Human‐specific increase of dopaminergic innervation in a striatal region associated with speech and language: A comparative analysis of the primate basal ganglia |
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| Authors: | Mary Ann Raghanti Melissa K. Edler Alexa R. Stephenson Lakaléa J. Wilson William D. Hopkins John J. Ely Joseph M. Erwin Bob Jacobs Patrick R. Hof Chet C. Sherwood |
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| Affiliation: | 1. Department of Anthropology, Kent State University, Kent, Ohio;2. School of Biomedical Sciences, Kent State University, Kent, Ohio;3. Neuroscience Institute and Language Research Center, Georgia State University, Atlanta, GA;4. MAEBIOS, Alamogordo, New Mexico;5. Department of Anthropology and Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC;6. California National Primate Research Center, University of California, Davis, California;7. Laboratory of Quantitative Neuromorphology, Psychology, Colorado College, Colorado Springs, Colorado;8. Fishberg Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, New York;9. New York Consortium in Evolutionary Primatology, New York, New York |
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| Abstract: | The dopaminergic innervation of the striatum has been implicated in learning processes and in the development of human speech and language. Several lines of evidence suggest that evolutionary changes in dopaminergic afferents of the striatum may be associated with uniquely human cognitive and behavioral abilities, including the association of the human‐specific sequence of the FOXP2 gene with decreased dopamine in the dorsomedial striatum of mice. To examine this possibility, we quantified the density of tyrosine hydroxylase‐immunoreactive axons as a measure of dopaminergic innervation within five basal ganglia regions in humans, great apes, and New and Old World monkeys. Our results indicate that humans differ from nonhuman primate species in having a significant increase in dopaminergic innervation selectively localized to the medial caudate nucleus. This region of the striatum is highly interconnected, receiving afferents from multiple neocortical regions, and supports behavioral and cognitive flexibility. The medial caudate nucleus also shows hyperactivity in humans lacking a functional FOXP2 allele and exhibits altered dopamine concentrations in humanized Foxp2 mice. Additionally, striatal dopaminergic input was not altered in chimpanzees that used socially learned attention‐getting sounds versus those that did not. This evidence indicates that the increase in dopamine innervation of the medial caudate nucleus in humans is a species‐typical characteristic not associated with experience‐dependent plasticity. The specificity of this increase may be related to the degree of convergence from cortical areas within this region of the striatum and may also be involved in human speech and language. J. Comp. Neurol. 524:2117–2129, 2016. © 2015 Wiley Periodicals, Inc. |
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| Keywords: | caudate nucleus putamen striatum dopamine tyrosine hydroxylase evolution FOXP2 RRID AB_390204 RRID SciRes_000114 |
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