Proceedings of the Royal Society B: Biological Sciences
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Inhibitory interneurons of the human prefrontal cortex display conserved evolution of the phenotype and related genes

Chet C. Sherwood

Chet C. Sherwood

Department of Anthropology, The George Washington University, Washington, DC 20052, USA

[email protected]

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Mary Ann Raghanti

Mary Ann Raghanti

Department of Anthropology and School of Biomedical Sciences, Kent State University, Kent, OH 44242, USA

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Cheryl D. Stimpson

Cheryl D. Stimpson

Department of Anthropology, The George Washington University, Washington, DC 20052, USA

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Muhammad A. Spocter

Muhammad A. Spocter

Department of Anthropology, The George Washington University, Washington, DC 20052, USA

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Monica Uddin

Monica Uddin

Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI 48109, USA

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Amy M. Boddy

Amy M. Boddy

Center for Molecular Medicine and Genetics, Wayne State University School of Medicine, Detroit, MI 48201, USA

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Derek E. Wildman

Derek E. Wildman

Center for Molecular Medicine and Genetics, Wayne State University School of Medicine, Detroit, MI 48201, USA

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Christopher J. Bonar

Christopher J. Bonar

Cleveland Metroparks Zoo, Cleveland, OH 44109, USA

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Albert H. Lewandowski

Albert H. Lewandowski

Cleveland Metroparks Zoo, Cleveland, OH 44109, USA

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Kimberley A. Phillips

Kimberley A. Phillips

Department of Psychology, Trinity University, San Antonio, TX 78212, USA

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Joseph M. Erwin

Joseph M. Erwin

Department of Biomedical Sciences and Pathobiology, Virginia-Maryland Regional College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, VA 24036, USA

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Patrick R. Hof

Patrick R. Hof

Department of Neuroscience, Mount Sinai School of Medicine, New York, NY 10029, USA

New York Consortium in Evolutionary Primatology, New York, NY, USA

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Published:https://doi.org/10.1098/rspb.2009.1831

    Inhibitory interneurons participate in local processing circuits, playing a central role in executive cognitive functions of the prefrontal cortex. Although humans differ from other primates in a number of cognitive domains, it is not currently known whether the interneuron system has changed in the course of primate evolution leading to our species. In this study, we examined the distribution of different interneuron subtypes in the prefrontal cortex of anthropoid primates as revealed by immunohistochemistry against the calcium-binding proteins calbindin, calretinin and parvalbumin. In addition, we tested whether genes involved in the specification, differentiation and migration of interneurons show evidence of positive selection in the evolution of humans. Our findings demonstrate that cellular distributions of interneuron subtypes in human prefrontal cortex are similar to other anthropoid primates and can be explained by general scaling rules. Furthermore, genes underlying interneuron development are highly conserved at the amino acid level in primate evolution. Taken together, these results suggest that the prefrontal cortex in humans retains a similar inhibitory circuitry to that in closely related primates, even though it performs functional operations that are unique to our species. Thus, it is likely that other significant modifications to the connectivity and molecular biology of the prefrontal cortex were overlaid on this conserved interneuron architecture in the course of human evolution.

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