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J Comp Neurol. 2017 Feb 1;525(2):319-332. doi: 10.1002/cne.24067. Epub 2016 Jul 8.

Cholinergic innervation of the basal ganglia in humans and other anthropoid primates.

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Department of Anthropology, Kent State University, Kent, Ohio, 44242.
School of Biomedical Sciences, Kent State University, Kent, Ohio, 44242.
Department of Anthropology and Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC, 20052.
Behavioral Health Services Department, California National Primate Research Center, University of California, Davis, California, 95616.
Laboratory of Quantitative Neuromorphology, Department of Psychology, Colorado College, Colorado Springs, Colorado, 80903.
Neuroscience Institute and Language Research Center, Georgia State University, Atlanta, Georgia, 30322.
Fishberg Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, New York, 10029.
New York Consortium in Evolutionary Primatology, New York, New York, 10024.


Cholinergic innervation of the basal ganglia is important in learning and memory. Striatal cholinergic neurons integrate cognitive and motivational states with behavior. Given these roles, it is not surprising that deficits in cortical cholinergic innervation have been correlated with loss of cognitive function in Alzheimer's disease and schizophrenia. Such evidence suggests the potential significance of subcortical cholinergic innervation in the evolution of the human brain. To compare humans with other closely related primates, the present study quantified axons and interneurons immunoreactive for choline acetyltransferase (ChAT) in regions of the executive and motor loops of the basal ganglia of humans, great apes, and monkeys. We also compared ChAT-immunoreactive (ir) interneuron morphological types among species within striatal regions. The results indicate that humans and great apes differ from monkeys in having a preponderance of multipolar ChAT-ir interneurons in the caudate nucleus and putamen, whereas monkeys have a more heterogeneous representation of multipolar, bipolar, and unipolar interneurons. Cholinergic innervation, as measured by axon and interneuron densities, did not differ across species in the medial caudate nucleus. Differences were detected in the dorsal caudate nucleus, putamen, and globus pallidus but the observed variation did not associate with the phylogenetic structure of the species in the sample. However, combining the present results with previously published data for dopamine revealed a unique pattern of innervation for humans, with higher amounts of dopamine compared with acetylcholine in the striatum. Taken together, these findings indicate a potential evolutionary shift in basal ganglia neurotransmission in humans that may favor increased synaptic plasticity. J. Comp. Neurol. 525:319-332, 2017.


RRID:AB_2079751; acetylcholine; caudate nucleus; choline acetyltransferase; evolution; globus pallidus; putamen; striatum

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