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An analysis of von Economo neurons in the cerebral cortex of cetaceans, artiodactyls, and perissodactyls

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Abstract

Von Economo neurons (VENs) are specialized projection neurons with a characteristic spindle-shaped soma and thick basal and apical dendrites. VENs have been described in restricted cortical regions, with their most frequent appearance in layers III and V of the anterior cingulate cortex, anterior insula, and frontopolar cortex of humans, great apes, macaque monkeys, elephants, and some cetaceans. Recently, a ubiquitous distribution of VENs was reported in various cortical areas in the pygmy hippopotamus, one of the closest living relatives of cetaceans. That finding suggested that VENs might not be unique to only a few species that possess enlarged brains. In the present analysis, we assessed the phylogenetic distribution of VENs within species representative of the superordinal clade that includes cetartiodactyls and perissodactyls, as well as afrotherians. In addition, the distribution of fork cells that are often found in close proximity to VENs was also assessed. Nissl-stained sections from the frontal pole, anterior cingulate cortex, anterior insula, and occipital pole of bowhead whale, cow, sheep, deer, horse, pig, rock hyrax, and human were examined using stereologic methods to quantify VENs and fork cells within layer V of all four cortical regions. VENs and fork cells were found in each of the species examined here with species-specific differences in distributions and densities. The present results demonstrated that VENs and fork cells were not restricted to highly encephalized or socially complex species, and their repeated emergence among distantly related species seems to represent convergent evolution of specialized pyramidal neurons. The widespread phylogenetic presence of VENs and fork cells indicates that these neuron morphologies readily emerged in response to selective forces,whose variety and nature are yet to be identified.

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Acknowledgments

This work was supported by the National Science Foundation (BCS-0921079 and BCS-1316829) and the James S. McDonnell Foundation (grant 22002078). Brain materials used in this study were obtained through the Northwestern University Alzheimer’s Disease Center Brain Bank (supported by an Alzheimer’s Disease Core Center grant, P30 AG013854, from the National Institute on Aging to Northwestern University, Chicago, Illinois), Ward’s Scientific (horse, pig, and calf), and Jessica Sudduth (white-tailed deer, permit # 6739695382), and the Department of Wildlife Management, North Slope Borough, Barrow, AK (bowhead whale). We thank the J. Craig George, Barrow captains and crew members, the Barrow Whaling Commission, and the Alaska Eskimo Whaling Commission for allowing collection of bowhead whale brain samples. Through this and other projects, the Inupiat Eskimos have made significant contributions to the general scientific knowledge of cetaceans. The samples were collected under the authority of NOAA-NMFS permit No. 814-1899 to the North Slope Borough. We thank Paul Nader for extracting the bowhead whale brains nearly two decades ago. We also thank Jessica Sudduth, Nathan Heinrichs, Melissa Edler, and Alexa Stephenson for their expert technical assistance.

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Authors and Affiliations

  1. Department of Anthropology and School of Biomedical Sciences, Kent State University, 750 Hilltop Drive, 222 Lowry Hall, Kent, OH, 44242, USA

    Mary Ann Raghanti, Linda B. Spurlock & Sara E. Weigel

  2. Department of Psychology, Kent State University, Kent, OH, USA

    F. Robert Treichler

  3. Department of Wildlife Management, North Slope Borough, Barrow, AK, USA

    Raphaela Stimmelmayr

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

    Camilla Butti & Patrick R. Hof

  5. Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, OH, USA

    J. G. M. Hans Thewissen

  6. New York Consortium in Evolutionary Primatology, New York, NY, USA

    Patrick R. Hof

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  1. Mary Ann Raghanti
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  2. Linda B. Spurlock
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Correspondence to Mary Ann Raghanti.

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Raghanti, M.A., Spurlock, L.B., Robert Treichler, F. et al. An analysis of von Economo neurons in the cerebral cortex of cetaceans, artiodactyls, and perissodactyls. Brain Struct Funct 220, 2303–2314 (2015). https://doi.org/10.1007/s00429-014-0792-y

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