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«Introduction. As our closest living relatives, great apes share similarities with humans in terms of cognition, emotion, sociality, and ...»

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THE GREAT APE NEUROSCIENCE PROJECT

PROGRESS REPORT – FEBRUARY 2011

Introduction. As our closest living relatives, great apes share similarities with humans in terms of

cognition, emotion, sociality, and susceptibility to some diseases of aging. Yet despite these striking

similarities, important differences exist that set humans apart with regard to brain structure and

function. The overarching goal of the Great Ape Neuroscience Project is to investigate the neurobiological basis of variation that distinguishes great apes from other primates, defines each great ape species as unique, and helps us to better understand humans’ place in nature. The Great Ape Neuroscience Project has been active for just over a decade and continues to be at the forefront of comparative research in primate neuroscience. Our research publications have garnered thousands of citations in diverse journals spanning biology, psychology, veterinary medicine, primatology, and anthropology. Our accomplishments are the result of a community of collaborators from zoos, academic institutions, and governmental organizations. The contribution of each member in this network is essential to advancing the science of great ape neurobiology. This report was prepared to provide an update on the outcomes of the Great Ape Neuroscience Project. We look forward to working together in the future.

Background. The Great Ape Neuroscience Project originated as an extension of the Great Ape Aging Project (funded by the National Institute on Aging of the National Institutes of Health). The Great Ape Aging Project was conceived of as a means of adding scientific value to elderly apes in captivity. The need was seen by members of the Association of Zoos and Aquariums Ape Taxon Advisory Group (ApeTAG) to increase the quantity and quality of humane scientific studies of apes in zoological collections. It also became clear that many chimpanzees in research facilities were regarded as “surplus to research needs,” and were thought to be unsupportable with research funds. Medical scientists studying the causes of neurodegenerative diseases such as Alzheimer’s and Parkinson’s diseases expressed interest in studies of brain and behavior in great apes to determine whether or not the same neurodegenerative processes occurred in them as in afflicted humans. The convergence of these interests and needs led to the development of the Great Ape Aging Project in 1997.

Progress. Soon after the first brain specimens were received, it became clear that much remained to be learned about the basic similarities and differences in the neuroanatomy of great apes and humans, as well as other primates and mammals. One of the first achievements was discovery that a neuronal type dramatically affected in advanced Alzheimer’s disease (and thought to exist exclusively in humans), called the von Economo neuron, is present in the brains of all the great apes. Since its inception, the project has acquired more than 100 great ape brains that have been involved in detailed comparisons with human and other primate and mammalian brains, using advanced imaging, immunohistochemical, and stereological techniques.

Highlights of major findings include:

 The overt shrinkage of the frontal lobe and hippocampus that is characteristic of human brain aging is not observed in aged chimpanzees.

 Comparisons of gene expression in the cerebral cortex of humans, chimpanzees, and gorillas indicate that there has been upregulation of genes involved in metabolism and synaptic function in humans. Consistent with this idea, the neurons of the frontal cortex become progressively more metabolically costly with brain enlargement in primates, as indicated by counts of surrounding glial cells. This greater requirement for energy uptake may be associated with vulnerability to oxidative damage, which characterizes diseases of aging, such as Alzheimer’s disease.

 The anatomical supply of the neurotransmitters dopamine, serotonin, and acetylcholine to the prefrontal cortex of humans and chimpanzees are similar, but differ from macaque monkeys.

This indicates that some aspects of the neuromodulation of cognitive processing are evolutionarily derived in the ape-human lineage.

 Compared to great apes, only humans show a leftward asymmetry of Broca’s area of the cerebral cortex, a region that is important for the production of speech and language. In contrast, humans and great apes are similar in displaying asymmetry of Wernicke’s area, a region that is important for decoding complex sounds used in language.

Funding. The initial phases of this project were supported by grants from the National Institute on Aging of the National Institutes of Health (AG14308). Later phases have received grant support from the National Science Foundation, National Institutes of Health, Wenner-Gren Foundation, and James S.

McDonnell Foundation. We are well supported by external funds, postdoctoral scientists, and graduate students to continue pursuing the most cutting-edge research on great ape neurobiology.

Moving Forward. We hope to develop a strong communications network that will enable information to flow between ourselves and the staff who provide care, clinical, and curatorial expertise at the home institution of each participating ape. People who had a special interest or affinity with a specific ape will be able to find out exactly what was learned from that individual. To sustain progress in our studies of the comparative neurobiology of great apes and other primates, we renew our request for collaboration. We continue to seek intact brains from great apes, as well as other primates and mammals. Whole fixed brains are best suited for MRI scanning prior to histological sectioning for research and pathology diagnosis. If the postmortem interval before brain collection is less than 12 hours, we request the left hemisphere fixed and the right hemisphere snap frozen or placed in RNAlater.





When brain tissue specimens are provided, we will make every effort to secure a collaborating neuropathologist to provide a detailed neurological report to the institutional veterinarian.

Alternatively, we will coordinate dissection and sampling directly with the originating institutions in case they desire performing their own neuropathologic examination and we will return sufficient materials for the diagnostic procedures. We will also provide a high-quality 3 T MRI (and as of spring 2011, 7 T) with DTI of each brain, if intact. All our research on postmortem brains is conducted in coordination with Dr. William Hopkins (Division of Psychobiology, Yerkes National Primate Research Center and Department of Psychology, Agnes Scott College), a comparative psychologist with decades of experience collecting behavioral data in captive populations of great apes. We will continue to work together with Dr. Hopkins to correlate studies of brain structure with the behavioral measures he has obtained from these apes during their lifetime.

We will present progress reports to all participating institutions on an annual basis to apprise them of the general scientific findings arising from the project and to make them aware of the contributions made by specific animals that were housed under their care.

Contacts. Please contact us if you have any questions about the contents of this report, or if additional agreements and applications are required to renew our collaboration. Upon request, we can provide shipping account information for billing, as well as other supplies for brain specimen collection.

Patrick R. Hof, MD Regenstreif Professor of Neuroscience Vice-Chair, Department of Neuroscience Mount Sinai School of Medicine, Box 1065 One Gustave L. Levy Place New York, NY 10029 patrick.hof@mssm.edu 212-659-5904 Chet C. Sherwood, PhD Associate Professor Department of Anthropology GW Institute for Neuroscience The George Washington University 2110 G Street, NW Washington, D.C. 20052 sherwood@gwu.edu 202-994-6346 Joseph M. Erwin, PhD 4139 Gem Bridge Road Needmore, PA 17238 agingapes@gmail.com 717-573-2081 (home/office) 301-938-8955 (cell phone) Dr. Erwin is a semi-retired consultant and serves as the Executive Director of the nonprofit Foundation for Comparative and Conservation Biology (FCCB). He holds academic affiliate appointments as a Research Professor of Anthropology at The George Washington University, Washington, D.C., and Adjunct Professor of Biomedical Sciences and Pathobiology at the Virginia-Maryland Regional College of Veterinary Medicine at Virginia Tech, Blacksburg, VA.

Bibliography of the Great Ape Neuroscience Project Peer-reviewed Journal Articles Nimchinsky E.A., Gilissen E., Allman J.M., Perl D.P., Erwin J.M., Hof P.R. (1999) A neuronal morphologic type unique to humans and great apes. Proc. Natl. Acad. Sci. USA 96, 5268-5273.

Hof P.R., Glezer I.I., Nimchinsky E.A., Erwin J.M. (2000) Neurochemical and cellular specializations in the mammalian neocortex reflect phylogenetic relationships: evidence from cetaceans, artiodactyls, and primates. Brain Behav. Evol. 55, 300-310.

Perl D.P., Good P., Morrison J.H., Erwin J.M., Hof P.R. (2000) Practical approaches to stereology in the setting of aging- and disease-related brain banks. J. Chem. Neuroanat. 20, 7-19.

Allman J.M., Hakeem A., Erwin J.M., Nimchinsky E.A., Hof P.R. (2001) The anterior cingulate cortex: the evolution of an interface between emotion and cognition. Ann. NY Acad. Sci. 935, 107-117.

Hof P.R., Nimchinsky E.A., Perl D.P., Erwin J.M. (2001) An unusual population of pyramidal neurons in the anterior cingulate cortex of hominids contains the calcium-binding protein calretinin.

Neurosci. Lett. 307, 139-142.

Sherwood C.C., Broadfield D.C., Holloway R.L., Gannon P.J., Hof P.R. (2003) Variability of Broca's area homologue in African great apes: implications for language evolution. Anat. Rec. 271, 276-285.

Sherwood C.C., Holloway R.L., Gannon P.J., Semendeferi K., Erwin J.M., Zilles K., Hof P.R. (2003) Neuroanatomical basis of facial expression in monkeys, apes, and humans. Ann. NY Acad. Sci.

1000, 99-103.

Sherwood C.C., Lee P.W.H., Rivara C.B., Holloway R.L., Gilissen E.P.E., Simmons R.M.T., Hakeem A., Allman J.M., Erwin J.M., Hof P.R. (2003) Evolution of specialized pyramidal neurons in primate visual and motor cortex. Brain Behav. Evol. 61, 28-44.

Sherwood C.C., Holloway R.L., Erwin J.M., Schleicher A., Zilles K., Hof P.R. (2004) Cortical orofacial motor representation in Old World monkeys, great apes, and humans. I: Quantitative cytoarchitectural analysis of primary motor cortex. Brain Behav. Evol. 63, 61-81.

Sherwood C.C., Holloway R.L., Erwin J.M., Hof P.R. (2004) Cortical orofacial motor representation in Old World monkeys, great apes, and humans. II: Stereologic analysis of chemoarchitecture. Brain Behav. Evol. 63, 82-106. Erratum, Brain Behav. Evol. 65, 71-72, 2005.

Uddin M., Wildman D.E., Liu G., Xu W., Johnson R.M., Hof P.R., Kapatos G., Grossman L.I., Goodman M.

(2004) Sister-grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. Proc. Natl. Acad. Sci. USA 101, 2957-2962.

Colombo J.A., Sherwood C.C., Hof P.R. (2004) Interlaminar astroglial processes in the cerebral cortex of great apes. Anat. Embryol. 208, 215-218.

Sherwood C.C., Cranfield M.R., Mehlman P.T., Lilly A.A., Garbe J., Rein T.R., Bruner H.J., Holloway R.L., Tang C.Y., Naidich T.P., Delman B.N., Erwin J.M., Whittier C., Nutter F., Hof P.R. (2004) Brain structure variation of great apes, with attention to the mountain gorilla (Gorilla beringei beringei). Am. J. Primatol. 63, 149-164.

Sherwood C.C., Hof P.R., Holloway R.L., Semendeferi K., Gannon P.J., Frahm H., Zilles K. (2005) Evolution of the brainstem orofacial motor system in primates: a comparative quantitative study of trigeminal, facial and hypoglossal motor nuclei. J. Hum. Evol. 48, 45-84.

Sherwood C.C., Holloway R.L., Semendeferi K., Hof P.R. (2005) Is prefrontal white matter enlargement a human evolutionary specialization? [Correspondence] Nature Neurosci. 8, 537-538.

Hof P.R., Sherwood C.C. (2005) Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat. Rec. 287, 1153-1163.

Sherwood C.C. (2005) Comparative anatomy of the facial motor nucleus in mammals, with an analysis of neuron numbers in primates. Anat. Rec. 287, 1067-1079.

Sherwood C.C., Stimpson C.D., Raghanti M.A., Wildman D.E., Uddin M., Grossman L.I., Goodman M., Redmond J.C., Bonar C., Erwin J.M., Hof P.R. (2006) Evolution of increased glia-neuron ratio in the human frontal cortex. Proc. Natl. Acad. Sci. USA 103, 13606-13611.

Sherwood C.C., Raghanti M.A., Stimpson C.D., Bonar C.J., de Sousa A.A., Preuss T.M., Hof P.R. (2007) Scaling of inhibitory microcircuitry in areas V1 and V2 of anthropoid primates revealed by calcium-binding protein immunohistochemistry. Brain Behav. Evol. 69, 176-195.

Sherwood C.C., Wahl E., Erwin J.M., Hof P.R., Hopkins W.D. (2007) Histological asymmetries of primary

motor cortex predict handedness in chimpanzees (Pan troglodytes). J. Comp. Neurol. 503, 525Tigno X., Shi Y-D, Erwin J.M., Aslam S., Hansen B. (2007) Understanding type 2 diabetes and aging:

lessons from nonhuman primates. Asian Biomedicine 1, 359-376.

Raghanti M.A., Stimpson C.D., Marcinkiewicz J.L., Erwin J.M., Hof P.R., Sherwood C.C. (2008) Differences in cortical serotonergic innervation among humans, chimpanzees and macaque monkeys: a comparative study. Cereb. Cortex 18, 584-597.

Raghanti M.A., Stimpson C.D., Marcinkiewicz J.L., Erwin J.M., Hof P.R., Sherwood C.C. (2008) Cortical cholinergic innervation of the frontal cortex: differences among humans, chimpanzees, and macaque monkeys. J. Comp. Neurol. 506, 409-424.

Uddin M., Opazo J.C., Wildman D.E., Sherwood C.C., Hof P.R., Goodman M., Grossman L.I. (2008) Molecular evolution of the cytochrome c oxidase subunit 5A gene in primates. BMC Evol. Biol. 8, 8 (12 pp.).

Wang S.S.H., Shultz J.R., Burish M.J., Harrison K.H., Hof P.R., Towns L.C., Wagers M.W., Wyatt K.D. (2008) Shaping of white matter composition by biophysical scaling constraints. J. Neurosci. 28, 4056Raghanti M.A., Stimpson C.D., Marcinkiewicz J.L., Erwin J.M., Hof P.R., Sherwood C.C. (2008) Differences in cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: a comparative study. Neuroscience 155, 203-220.



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