Quantification of neurons in the hippocampal formation of chimpanzees: comparison to rhesus monkeys and humans

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ORIGINAL ARTICLE

Quantification of neurons in the hippocampal formation of chimpanzees: comparison to rhesus monkeys and humans Christina N. Rogers Flattery1   · Rebecca F. Rosen2   · Aaron S. Farberg3   · Jeromy M. Dooyema3 · Patrick R. Hof4   · Chet C. Sherwood5   · Lary C. Walker3,6   · Todd M. Preuss3,7  Received: 30 June 2020 / Accepted: 29 August 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract The hippocampal formation is important for higher brain functions such as spatial navigation and the consolidation of memory, and it contributes to abilities thought to be uniquely human, yet little is known about how the human hippocampal formation compares to that of our closest living relatives, the chimpanzees. To gain insight into the comparative organization of the hippocampal formation in catarrhine primates, we quantified neurons stereologically in its major subdivisions—the granular layer of the dentate gyrus, CA4, CA2-3, CA1, and the subiculum—in archival brain tissue from six chimpanzees ranging from 29 to 43 years of age. We also sought evidence of Aβ deposition and hyperphosphorylated tau in the hippocampus and adjacent neocortex. A 42-year-old animal had moderate cerebral Aβ-amyloid angiopathy and tauopathy, but Aβ was absent and tauopathy was minimal in the others. Quantitatively, granule cells of the dentate gyrus were most numerous, followed by CA1, subiculum, CA4, and CA2-3. In the context of prior investigations of rhesus monkeys and humans, our findings indicate that, in the hippocampal formation as a whole, the proportions of neurons in CA1 and the subiculum progressively increase, and the proportion of dentate granule cells decreases, from rhesus monkeys to chimpanzees to humans. Because CA1 and the subiculum engender key hippocampal projection pathways to the neocortex, and because the neocortex varies in volume and anatomical organization among these species, these findings suggest that differences in the proportions of neurons in hippocampal subregions of catarrhine primates may be linked to neocortical evolution. Keywords  Stereology · CA1 region · Dentate gyrus · Alzheimer’s disease · Abeta · Tauopathy Christina N. Rogers Flattery and Rebecca F. Rosen should be considered joint first author. * Christina N. Rogers Flattery [email protected] 1



Department of Human Evolutionary Biology, Harvard University, 11 Divinity Ave, Cambridge, MA 02138, USA

2



National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20814, USA

3

Yerkes National Primate Research Center, Emory University, Atlanta, GA 30329, USA

4

Nash Family Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA

5

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

6

Department of Neurology, Emory University School of Medicine, Atlanta, GA 30322, USA

7

Department of Pathology and Laboratory Medicine, Emory Uni