Publications by authors named "William D Hopkins"

213 Publications

Comparative analysis reveals distinctive epigenetic features of the human cerebellum.

PLoS Genet 2021 May 6;17(5):e1009506. Epub 2021 May 6.

Department of Anthropology and Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, District of Columbia, United States of America.

Identifying the molecular underpinnings of the neural specializations that underlie human cognitive and behavioral traits has long been of considerable interest. Much research on human-specific changes in gene expression and epigenetic marks has focused on the prefrontal cortex, a brain structure distinguished by its role in executive functions. The cerebellum shows expansion in great apes and is gaining increasing attention for its role in motor skills and cognitive processing, including language. However, relatively few molecular studies of the cerebellum in a comparative evolutionary context have been conducted. Here, we identify human-specific methylation in the lateral cerebellum relative to the dorsolateral prefrontal cortex, in a comparative study with chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). Specifically, we profiled genome-wide methylation levels in the three species for each of the two brain structures and identified human-specific differentially methylated genomic regions unique to each structure. We further identified which differentially methylated regions (DMRs) overlap likely regulatory elements and determined whether associated genes show corresponding species differences in gene expression. We found greater human-specific methylation in the cerebellum than the dorsolateral prefrontal cortex, with differentially methylated regions overlapping genes involved in several conditions or processes relevant to human neurobiology, including synaptic plasticity, lipid metabolism, neuroinflammation and neurodegeneration, and neurodevelopment, including developmental disorders. Moreover, our results show some overlap with those of previous studies focused on the neocortex, indicating that such results may be common to multiple brain structures. These findings further our understanding of the cerebellum in human brain evolution.
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http://dx.doi.org/10.1371/journal.pgen.1009506DOI Listing
May 2021

Age- and cognition-related differences in the gray matter volume of the chimpanzee brain (Pan troglodytes): A voxel-based morphometry and conjunction analysis.

Am J Primatol 2021 Apr 26:e23264. Epub 2021 Apr 26.

Department of Comparative Medicine, The University of Texas MD Anderson Cancer Center, Bastrop, Texas, USA.

Several primate species have been shown to exhibit age-related changes in cognition, brain, and behavior. However, severe neurodegenerative illnesses, such as Alzheimer's disease (AD), were once thought to be uniquely human. Recently, some chimpanzees naturally were documented to develop both neurofibrillary tangles and amyloid plaques, the main characteristics of AD pathology. In addition, like humans and other primates, chimpanzees show similar declines in cognition and motor function with age. Here, we used voxel-based morphometry to examine the relationships among gray matter volume, age, and cognition using magnetic resonance imaging scans previously acquired from chimpanzees (N = 216). We first determined the relationship between age and gray matter volume, identifying the regions that declined with age. With a subset of our sample (N = 103), we also determined differences in gray matter volume between older chimpanzees with higher cognition scores than expected for their age, and older chimpanzees with lower than expected scores. Finally, we ran a conjunction analysis to determine any overlap in brain regions between these two analyses. We found that as chimpanzees age, they lose gray matter in regions associated with cognition. In addition, cognitively healthy older chimpanzees (those performing better for their age) have greater gray matter volume in many brain regions compared with chimpanzees who underperform for their age. Finally, the conjunction analysis revealed that regions of age-related decline overlap with the regions that differ between cognitively healthy chimpanzees and those who underperform. This study provides further evidence that chimpanzees are an important model for research on the neurobiology of aging. Future studies should investigate the effects of cognitive stimulation on both cognitive performance and brain structure in aging nonhuman primates.
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http://dx.doi.org/10.1002/ajp.23264DOI Listing
April 2021

Sulcal Morphology in Cingulate Cortex is Associated with Voluntary Oro-Facial Motor Control and Gestural Communication in Chimpanzees (Pan troglodytes).

Cereb Cortex 2021 May;31(6):2845-2854

Univ Lyon, Université Claude Bernard Lyon I, Institut National de la Santé Et de la Recherche Médicale, Stem Cell and Brain Research Institute U1208, Bron, France.

Individual differences in sulcal variation within the anterior and mid-cingulate cortex of the human brain, particularly the presence or absence of a paracingulate sulcus (PCGS), are associated with various motor and cognitive processes. Recently, it has been reported that chimpanzees possess a PCGS, previously thought to be a unique feature of the human brain. Here, we examined whether individual variation in the presence or absence of a PCGS as well as the variability in the intralimbic sulcus (ILS) are associated with oro-facial motor control, handedness for manual gestures, and sex in a sample of MRI scans obtained in 225 chimpanzees. Additionally, we quantified the depth of the cingulate sulcus (CGS) along the anterior-posterior axis and tested for association with oro-facial motor control, handedness, and sex. Chimpanzees with better oro-facial motor control were more likely to have a PCGS, particularly in the left hemisphere compared to those with poorer control. Male chimpanzees with better oro-facial motor control showed increased leftward asymmetries in the depth of the anterior CGS, whereas female chimpanzees showed the opposite pattern. Significantly, more chimpanzees had an ILS in the left compared to the right hemisphere, but variability in this fold was not associated with sex, handedness, or oro-facial motor control. Finally, significant population-level leftward asymmetries were found in the anterior portion of the CGS, whereas significant rightward biases were evident in the posterior regions. The collective results suggest that the emergence of a PCGS and enhanced gyrification within the anterior and mid-cingulate gyrus may have directly or indirectly evolved in response to selection for increasing oro-facial motor control in primates.
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http://dx.doi.org/10.1093/cercor/bhaa392DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8107786PMC
May 2021

Chimpanzee histology and functional brain imaging show that the paracingulate sulcus is not human-specific.

Commun Biol 2021 Jan 8;4(1):54. Epub 2021 Jan 8.

Montreal Neurological Institute, Department of Neurology and Neurosurgery and Department of Psychology, McGill University, Montreal, Quebec, Canada.

The paracingulate sulcus -PCGS- has been considered for a long time to be specific to the human brain. Its presence/absence has been discussed in relation to interindividual variability of personality traits and cognitive abilities. Recently, a putative PCGS has been observed in chimpanzee brains. To demonstrate that this newly discovered sulcus is the homologue of the PCGS in the human brain, we analyzed cytoarchitectonic and resting-state functional magnetic resonance imaging data in chimpanzee brains which did or did not display a PCGS. The results show that the organization of the mid-cingulate cortex of the chimpanzee brain is comparable to that of the human brain, both cytoarchitectonically and in terms of functional connectivity with the lateral frontal cortex. These results demonstrate that the PCGS is not human-specific but is a shared feature of the primate brain since at least the last common ancestor to humans and great apes ~6 mya.
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http://dx.doi.org/10.1038/s42003-020-01571-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7794552PMC
January 2021

Neutrophil to Lymphocyte Ratio (NLR) in captive chimpanzees (Pan troglodytes): The effects of sex, age, and rearing.

PLoS One 2020 16;15(12):e0244092. Epub 2020 Dec 16.

Michale E. Keeling Center for Comparative Medicine and Research, National Center for Chimpanzee Care, The University of Texas MD Anderson Cancer Center, Bastrop, Texas, United States of America.

In humans, neutrophil to lymphocyte ratio (NLR) has been used as a clinical tool in diagnosis and/or prognosis of a variety of cancers and medical conditions, as well as in measuring physiological stress over time. Given the close phylogenetic relationship and physical similarities between humans and apes, NLR may similarly be a useful diagnostic tool in assessing chimpanzee health. Only one study has examined NLR in apes, reporting that NLR increased with age and was affected by body-mass index and sex. In the current study, we examined changes in NLR data from longitudinal health records for 443 chimpanzees in two captive chimpanzee populations. Using these data, we analyzed intra-individual changes and inter-individual differences in NLR as a function of age, rearing history, and sex. Contrary to previous studies in humans and the one previous study in chimpanzees, NLR values did not change over a 10-year timespan within individual chimpanzees. However, cross-sectional comparisons revealed a significant quadratic relationship between age and NLR, with the highest values during mid-life (20-30 years of age) and the lowest values in younger and older individuals. Additionally, males and mother-reared individuals had higher NLR than females and nursery-reared chimpanzees, respectively. Lastly, males and those with higher NLR values died at younger ages. These findings suggest that NLR may be useful as a predictor of longevity in chimpanzees. However, given the complexities of these relationships, more research is needed to determine the utility of NLR as a diagnostic health tool for chimpanzees.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0244092PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7743966PMC
March 2021

Chimpanzee brain morphometry utilizing standardized MRI preprocessing and macroanatomical annotations.

Elife 2020 11 23;9. Epub 2020 Nov 23.

Institute of Systems Neuroscience, Medical Faculty, Heinrich-Heine-University, Düsseldorf, Germany.

Chimpanzees are among the closest living relatives to humans and, as such, provide a crucial comparative model for investigating primate brain evolution. In recent years, human brain mapping has strongly benefited from enhanced computational models and image processing pipelines that could also improve data analyses in animals by using species-specific templates. In this study, we use structural MRI data from the National Chimpanzee Brain Resource (NCBR) to develop the chimpanzee brain reference template Juna.Chimp for spatial registration and the macro-anatomical brain parcellation Davi130 for standardized whole-brain analysis. Additionally, we introduce a ready-to-use image processing pipeline built upon the CAT12 toolbox in SPM12, implementing a standard human image preprocessing framework in chimpanzees. Applying this approach to data from 194 subjects, we find strong evidence for human-like age-related gray matter atrophy in multiple regions of the chimpanzee brain, as well as, a general rightward asymmetry in brain regions.
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http://dx.doi.org/10.7554/eLife.60136DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7723405PMC
November 2020

Age-related changes in chimpanzee (Pan troglodytes) cognition: Cross-sectional and longitudinal analyses.

Am J Primatol 2021 03 10;83(3):e23214. Epub 2020 Nov 10.

Department of Anthropology and Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, District of Columbia, USA.

Chimpanzees are the species most closely related to humans, yet age-related changes in brain and cognition remain poorly understood. The lack of studies on age-related changes in cognition in chimpanzees is particularly unfortunate in light of the recent evidence demonstrating that this species naturally develops Alzheimer's disease (AD) neuropathology. Here, we tested 213 young, middle-aged, and elderly captive chimpanzees on the primate cognitive test battery (PCTB), a set of 13 tasks that assess physical and social cognition in nonhuman primates. A subset of these chimpanzees (n = 146) was tested a second time on a portion of the PCTB tasks as a means of evaluating longitudinal changes in cognition. Cross-sectional analyses revealed a significant quadratic association between age and cognition with younger and older chimpanzees performing more poorly than middle-aged individuals. Longitudinal analyses showed that the oldest chimpanzees at the time of the first test showed the greatest decline in cognition, although the effect was mild. The collective data show that chimpanzees, like other nonhuman primates, show age-related decline in cognition. Further investigations into whether the observed cognitive decline is associated with AD pathologies in chimpanzees would be invaluable in understanding the comparative biology of aging and neuropathology in primates.
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http://dx.doi.org/10.1002/ajp.23214DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7904603PMC
March 2021

Sulcal morphology of ventral temporal cortex is shared between humans and other hominoids.

Sci Rep 2020 10 13;10(1):17132. Epub 2020 Oct 13.

Helen Wills Neuroscience Institute, 210 Barker Hall, University of California, Berkeley, Berkeley, CA, 94720, USA.

Hominoid-specific brain structures are of particular importance in understanding the evolution of human brain structure and function, as they are absent in mammals that are widely studied in the extended neuroscience field. Recent research indicates that the human fusiform gyrus (FG), which is a hominoid-specific structure critical for complex object recognition, contains a tertiary, longitudinal sulcus (mid-fusiform sulcus, MFS) that bisects the FG into lateral and medial parallel gyri. The MFS is a functional and architectonic landmark in the human brain. Here, we tested if the MFS is specific to the human FG or if the MFS is also identifiable in other hominoids. Using magnetic resonance imaging and cortical surface reconstructions in 30 chimpanzees and 30 humans, we show that the MFS is also present in chimpanzees. The MFS is relatively deeper and cortically thinner in chimpanzees compared to humans. Additional histological analyses reveal that the MFS is not only present in humans and chimpanzees, but also in bonobos, gorillas, orangutans, and gibbons. Taken together, these results reveal that the MFS is a sulcal landmark that is shared between humans and other hominoids. These results require a reconsideration of the sulcal patterning in ventral temporal cortex across hominoids, as well as revise the compensation theory of cortical folding.
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http://dx.doi.org/10.1038/s41598-020-73213-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7555511PMC
October 2020

Comparison of Surface Area and Cortical Thickness Asymmetry in the Human and Chimpanzee Brain.

Cereb Cortex 2020 Oct 7. Epub 2020 Oct 7.

School of Clinical Sciences, University of Edinburgh, Edinburgh EH16 4TJ, UK.

Comparative study of the structural asymmetry of the human and chimpanzee brain may shed light on the evolution of language and other cognitive abilities in humans. Here we report the results of vertex-wise and ROI-based analyses that compared surface area (SA) and cortical thickness (CT) asymmetries in 3D MR images obtained for 91 humans and 77 chimpanzees. The human brain is substantially more asymmetric than the chimpanzee brain. In particular, the human brain has 1) larger total SA in the right compared with the left cerebral hemisphere, 2) a global torque-like asymmetry pattern of widespread thicker cortex in the left compared with the right frontal and the right compared with the left temporo-parieto-occipital lobe, and 3) local asymmetries, most notably in medial occipital cortex and superior temporal gyrus, where rightward asymmetry is observed for both SA and CT. There is also 4) a prominent asymmetry specific to the chimpanzee brain, namely, rightward CT asymmetry of precentral cortex. These findings provide evidence of there being substantial differences in asymmetry between the human and chimpanzee brain. The unique asymmetries of the human brain are potential neural substrates for cognitive specializations, and the presence of significant CT asymmetry of precentral gyrus in the chimpanzee brain should be further investigated.
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http://dx.doi.org/10.1093/cercor/bhaa202DOI Listing
October 2020

Comparative morphology of the corpus callosum across the adult lifespan in chimpanzees (Pan troglodytes) and humans.

J Comp Neurol 2021 May 26;529(7):1584-1596. Epub 2020 Sep 26.

Department of Comparative Medicine, Michael E. Keeling Center for Comparative Medicine and Research, UT MD Anderson Cancer Center, Bastrop, Texas, USA.

The human corpus callosum exhibits substantial atrophy in old age, which is stronger than what would be predicted from parallel changes in overall brain anatomy. To date, however, it has not been conclusively established whether this accentuated decline represents a common feature of brain aging across species, or whether it is a specific characteristic of the aging human brain. In the present cross-sectional study, we address this question by comparing age-related difference in corpus callosum morphology of chimpanzees and humans. For this purpose, we measured total midsagittal area and regional thickness of the corpus callosum from T1-weighted MRI data from 213 chimpanzees, aged between 9 and 54 years. The results were compared with data drawn from a large-scale human sample which was age-range matched using two strategies: (a) matching by chronological age (human sample size: n = 562), or (b) matching by accounting for differences in longevity and various maturational events between the species (i.e., adjusted human age range: 13.6 to 80.9 years; n = 664). Using generalized additive modeling to fit and compare aging trajectories, we found significant differences between the two species. The chimpanzee aging trajectory compared with the human trajectory was characterized by a slower increase from adolescence to middle adulthood, and by a lack of substantial decline from middle to old adulthood, which, however, was present in humans. Thus, the accentuated decline of the corpus callosum found in aging humans is not a universal characteristic of the aging brain, and appears to be human-specific.
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http://dx.doi.org/10.1002/cne.25039DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7987726PMC
May 2021

Age-associated epigenetic change in chimpanzees and humans.

Philos Trans R Soc Lond B Biol Sci 2020 11 21;375(1811):20190616. Epub 2020 Sep 21.

Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington, DC 20052, USA.

Methylation levels have been shown to change with age at sites across the human genome. Change at some of these sites is so consistent across individuals that it can be used as an 'epigenetic clock' to predict an individual's chronological age to within a few years. Here, we examined how the pattern of epigenetic ageing in chimpanzees compares with humans. We profiled genome-wide blood methylation levels by microarray for 113 samples from 83 chimpanzees aged 1-58 years (26 chimpanzees were sampled at multiple ages during their lifespan). Many sites (greater than 65 000) showed significant change in methylation with age and around one-third (32%) of these overlap with sites showing significant age-related change in humans. At over 80% of sites showing age-related change in both species, chimpanzees displayed a significantly faster rate of age-related change in methylation than humans. We also built a chimpanzee-specific epigenetic clock that predicted age in our test dataset with a median absolute deviation from known age of only 2.4 years. However, our chimpanzee clock showed little overlap with previously constructed human clocks. Methylation at CpGs comprising our chimpanzee clock showed moderate heritability. Although the use of a human microarray for profiling chimpanzees biases our results towards regions with shared genomic sequence between the species, nevertheless, our results indicate that there is considerable conservation in epigenetic ageing between chimpanzees and humans, but also substantial divergence in both rate and genomic distribution of ageing-associated sites. This article is part of the theme issue 'Evolution of the primate ageing process'.
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http://dx.doi.org/10.1098/rstb.2019.0616DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7540949PMC
November 2020

Age-related decline in executive function as a hallmark of cognitive ageing in primates: an overview of cognitive and neurobiological studies.

Philos Trans R Soc Lond B Biol Sci 2020 11 21;375(1811):20190618. Epub 2020 Sep 21.

Department of Psychology, Emory University, Atlanta, GA, USA.

Executive function (EF) is a complex construct that reflects multiple higher-order cognitive processes such as planning, updating, inhibiting and set-shifting. Decline in these functions is a hallmark of cognitive ageing in humans, and age differences and changes in EF correlate with age-related differences and changes in association cortices, particularly the prefrontal areas. Here, we review evidence for age-related decline in EF and associated neurobiological changes in prosimians, New World and Old World monkeys, apes and humans. While EF declines with age in all primate species studied, the relationship of this decline with age-related alterations in the prefrontal cortex remains unclear, owing to the scarcity of neurobiological studies focusing on the ageing brain in most primate species. In addition, the influence of sex, vascular and metabolic risk, and hormonal status has rarely been considered. We outline several methodological limitations and challenges with the goal of producing a comprehensive integration of cognitive and neurobiological data across species and elucidating how ageing shapes neurocognitive trajectories in primates with different life histories, lifespans and brain architectures. Such comparative investigations are critical for fostering translational research and understanding healthy and pathological ageing in our own species. This article is part of the theme issue 'Evolution of the primate ageing process'.
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http://dx.doi.org/10.1098/rstb.2019.0618DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7540957PMC
November 2020

Neuron loss associated with age but not Alzheimer's disease pathology in the chimpanzee brain.

Philos Trans R Soc Lond B Biol Sci 2020 11 21;375(1811):20190619. Epub 2020 Sep 21.

School of Biomedical Sciences, Kent State University, Kent, OH 44242, USA.

In the absence of disease, ageing in the human brain is accompanied by mild cognitive dysfunction, gradual volumetric atrophy, a lack of significant cell loss, moderate neuroinflammation, and an increase in the amyloid beta (A) and tau proteins. Conversely, pathologic age-related conditions, particularly Alzheimer's disease (AD), result in extensive neocortical and hippocampal atrophy, neuron death, substantial A plaque and tau-associated neurofibrillary tangle pathologies, glial activation and severe cognitive decline. Humans are considered uniquely susceptible to neurodegenerative disorders, although recent studies have revealed A and tau pathology in non-human primate brains. Here, we investigate the effect of age and AD-like pathology on cell density in a large sample of postmortem chimpanzee brains ( = 28, ages 12-62 years). Using a stereologic, unbiased design, we quantified neuron density, glia density and glia:neuron ratio in the dorsolateral prefrontal cortex, middle temporal gyrus, and CA1 and CA3 hippocampal subfields. Ageing was associated with decreased CA1 and CA3 neuron densities, while AD pathologies were not correlated with changes in neuron or glia densities. Differing from cerebral ageing and AD in humans, these data indicate that chimpanzees exhibit regional neuron loss with ageing but appear protected from the severe cell death found in AD. This article is part of the theme issue 'Evolution of the primate ageing process'.
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http://dx.doi.org/10.1098/rstb.2019.0619DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7540958PMC
November 2020

Cortical Interlaminar Astrocytes Are Generated Prenatally, Mature Postnatally, and Express Unique Markers in Human and Nonhuman Primates.

Cereb Cortex 2021 Jan;31(1):379-395

Department of Pathology and Laboratory Medicine, UC Davis School of Medicine, Sacramento, CA 95817, USA.

Interlaminar astrocytes (ILAs) are a subset of cortical astrocytes that reside in layer I, express GFAP, have a soma contacting the pia, and contain long interlaminar processes that extend through several cortical layers. We studied the prenatal and postnatal development of ILAs in three species of primates (rhesus macaque, chimpanzee, and human). We found that ILAs are generated prenatally likely from radial glial (RG) cells, that ILAs proliferate locally during gestation, and that ILAs extend interlaminar processes during postnatal stages of development. We showed that the density and morphological complexity of ILAs increase with age, and that ILAs express multiple markers that are expressed by RG cells (Pax6, Sox2, and Nestin), specific to inner and outer RG cells (Cryab and Hopx), and astrocyte markers (S100β, Aqp4, and GLAST) in prenatal stages and in adult. Finally, we demonstrated that rudimentary ILAs in mouse also express the RG markers Pax6, Sox2, and Nestin, but do not express S100β, Cryab, or Hopx, and that the density and morphological complexity of ILAs differ between primate species and mouse. Together these findings contribute new information on astrogenesis of this unique class of cells and suggest a lineal relationship between RG cells and ILAs.
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http://dx.doi.org/10.1093/cercor/bhaa231DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7947181PMC
January 2021

Reproducibility of leftward planum temporale asymmetries in two genetically isolated populations of chimpanzees ().

Proc Biol Sci 2020 09 9;287(1934):20201320. Epub 2020 Sep 9.

Department of Comparative Medicine, UT MD Anderson Cancer Center Bastrop, TX 78602, USA.

Once considered a hallmark of human uniqueness, brain asymmetry has emerged as a feature shared with several other species, including chimpanzees, one of our closest living relatives. Most notable has been the discovery of asymmetries in homologues of cortical language areas in apes, particularly in the planum temporale (PT), considered a central node of the human language network. Several lines of evidence indicate a role for genetic mechanisms in the emergence of PT asymmetry; however, the genetic determinants of cerebral asymmetries have remained elusive. Studies in humans suggest that there is heritability of brain asymmetries of the PT, but this has not been explored to any extent in chimpanzees. Furthermore, the potential influence of non-genetic factors has raised questions about the reproducibility of earlier observations of PT asymmetry reported in chimpanzees. As such, the present study was aimed at examining both the heritability of phenotypic asymmetries in PT morphology, as well as their reproducibility. Using magnetic resonance imaging, we evaluated morphological asymmetries of PT surface area (mm) and mean depth (mm) in captive chimpanzees ( = 291) derived from two genetically isolated populations. Our results confirm that chimpanzees exhibit a significant population-level leftward asymmetry for PT surface area, as well as significant heritability in the surface area and mean depth of the PT. These results conclusively demonstrate the existence of a leftward bias in PT asymmetry in chimpanzees and suggest that genetic mechanisms play a key role in the emergence of anatomical asymmetry in this region.
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http://dx.doi.org/10.1098/rspb.2020.1320DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7542794PMC
September 2020

Differences in the mutual eye gaze of bonobos (Pan paniscus) and chimpanzees (Pan troglodytes).

J Comp Psychol 2020 08;134(3):318-322

Department of Comparative Medicine, The University of Texas MD Anderson Cancer Center.

Eye gaze is widespread in nonhuman primate taxa and important for social cognition and communicative signaling. Bonobos and chimpanzees, two closely related primate species, differ in social organization, behavior, and cognition. Chimpanzees' eye gaze and gaze following has been studied extensively, whereas less is known about bonobos' eye gaze. To examine species differences using a more ecologically relevant measure than videos or pictures, the current study compared bonobo and chimpanzee mutual eye gaze with a human observer. A multivariate analysis of variance revealed significant species differences in frequency and total duration, but not bout length, of mutual eye gaze ( < .001). Specifically, bonobos engage in mutual eye gaze more frequently and for longer total duration than chimpanzees. These results are likely related to species differences in social behavior and temperament and are consistent with eye-tracking studies in which bonobos looked at the eye region of conspecifics (in pictures and videos) longer than chimpanzees. Future research should examine the relationship between mutual eye gaze and gaze following, as well as examine its genetic and neurological correlates. (PsycInfo Database Record (c) 2020 APA, all rights reserved).
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http://dx.doi.org/10.1037/com0000247DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7780221PMC
August 2020

Author Correction: Sulcal organization in the medial frontal cortex provides insights into primate brain evolution.

Nat Commun 2020 08 6;11(1):4021. Epub 2020 Aug 6.

Montreal Neurological Institute, Department of Neurology and Neurosurgery and Department of Psychology, McGill University, Montreal, QC, H3A 2B4, Canada.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41467-020-17973-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7413537PMC
August 2020

The role of early social rearing, neurological, and genetic factors on individual differences in mutual eye gaze among captive chimpanzees.

Sci Rep 2020 05 4;10(1):7412. Epub 2020 May 4.

Department of Comparative Medicine, The University of Texas MD Anderson Cancer Center, Michale E. Keeling Center for Comparative Medicine and Research, 650 Cool Water Drive, Bastrop, Texas, 78602, USA.

Mutual eye gaze plays an important role in primate social development and communication. In the current study, we examined the underlying experiential, genetic, and neuroanatomical basis of mutual eye gaze variation in adult captive chimpanzees. A multivariate analysis of variance revealed a significant rearing effect on bout length, with human-reared chimpanzees engaging in longer bouts of mutual gaze compared to mother-reared and wild-born individuals. Next, we utilized source-based morphometry (SBM) to examine gray matter covariation in magnetic resonance imaging scans and determine the relationship between the resulting gray matter covariation components and mutual eye gaze. One SBM component was negatively correlated with gaze duration (nucleus accumbens and anterior insular cortex), while two components were positively correlated with bout length (posterior cingulate cortex, inferior occipital cortex, middle temporal cortex, hippocampus, and the precentral sulcus). Finally, heritability analyses revealed mutual eye gaze to be modestly heritable and significant genetic correlations between bout length and two gray matter covariation components. This study reveals that non-genetic factors, and to a lesser extent, genetic factors appear to influence mutual eye gaze in adult chimpanzees, and is the first to report neuroanatomical correlates of mutual eye gaze variation in chimpanzees.
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http://dx.doi.org/10.1038/s41598-020-64051-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7198555PMC
May 2020

The genetic architecture of the human cerebral cortex.

Science 2020 03;367(6484)

The cerebral cortex underlies our complex cognitive capabilities, yet little is known about the specific genetic loci that influence human cortical structure. To identify genetic variants that affect cortical structure, we conducted a genome-wide association meta-analysis of brain magnetic resonance imaging data from 51,665 individuals. We analyzed the surface area and average thickness of the whole cortex and 34 regions with known functional specializations. We identified 199 significant loci and found significant enrichment for loci influencing total surface area within regulatory elements that are active during prenatal cortical development, supporting the radial unit hypothesis. Loci that affect regional surface area cluster near genes in Wnt signaling pathways, which influence progenitor expansion and areal identity. Variation in cortical structure is genetically correlated with cognitive function, Parkinson's disease, insomnia, depression, neuroticism, and attention deficit hyperactivity disorder.
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http://dx.doi.org/10.1126/science.aay6690DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7295264PMC
March 2020

Cognitive control of orofacial motor and vocal responses in the ventrolateral and dorsomedial human frontal cortex.

Proc Natl Acad Sci U S A 2020 03 14;117(9):4994-5005. Epub 2020 Feb 14.

Univ Lyon, Université Lyon 1, INSERM, Stem Cell and Brain Research Institute U1208, 69500 Bron, France;

In the primate brain, a set of areas in the ventrolateral frontal (VLF) cortex and the dorsomedial frontal (DMF) cortex appear to control vocalizations. The basic role of this network in the human brain and how it may have evolved to enable complex speech remain unknown. In the present functional neuroimaging study of the human brain, a multidomain protocol was utilized to investigate the roles of the various areas that comprise the VLF-DMF network in learning rule-based cognitive selections between different types of motor actions: manual, orofacial, nonspeech vocal, and speech vocal actions. Ventrolateral area 44 (a key component of the Broca's language production region in the human brain) is involved in the cognitive selection of orofacial, as well as, speech and nonspeech vocal responses; and the midcingulate cortex is involved in the analysis of speech and nonspeech vocal feedback driving adaptation of these responses. By contrast, the cognitive selection of speech vocal information requires this former network and the additional recruitment of area 45 and the presupplementary motor area. We propose that the basic function expressed by the VLF-DMF network is to exert cognitive control of orofacial and vocal acts and, in the language dominant hemisphere of the human brain, has been adapted to serve higher speech function. These results pave the way to understand the potential changes that could have occurred in this network across primate evolution to enable speech production.
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http://dx.doi.org/10.1073/pnas.1916459117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7060705PMC
March 2020

AVPR1A variation is linked to gray matter covariation in the social brain network of chimpanzees.

Genes Brain Behav 2020 04 2;19(4):e12631. Epub 2020 Jan 2.

Keeling Center for Comparative Medicine and Research, The University of Texas MD Anderson Cancer Center, Bastrop, Texas.

The vasopressin system has been implicated in the regulation of social behavior and cognition in humans, nonhuman primates and other social mammals. In chimpanzees, polymorphisms in the vasopressin V1a receptor gene (AVPR1A) have been associated with social dimensions of personality, as well as to responses to sociocommunicative cues and mirror self-recognition. Despite evidence of this association with social cognition and behavior, there is little research on the neuroanatomical correlates of AVPR1A variation. In the current study, we tested the association between AVPR1A polymorphisms in the RS3 promotor region and gray matter covariation in chimpanzees using magnetic resonance imaging and source-based morphometry. The analysis identified 13 independent brain components, three of which differed significantly in covariation between the two AVPR1A genotypes (DupB-/- and DupB+/-; P < .05). DupB+/- chimpanzees showed greater covariation in gray matter in the premotor and prefrontal cortex, basal forebrain, lunate and cingulate cortex, and lesser gray matter covariation in the superior temporal sulcus and postcentral sulcus. Some of these regions were previously found to differ in vasopressin and oxytocin neural fibers between nonhuman primates, and in AVPR1A gene expression in humans with different RS3 alleles. This is the first report of an association between AVPR1A and gray matter covariation in nonhuman primates, and specifically links an AVPR1A polymorphism to structural variation in the social brain network. These results further affirm the value of chimpanzees as a model species for investigating the relationship between genetic variation, brain structure and social cognition with relevance to psychiatric disorders, including autism.
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http://dx.doi.org/10.1111/gbb.12631DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7141960PMC
April 2020

Evidence for independent brain and neurocranial reorganization during hominin evolution.

Proc Natl Acad Sci U S A 2019 10 14;116(44):22115-22121. Epub 2019 Oct 14.

Department of Anthropology, University of Zurich, 8057 Zurich, Switzerland;

Throughout hominin evolution, the brain of our ancestors underwent a 3-fold increase in size and substantial structural reorganization. However, inferring brain reorganization from fossil hominin neurocrania (=braincases) remains a challenge, above all because comparative data relating brain to neurocranial structures in living humans and great apes are still scarce. Here we use MRI and same-subject spatially aligned computed tomography (CT) and MRI data of humans and chimpanzees to quantify the spatial relationships between these structures, both within and across species. Results indicate that evolutionary changes in brain and neurocranial structures are largely independent of each other. The brains of humans compared to chimpanzees exhibit a characteristic posterior shift of the inferior pre- and postcentral gyri, indicative of reorganization of the frontal opercular region. Changes in human neurocranial structure do not reflect cortical reorganization. Rather, they reflect constraints related to increased encephalization and obligate bipedalism, resulting in relative enlargement of the parietal bones and anterior displacement of the cerebellar fossa. This implies that the relative position and size of neurocranial bones, as well as overall endocranial shape (e.g., globularity), should not be used to make inferences about evolutionary changes in the relative size or reorganization of adjacent cortical regions of fossil hominins.
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http://dx.doi.org/10.1073/pnas.1905071116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6825280PMC
October 2019

"Plis de passage" Deserve a Role in Models of the Cortical Folding Process.

Brain Topogr 2019 11 3;32(6):1035-1048. Epub 2019 Oct 3.

Neurospin, CEA, Paris-Saclay University, 91191, Gif-sur-Yvette, France.

Cortical folding is a hallmark of brain topography whose variability across individuals remains a puzzle. In this paper, we call for an effort to improve our understanding of the pli de passage phenomenon, namely annectant gyri buried in the depth of the main sulci. We suggest that plis de passage could become an interesting benchmark for models of the cortical folding process. As an illustration, we speculate on the link between modern biological models of cortical folding and the development of the Pli de Passage Frontal Moyen (PPFM) in the middle of the central sulcus. For this purpose, we have detected nine interrupted central sulci in the Human Connectome Project dataset, which are used to explore the organization of the hand sensorimotor areas in this rare configuration of the PPFM.
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http://dx.doi.org/10.1007/s10548-019-00734-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6882753PMC
November 2019

Mirror self-recognition and its relationship to social cognition in chimpanzees.

Anim Cogn 2019 Nov 21;22(6):1171-1183. Epub 2019 Sep 21.

Department of Comparative Medicine, University of Texas MD Anderson Cancer Center, Bastrop, TX, USA.

Chimpanzees and humans are capable of recognizing their own reflection in mirrors. Little is understood about the selective pressures that led to this evolved trait and about the mechanisms that underlie it. Here, we investigated the hypothesis that mirror self-recognition in chimpanzees is the byproduct of a developed form of self-awareness that was naturally selected for its adaptive use in social cognitive behaviors. We present here the first direct attempt to assess the social cognition hypothesis by analyzing the association between mirror self-recognition in chimpanzees, as measured by a mirror-mark test, and their performance on a variety of social cognition tests. Consistent with the social cognition hypothesis, chimpanzees who showed evidence of mirror self-recognition in the mark test tended to perform significantly better on the social cognition tasks than those who failed the mark test. Additionally, the data as a whole fit the social cognition hypothesis better than the main competing hypothesis of mirror self-recognition in great apes, the secondary representation hypothesis. Our findings strongly suggest that the evolutionary origins of great apes' and humans' capacity to understand ourselves, as revealed by our capacity to recognize ourselves in mirrors, are intimately linked to our ability to understand others.
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http://dx.doi.org/10.1007/s10071-019-01309-7DOI Listing
November 2019

Optional-switch cognitive flexibility in primates: Chimpanzees' (Pan troglodytes) intermediate susceptibility to cognitive set.

J Comp Psychol 2020 02 19;134(1):98-109. Epub 2019 Aug 19.

Division of Developmental and Cognitive Neuroscience.

Within human problem-solving, the propensity to use a familiar approach, rather than switch to a more efficient alternative is pervasive. This susceptibility to "cognitive set" prevents optimization by biasing response patterns toward known solutions. In a recent study, which used a nonverbal touch screen task, baboons exhibited a striking ability to deviate from their learned strategy to use a more efficient shortcut. Humans, on the other hand, displayed the opposite response pattern and almost exclusively used a less efficient, but familiar, response. In the current study, we sought to further explore variation in susceptibility to cognitive set within the primate lineage by conducting the Learned Strategy-Direct Strategy task with 10 chimpanzees (). Using multilevel multinomial modeling, we found that chimpanzees' shortcut use was intermediate to baboons' and humans'. However, unlike either baboons or humans, there was pronounced inter- and intraindividual variability in chimpanzees' shortcut use. Additionally, a subset of chimpanzees employed a unique solution, wherein they switched strategies midtrial. Further, we found that chimpanzees did not exhibit switch costs when switching between the learned strategy and the shortcut, but humans did. We propose that differences in abstract rule encoding may underlie differences in susceptibility to cognitive set on the Learned Strategy-Direct Strategy task within the primate lineage. (PsycINFO Database Record (c) 2020 APA, all rights reserved).
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http://dx.doi.org/10.1037/com0000194DOI Listing
February 2020

Evolutionary divergence of neuroanatomical organization and related genes in chimpanzees and bonobos.

Cortex 2019 09 5;118:154-164. Epub 2018 Oct 5.

Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington, DC, USA.

Given their close genetic relatedness to humans, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes) offer an essential comparative framework for studying the evolution of uniquely human traits. These two species differ markedly in their socio-behavioral repertoires, which is reflected in neuroanatomical differences that have been reported in the literature. However, phylogenetic comparative methods have not yet been used to map the evolution of neuroanatomical traits in bonobos and chimpanzees, limiting our ability to understand which neural systems are derived in each species in relation to the last common ancestor of Pan (Pan-LCA). Here, we examine evolutionary changes in neuroanatomical traits of bonobos and chimpanzees relative to ancestral character reconstructions of the Pan-LCA using comparative datasets from hominoids. We found that bonobo brains are derived in showing reduction of whole brain and white matter volumes, with particularly striking reduction of male brain size compared to the inferred Pan-LCA value. Brain structures related to social cognition and emotional regulation, like the insular cortex and amygdala, display a mosaic pattern of evolution with certain traits changing to a greater extent in each species. Examination of potential genetic mechanisms underlying divergence of neural and social traits did not reveal clear differences in protein evolution patterns between the two species. These findings suggest that the brain anatomy of extant bonobos and chimpanzees show lineage-specific specializations and neither can be considered to more closely retain the ancestral state of Pan. Consequently, this raises questions about the extent that modern chimpanzees or bonobos may serve as referential models for the neuroanatomy of the LCA of humans and apes.
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http://dx.doi.org/10.1016/j.cortex.2018.09.016DOI Listing
September 2019

Sulcal organization in the medial frontal cortex provides insights into primate brain evolution.

Nat Commun 2019 07 31;10(1):3437. Epub 2019 Jul 31.

Montreal Neurological Institute, Department of Neurology and Neurosurgery and Department of Psychology, McGill University, Montreal, QC, H3A 2B4, Canada.

Although the relative expansion of the frontal cortex in primate evolution is generally accepted, the nature of the human uniqueness, if any, and between-species anatomo-functional comparisons of the frontal areas remain controversial. To provide a novel interpretation of the evolution of primate brains, sulcal morphological variability of the medial frontal cortex was assessed in Old World monkeys (macaque/baboon) and Hominoidea (chimpanzee/human). We show that both Hominoidea possess a paracingulate sulcus, which was previously thought to be unique to the human brain and linked to higher cognitive functions, such as mentalizing. Also, we show systematic sulcal morphological organization of the medial frontal cortex that can be traced from Old World monkeys to Hominoidea species, demonstrating an evolutionarily conserved organizational principle. These data provide a new framework to compare sulcal morphology, cytoarchitectonic areal distribution, connectivity, and function across the primate order, leading to clear predictions about how other primate brains might be anatomo-functionally organized.
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http://dx.doi.org/10.1038/s41467-019-11347-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668397PMC
July 2019

Further evidence of a left hemisphere specialization and genetic basis for tool use skill in chimpanzees (Pan troglodytes): Reproducibility in two genetically isolated populations of apes.

J Comp Psychol 2019 11 27;133(4):512-519. Epub 2019 Jun 27.

National Center for Chimpanzee Care.

It has been hypothesized that the evolution of tool use may have served as a preadaptation for the emergence of left hemispheric specialization in motor skill in humans. Here, we tested for intermanual differences in performance on a tool use task in a sample of 206 captive chimpanzees in relation to their sex, age, and hand preference. In addition, we examined heritability in tool use skill for the entire sample, as well as within 2 genetically isolated populations of captive chimpanzees. This was done to determine the degree of reproducibility in heritability on motor performance. The results revealed a significant effect of hand preference on intermanual differences in performance. Right-handed chimpanzees performed the task more quickly with their right compared with left hand. In contrast, no significant intermanual differences in performance were found in left- and ambiguous-handed apes. Tool use performance was found to be significantly heritable for overall performance, as well as separately for the left and right hands. Further, significant heritability in tool use performance was found in both populations of apes, suggesting these results were reproducible. The results are discussed in the context of evolutionary theories of handedness and hemispheric specialization and the genetic mechanisms that underlie their expression in primates, including humans. (PsycINFO Database Record (c) 2019 APA, all rights reserved).
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http://dx.doi.org/10.1037/com0000183DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6813849PMC
November 2019

Investigating individual differences in chimpanzee mirror self-recognition and cortical thickness: A vertex-based and region-of-interest analysis.

Cortex 2019 09 16;118:306-314. Epub 2019 May 16.

Clinical Research Imaging Centre (CRIC), School of Clinical Sciences, University of Edinburgh, 47 Little France Crescent, Edinburgh, EH16 4TJ, UK.

Mirror self-recognition (MSR), a recently evolved cognitive trait, is one of the most significant abilities that separate humans and great apes from more distantly related nonhuman primates. MSR may serve as the foundation for a number of related but more complex social cognitive abilities unique to humans and great apes including imitation, empathy, theory-of-mind, perspective taking and deception. However, our understanding of the neural basis of MSR in nonhuman primates remains largely unknown. The current study aimed to begin to fill this gap in the literature by investigating the neuroanatomical foundations of MSR in a sample of 67 captive chimpanzees. Vertex-based and region-of-interest analysis revealed significant differences in cortical thickness, particularly in males, in the cingulate cortex, inferior frontal gyrus and superior temporal and frontal cortex. The current study provides further evidence for the neuroanatomical foundations of mirror self-recognition abilities in chimpanzees.
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http://dx.doi.org/10.1016/j.cortex.2019.05.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697634PMC
September 2019

Evolution of ASPM coding variation in apes and associations with brain structure in chimpanzees.

Genes Brain Behav 2019 09 11;18(7):e12582. Epub 2019 Jun 11.

Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington, District of Columbia.

Studying genetic mechanisms underlying primate brain morphology can provide insight into the evolution of human brain structure and cognition. In humans, loss-of-function mutations in the gene coding for ASPM (Abnormal Spindle Microtubule Assembly) have been associated with primary microcephaly, which is defined by a significantly reduced brain volume, intellectual disability and delayed development. However, less is known about the effects of common ASPM variation in humans and other primates. In this study, we characterized the degree of coding variation at ASPM in a large sample of chimpanzees (N = 241), and examined potential associations between genotype and various measures of brain morphology. We identified and genotyped five non-synonymous polymorphisms in exons 3 (V588G), 18 (Q2772K, K2796E, C2811Y) and 27 (I3427V). Using T1-weighted magnetic resonance imaging of brains, we measured total brain volume, cerebral gray and white matter volume, cerebral ventricular volume, and cortical surface area in the same chimpanzees. We found a potential association between ASPM V588G genotype and cerebral ventricular volume but not with the other measures. Additionally, we found that chimpanzee, bonobo, and human lineages each independently show a signature of accelerated ASPM protein evolution. Overall, our results suggest the potential effects of ASPM variation on cerebral cortical development, and emphasize the need for further functional studies. These results are the first evidence suggesting ASPM variation might play a role in shaping natural variation in brain structure in nonhuman primates.
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http://dx.doi.org/10.1111/gbb.12582DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7798362PMC
September 2019