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Evolutionary scaling and cognitive correlates of primate frontal cortex microstructure

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Abstract

Investigating evolutionary changes in frontal cortex microstructure is crucial to understanding how modifications of neuron and axon distributions contribute to phylogenetic variation in cognition. In the present study, we characterized microstructural components of dorsolateral prefrontal cortex, orbitofrontal cortex, and primary motor cortex from 14 primate species using measurements of neuropil fraction and immunohistochemical markers for fast-spiking inhibitory interneurons, large pyramidal projection neuron subtypes, serotonergic innervation, and dopaminergic innervation. Results revealed that the rate of evolutionary change was similar across these microstructural variables, except for neuropil fraction, which evolves more slowly and displays the strongest correlation with brain size. We also found that neuropil fraction in orbitofrontal cortex layers V–VI was associated with cross-species variation in performance on experimental tasks that measure self-control. These findings provide insight into the evolutionary reorganization of the primate frontal cortex in relation to brain size scaling and its association with cognitive processes.

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Data availability

The dataset generated during the current study is available in Table 1.

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Acknowledgements

We acknowledge Cleveland Metroparks Zoo, Smithsonian National Zoological Park, Milwaukee County Zoo, and the National Chimpanzee Brain Resource (funded by NIH NS092988) for contributing brain specimens used in this study.

Funding

This research was supported by James S. McDonnell Foundation (220020293), NSF (SMA-1542848, EF-2021785, DRL-2219759), and NIH (AG067419, HG011641).

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Authors and Affiliations

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

    Cheryl D. Stimpson & Chet C. Sherwood

  2. DoD/USU Brain Tissue Repository and Neuropathology Program, Uniformed Services University (USU), Bethesda, MD, USA

    Cheryl D. Stimpson

  3. Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc, Bethesda, MD, USA

    Cheryl D. Stimpson

  4. Department of Anthropology, Stony Brook University, Stony Brook, NY, USA

    Jeroen B. Smaers

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

    Mary Ann Raghanti

  6. Department of Psychology, Trinity University, San Antonio, TX, USA

    Kimberley A. Phillips

  7. Southwest National Primate Research Center, Texas Biomedical Research Institute, San Antonio, TX, USA

    Kimberley A. Phillips

  8. Department of Psychology, Laboratory of Quantitative Neuromorphology, Colorado College, Colorado Springs, CO, USA

    Bob Jacobs

  9. Department of Comparative Medicine, Michale E Keeling Center for Comparative Medicine and Research, M D Anderson Cancer Center, Bastrop, TX, USA

    William D. Hopkins

  10. Nash Family Department of Neuroscience, Center for Discovery and Innovation, and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Patrick R. Hof

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  1. Cheryl D. Stimpson
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Cheryl Stimpson, Jeroen Smaers, and Chet Sherwood. The first draft of the manuscript was written by Cheryl Stimpson, Jeroen Smaers, and Chet Sherwood and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Chet C. Sherwood.

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Conflict of interest

The authors have no relevant financial or non-financial interests to disclose. This study utilized human tissue that was procured via the El Paso County coroner’s office in Colorado, which provides de-identified samples. Requests for human tissue samples, particularly in biomedical research, are typically processed through the medical examiner or coroner’s office, which serves as the legal authority responsible for verifying that all necessary consents and regulations are followed. The George Washington University Research Ethics Committee has confirmed that no ethical approval is required. The protocols are in accordance with the ethical standards of our institution and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Stimpson, C.D., Smaers, J.B., Raghanti, M.A. et al. Evolutionary scaling and cognitive correlates of primate frontal cortex microstructure. Brain Struct Funct (2023). https://doi.org/10.1007/s00429-023-02719-7

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