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

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A Correction to this article was published on 29 October 2020

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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.

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Availability of data and material

Data are accessible in a public repository at https://github.com/anthrochristina/ChimpHippocampus.

Change history

  • 29 October 2020

    The original version of this article contained a mistake in Figs.��3 and 4.

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Acknowledgements

These data were in part collected while Rebecca Rosen was employed at Emory University (2004–2010). The opinions expressed in this article are the author’s own and do not reflect the view of the National Institutes of Health, the Department of Health and Human Services, or the United States Government.

Funding

This research was supported by National Institutes of Health (NIH) Grants P01 AG026423 (to James G. Herndon), P50 AG025688 (to Allan I. Levey), and P50 AG005138 (to Patrick R. Hof), and by the James S. McDonnell Foundation (JSMF 21002093) to Todd M. Preuss.

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Author notes

  1. Christina N. Rogers Flattery and Rebecca F. Rosen should be considered joint first author.

Authors and Affiliations

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

    Christina N. Rogers Flattery

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

    Rebecca F. Rosen

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

    Aaron S. Farberg, Jeromy M. Dooyema, Lary C. Walker & Todd M. Preuss

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

    Patrick R. Hof

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

    Chet C. Sherwood

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

    Lary C. Walker

  7. Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Atlanta, GA, 30322, USA

    Todd M. Preuss

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Contributions

CNRF, RFR, LCW, and TMP wrote the paper. RFR, LCW, TMP, PRH, and CCS designed the research. JMD and ASF prepared samples. CNRF, RFR, and ASF collected and analyzed data. PRH and CCS provided intellectual content and interpretation of results. All authors contributed to the final preparation of the manuscript and approved it for submission.

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Correspondence to Christina N. Rogers Flattery.

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The authors have no conflicts of interest to report.

Ethics approval

Research was conducted on post-mortem/archival chimpanzee brain tissue that had been opportunistically collected at necropsy, thus IACUC approval was not required. All tissues were collected in accordance with federal and institutional guidelines for the humane care and use of experimental animals. The New Iberia and Yerkes Centers are fully accredited by AAALAC International.

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Rogers Flattery, C.N., Rosen, R.F., Farberg, A.S. et al. Quantification of neurons in the hippocampal formation of chimpanzees: comparison to rhesus monkeys and humans. Brain Struct Funct 225, 2521–2531 (2020). https://doi.org/10.1007/s00429-020-02139-x

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