white matter. Adjacent Nissl-stained sections were used to calculate local densities of all neurons. The ratio of NPY-ir neurons to total neurons within area Tpt and the total density of NPY-ir neurons within the white matter were compared among species. Overall, NPY-ir neurons represented only an average of 0.006% of the total neuron population. While there were significant differences among species, phylogenetic trends in NPY-ir neuron distributions were not observed and humans did not differ from other primates. However, variation among species warrants further investigation into the distribution of this neuromodulator system.
PMCID: PMC3560302  PMID: 23042407
Wernicke's area; area Tpt; area 22; evolution; NPY
11.  A volumetric comparison of the insular cortex and its subregions in primates 
Journal of human evolution  2013;64(4):263-279.
The neuronal composition of the insula in primates displays a gradient, transitioning from granular neocortex in the posterior-dorsal insula to agranular neocortex in the anterior-ventral insula with an intermediate zone of dysgranularity. Additionally, apes and humans exhibit a distinctive subdomain in the agranular insula, the frontoinsular cortex (FI), defined by the presence of clusters of von Economo neurons (VENs). Studies in humans indicate that the ventral anterior insula, including agranular insular cortex and FI, is involved in social awareness, and that the posterodorsal insula, including granular and dysgranular cortices, produces an internal representation of the body’s homeostatic state. We examined the volumes of these cytoarchitectural areas of insular cortex in 30 primate species, including the volume of FI in apes and humans. Results indicate that the whole insula scales hyperallometrically (exponent = 1.13) relative to total brain mass, and the agranular insula (including FI) scales against total brain mass with even greater positive allometry (exponent = 1.23), providing a potential neural basis for enhancement of social cognition in association with increased brain size. The relative volumes of the subdivisions of the insular cortex, after controlling for total brain volume, are not correlated with species typical social group size. Although its size is predicted by primate-wide allometric scaling patterns, we found that the absolute volume of the left and right agranular insula and left FI are among the most differentially expanded of the human cerebral cortex compared to our closest living relative, the chimpanzee.
PMCID: PMC3756831  PMID: 23466178
Allometry; Brain; Evolution; Frontoinsular cortex; Hominoids
12.  Lamination of the Lateral Geniculate Nucleus of Catarrhine Primates 
Brain, behavior and evolution  2013;81(2):93-108.
The lateral geniculate nucleus (LGN) of catarrhines – with the exception of gibbons – is typically described as a six-layered structure, comprised of two ventral magnocellular layers, and four dorsal parvocellular layers. The parvocellular layers of the LGN are involved in color vision. Therefore, it is hypothesized that a six-layered LGN is a shared-derived trait among catarrhines. This might suggest that in gibbons the lack of further subdivisions of the parvocellular layers is a recent change, and could be related to specializations of visual information processing in this taxon. To address these hypotheses, the lamination of the LGN was investigated in a range of catarrhine species, including several taxa not previously described, and the evolution of the LGN was reconstructed using phylogenetic information. The findings indicate that while all catarrhine species have four parvocellular leaflets, two main patterns of LGN parvocellular lamination occur: two undivided parvocellular layers in some species, and four parvocellular leaflets (with occasional subleaflets) in other species. LGN size was not found to be related to lamination pattern. Both patterns were found to occur in divergent clades, which is suggestive of homoplasy within the catarrhines in LGN morphology.
PMCID: PMC3741618  PMID: 23467282
evolution; phylogeny; catarrhines; primates; vision; lateral geniculate nucleus; parvocellular
13.  New insights into the classification and nomenclature of cortical GABAergic interneurons 
Nature reviews. Neuroscience  2013;14(3):202-216.
A systematic classification and accepted nomenclature of neuron types is much needed but is currently lacking. This article describes a possible taxonomical solution for classifying GABAergic interneurons of the cerebral cortex based on a novel, web-based interactive system that allows experts to classify neurons with pre-determined criteria. Using Bayesian analysis and clustering algorithms on the resulting data, we investigated the suitability of several anatomical terms and neuron names for cortical GABAergic interneurons. Moreover, we show that supervised classification models could automatically categorize interneurons in agreement with experts’ assignments. These results demonstrate a practical and objective approach to the naming, characterization and classification of neurons based on community consensus.
PMCID: PMC3619199  PMID: 23385869
14.  Humans and great apes share increased neocortical neuropeptide Y innervation compared to other haplorhine primates 
Neuropeptide Y (NPY) plays a role in a variety of basic physiological functions and has also been implicated in regulating cognition, including learning and memory. A decrease in neocortical NPY has been reported for Alzheimer's disease, schizophrenia, bipolar disorder, and depression, potentially contributing to associated cognitive deficits. The goal of the present analysis was to examine variation in neocortical NPY-immunoreactive axon and varicosity density among haplorhine primates (monkeys, apes, and humans). Stereologic methods were used to measure the ratios of NPY-expressing axon length density to total neuron density (ALv/Nv) and NPY-immunoreactive varicosity density to neuron density (Vv/Nv), as well as the mean varicosity spacing in neocortical areas 10, 24, 44, and 22 (Tpt) of humans, African great apes, New World monkeys, and Old World monkeys. Humans and great apes showed increased cortical NPY innervation relative to monkey species for ALv/Nv and Vv/Nv. Furthermore, humans and great apes displayed a conserved pattern of varicosity spacing across cortical areas and layers, with no differences between cortical layers or among cortical areas. These phylogenetic differences may be related to shared life history variables and may reflect specific cognitive abilities.
PMCID: PMC3937817  PMID: 24616688
NPY; Broca's area; Wernicke's area; primate evolution
15.  Comparative neuronal morphology of the cerebellar cortex in afrotherians, carnivores, cetartiodactyls, and primates 
Although the basic morphological characteristics of neurons in the cerebellar cortex have been documented in several species, virtually nothing is known about the quantitative morphological characteristics of these neurons across different taxa. To that end, the present study investigated cerebellar neuronal morphology among eight different, large-brained mammalian species comprising a broad phylogenetic range: afrotherians (African elephant, Florida manatee), carnivores (Siberian tiger, clouded leopard), cetartiodactyls (humpback whale, giraffe) and primates (human, common chimpanzee). Specifically, several neuron types (e.g., stellate, basket, Lugaro, Golgi, and granule neurons; N = 317) of the cerebellar cortex were stained with a modified rapid Golgi technique and quantified on a computer-assisted microscopy system. There was a 64-fold variation in brain mass across species in our sample (from clouded leopard to the elephant) and a 103-fold variation in cerebellar volume. Most dendritic measures tended to increase with cerebellar volume. The cerebellar cortex in these species exhibited the trilaminate pattern common to all mammals. Morphologically, neuron types in the cerebellar cortex were generally consistent with those described in primates (Fox et al., 1967) and rodents (Palay and Chan-Palay, 1974), although there was substantial quantitative variation across species. In particular, Lugaro neurons in the elephant appeared to be disproportionately larger than those in other species. To explore potential quantitative differences in dendritic measures across species, MARSplines analyses were used to evaluate whether species could be differentiated from each other based on dendritic characteristics alone. Results of these analyses indicated that there were significant differences among all species in dendritic measures.
PMCID: PMC4005950  PMID: 24795574
dendrite; morphometry; Golgi method; brain evolution; cerebellum
16.  Comparative organization of the claustrum: what does structure tell us about function? 
The claustrum is a subcortical nucleus present in all placental mammals. Many anatomical studies have shown that its inputs are predominantly from the cerebral cortex and its outputs are back to the cortex. This connectivity thus suggests that the claustrum serves to amplify or facilitate information processing in the cerebral cortex. The size and the complexity of the cerebral cortex varies dramatically across species. Some species have lissencephalic brains, with few cortical areas, while others have a greatly expanded cortex and many cortical areas. This evolutionary diversity in the cerebral cortex raises several questions about the claustrum. Does its volume expand in coordination with the expansion of cortex and does it acquire new functions related to the new cortical functions? Here we survey the organization of the claustrum in animals with large brains, including great apes and cetaceans. Our data suggest that the claustrum is not always a continuous structure. In monkeys and gorillas there are a few isolated islands of cells near the main body of the nucleus. In cetaceans, however, there are many isolated cell islands. These data suggest constraints on the possible function of the claustrum. Some authors propose that the claustrum has a more global role in perception or consciousness that requires intraclaustral integration of information. These theories postulate mechanisms like gap junctions between claustral cells or a “syncytium” to mediate intraclaustral processing. The presence of discontinuities in the structure of the claustrum, present but minimal in some primates, but dramatically clear in cetaceans, argues against the proposed mechanisms of intraclaustral processing of information. The best interpretation of function, then, is that each functional subdivision of the claustrum simply contributes to the function of its cortical partner.
PMCID: PMC4079070  PMID: 25071474
gorilla; whale; dolphin; calcium-binding proteins; visual cortex
18.  Planum Temporale Asymmetries Correlate with Corpus Callosum Axon Fiber Density in Chimpanzees (Pan troglodytes) 
Behavioural brain research  2012;234(2):248-254.
The corpus callosum (CC) is the major white matter tract that connects the two cerebral hemispheres. Some have theorized that individual differences in behavioral and brain asymmetries are linked to variation in the density of axon fibers that traverse different sections of the CC. In this study, we examined whether variation in axon fiber density in the CC was associated with variation in asymmetries in the planum temporale (PT) in a sample of 20 post-mortem chimpanzee brains. We further tested for sex differences in small and large CC fiber proportions and density in the chimpanzees. We found that the distribution of small and large fibers within the CC of chimpanzees follows a similar pattern to those reported in humans. We also found that chimpanzees with larger asymmetries in the PT had fewer large fibers in the posterior portion of the CC, particularly among females. As has been reported in human brains, the findings reported here indicate that individual differences in brain asymmetries are associated with variation in interhemispheric connectivity as manifest in axon fiber density and size.
PMCID: PMC3422564  PMID: 22766214
Chimpanzees; brain asymmetry; corpus callosum; axon fiber density; planum temporale
19.  Neuropil distribution in the cerebral cortex differs between humans and chimpanzees 
The Journal of comparative neurology  2012;520(13):2917-2929.
Increased connectivity of higher-order association regions in the neocortex has been proposed as a defining feature of human brain evolution. At present, however, there are limited comparative data to examine this claim fully. We tested the hypothesis that the distribution of neuropil across areas of the neocortex of humans differs from that of one of our closest living relatives, the common chimpanzee. The neuropil provides a proxy measure of total connectivity within a local region because it is comprised mostly of dendrites, axons, and synapses. Using image analysis techniques, we quantified the neuropil fraction from both hemispheres in six cytoarchitectonically defined regions including frontopolar cortex (area 10), Broca’s area (area 45), frontoinsular cortex (area FI), primary motor cortex (area 4), primary auditory cortex (area 41/42), and the planum temporale (area 22). Our results demonstrate that humans exhibit a unique distribution of neuropil in the neocortex compared to chimpanzees. In particular, the human frontopolar cortex and the frontoinsular cortex had a significantly higher neuropil fraction than the other areas. In chimpanzees these prefrontal regions did not display significantly more neuropil, but the primary auditory cortex had a lower neuropil fraction than other areas. Our results support the conclusion that enhanced connectivity in the prefrontal cortex accompanied the evolution of the human brain. These species differences in neuropil distribution may offer insight into the neural basis of human cognition, reflecting enhancement of the integrative capacity of the prefrontal cortex.
PMCID: PMC3556724  PMID: 22350926
cytoarchitecture; evolution; brain; asymmetry
20.  Age-Related Differences in Corpus Callosum Area of Capuchin Monkeys 
Neuroscience  2011;202:202-208.
Capuchin monkeys (Cebus apella) are New World primates with relatively large brains for their body size. The developmental trajectories of several brain regions – including cortical white matter, frontal lobe white matter, and basal ganglia nuclei – are similar to humans. Additionally, capuchins have independently evolved several behavioral and anatomical characteristics in common with humans and chimpanzees – including complex manipulative abilities, use of tools, and the use of precision grips – making them interesting species for studies of comparative brain morphology and organization. Here we report the first investigation into the development of the corpus callosum and its regional subdivisions in capuchins. Corpus callosum development was quantified using high-resolution structural MRI images from 39 socially reared subjects (male n = 22; female n = 18) ranging in age from 4 days (infancy) – 20 years (middle adulthood). The total area of the corpus callosum and the subdivisions of the genu, rostral midbody, medial midbody, caudal midbody, and splenium were traced from the midsagittal section. Total corpus callosum area displayed significant differences across this time span and was best explained by quadratic growth. Sustained linear growth was observed in the subdivisions of the genu, rostral midbody, and splenium; sustained quadratic growth was seen in the subdivision of the medial midbody. Differences in growth were not detected in the subdivision of the caudal midbody. Females had a larger raw area of the total CC and of the medial midbody and caudal midbody throughout the lifespan. Our results indicate that capuchins show continued white matter development beyond adolescence in regions related to cognitive and motor development.
PMCID: PMC3293371  PMID: 22173013
brain development; Cebus; corpus callosum
21.  Dynamic Gene Expression in the Human Cerebral Cortex Distinguishes Children from Adults 
PLoS ONE  2012;7(5):e37714.
In comparison with other primate species, humans have an extended juvenile period during which the brain is more plastic. In the current study we sought to examine gene expression in the cerebral cortex during development in the context of this adaptive plasticity. We introduce an approach designed to discriminate genes with variable as opposed to uniform patterns of gene expression and found that greater inter-individual variance is observed among children than among adults. For the 337 transcripts that show this pattern, we found a significant overrepresentation of genes annotated to the immune system process (pFDR≅0). Moreover, genes known to be important in neuronal function, such as brain-derived neurotrophic factor (BDNF), are included among the genes more variably expressed in childhood. We propose that the developmental period of heightened childhood neuronal plasticity is characterized by more dynamic patterns of gene expression in the cerebral cortex compared to adulthood when the brain is less plastic. That an overabundance of these genes are annotated to the immune system suggests that the functions of these genes can be thought of not only in the context of antigen processing and presentation, but also in the context of nervous system development.
PMCID: PMC3364291  PMID: 22666384
22.  Correlated evolution of brain regions involved in producing and processing facial expressions in anthropoid primates 
Biology Letters  2010;7(1):86-88.
Anthropoid primates are distinguished from other mammals by having relatively large primary visual cortices (V1) and complex facial expressions. We present a comparative test of the hypothesis that facial expression processing coevolved with the expansion of V1 in anthropoids. Previously published data were analysed using phylogenetic comparative methods. The results of our study suggest a pattern of correlated evolution linking social group size, facial motor control and cortical visual processing in catarrhines, but not platyrrhines. Catarrhines that live in relatively large social groups tended to have relatively large facial motor nuclei, and relatively large primary visual cortices. We conclude that catarrhine brains are adapted for producing and processing complex facial displays.
PMCID: PMC3030864  PMID: 20591852
brain evolution; facial motor nucleus; neocortex; face perception
23.  The Development of the Basal Ganglia in Capuchin Monkeys (Cebus apella) 
Brain research  2010;1329:82-88.
The basal ganglia are subcortical structures involved in the planning, initiation and regulation of movement as well as a variety of non-motor, cognitive and affective functions. Capuchin monkeys share several important characteristics of development with humans, including a prolonged infancy and juvenile period, a long lifespan, and complex manipulative abilities. This makes capuchins important comparative models for understanding age-related neuroanatomical changes in these structures. Here we report developmental volumetric data on the three subdivisions of the basal ganglia, the caudate, putamen and globus pallidus in brown capuchin monkeys (Cebus apella). Based on a cross-sectional sample, we describe brain development in 28 brown capuchin monkeys (male n = 17, female n = 11; age range = 2 months – 20 years) using high-resolution structural MRI. We found that the raw volumes of the putamen and caudate varied significantly with age, decreasing in volume from birth through early adulthood. Notably, developmental changes did not differ between sexes. Because these observed developmental patterns are similar to humans, our results suggest that capuchin monkeys may be useful animal models for investigating neurodevelopmental disorders of the basal ganglia.
PMCID: PMC3233974  PMID: 20227397
brain development; basal ganglia; Cebus
24.  A Voxel-Based Morphometry Analysis of White Matter Asymmetries in Chimpanzees (Pan troglodytes) 
Brain, Behavior and Evolution  2010;76(2):93-100.
Voxel-based morphometry (VBM) has become an increasingly common method for assessing neuroanatomical asymmetries in human in vivo magnetic resonance imaging (MRI). Here, we employed VBM to examine asymmetries in white matter in a sample of 48 chimpanzees (15 males and 33 females). T1-weighted MRI scans were segmented into white matter using FSL and registered to a common template. The segmented volumes were then flipped in the left-right axis and registered back to the template. The mirror image white matter volumes were then subtracted from the correctly oriented volumes and voxel-by-voxel t tests were performed. Twenty-seven significant lateralized clusters were found, including 18 in the left hemisphere and 9 in the right hemisphere. Several of the asymmetries were found in regions corresponding to well-known white matter tracts including the superior longitudinal fasciculus, inferior longitudinal fasciculus and corticospinal tract.
PMCID: PMC3202944  PMID: 20881357
Chimpanzees; Brain asymmetry; White matter; Language evolution
25.  Cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: A comparative study 
Neuroscience  2008;155(1):203-220.
In this study, we assessed the possibility that humans differ from other primate species in the supply of dopamine to the frontal cortex. To this end, quantitative comparative analyses were performed among humans, chimpanzees, and macaques using immunohistochemical methods to visualize tyrosine hydroxylase-immunoreactive axons within the cerebral cortex. Axon densities and neuron densities were quantified using computer-assisted stereology. Areas 9 and 32 were chosen for evaluation due to their roles in higher-order executive functions and theory of mind, respectively. Primary motor cortex (area 4) was also evaluated because it is not directly associated with cognition. We did not find an overt quantitative increase in cortical dopaminergic innervation in humans relative to the other primates examined. However, several differences in cortical dopaminergic innervation were observed among species which may have functional implications. Specifically, humans exhibited a sublaminar pattern of innervation in layer I of areas 9 and 32 that differed from that of macaques and chimpanzees. Analysis of axon length density to neuron density among species revealed that humans and chimpanzees together deviated from macaques in having increased dopaminergic afferents in layers III and V/VI of areas 9 and 32, but there were no phylogenetic differences in area 4. Finally, morphological specializations of axon coils that may be indicative of cortical plasticity events were observed in humans and chimpanzees, but not macaques. Our findings suggest significant modifications of dopamine’s role in cortical organization occurred in the evolution of the apes, with further changes in the descent of humans.
PMCID: PMC3177596  PMID: 18562124
tyrosine hydroxylase; prefrontal cortex; area 9; area 32; area 4; human evolution

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