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Neocortical neuron types in Xenarthra and Afrotheria: implications for brain evolution in mammals

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Abstract

Interpreting the evolution of neuronal types in the cerebral cortex of mammals requires information from a diversity of species. However, there is currently a paucity of data from the Xenarthra and Afrotheria, two major phylogenetic groups that diverged close to the base of the eutherian mammal adaptive radiation. In this study, we used immunohistochemistry to examine the distribution and morphology of neocortical neurons stained for nonphosphorylated neurofilament protein, calbindin, calretinin, parvalbumin, and neuropeptide Y in three xenarthran species—the giant anteater (Myrmecophaga tridactyla), the lesser anteater (Tamandua tetradactyla), and the two-toed sloth (Choloepus didactylus)—and two afrotherian species—the rock hyrax (Procavia capensis) and the black and rufous giant elephant shrew (Rhynchocyon petersi). We also studied the distribution and morphology of astrocytes using glial fibrillary acidic protein as a marker. In all of these species, nonphosphorylated neurofilament protein-immunoreactive neurons predominated in layer V. These neurons exhibited diverse morphologies with regional variation. Specifically, high proportions of atypical neurofilament-enriched neuron classes were observed, including extraverted neurons, inverted pyramidal neurons, fusiform neurons, and other multipolar types. In addition, many projection neurons in layers II–III were found to contain calbindin. Among interneurons, parvalbumin- and calbindin-expressing cells were generally denser compared to calretinin-immunoreactive cells. We traced the evolution of certain cortical architectural traits using phylogenetic analysis. Based on our reconstruction of character evolution, we found that the living xenarthrans and afrotherians show many similarities to the stem eutherian mammal, whereas other eutherian lineages display a greater number of derived traits.

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Acknowledgments

We thank Chad Lennon and Amy Garrison for technical assistance and Dr. Mary Ann Raghanti for helpful discussion. This work was supported by the National Science Foundation (BCS-0515484, BCS-0549117, and BCS-0453005) and the James S. McDonnell Foundation (22002078).

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Authors and Affiliations

  1. Department of Anthropology, The George Washington University, 2110 G Street, NW, Washington, DC, 20052, USA

    Chet C. Sherwood & Cheryl D. Stimpson

  2. Department of Experimental Veterinary Science, University of Padova, Padova, Italy

    Camilla Butti

  3. Department of Neuroscience, Mount Sinai School of Medicine, New York, NY, 10029, USA

    Camilla Butti & Patrick R. Hof

  4. Cleveland Metroparks Zoo, Cleveland, OH, 44109, USA

    Christopher J. Bonar

  5. Philadelphia Zoo, Philadelphia, PA, 19104, USA

    Alisa L. Newton

  6. Division of Biology, California Institute of Technology, Pasadena, CA, 91125, USA

    John M. Allman

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

    Patrick R. Hof

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Correspondence to Chet C. Sherwood.

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Sherwood, C.C., Stimpson, C.D., Butti, C. et al. Neocortical neuron types in Xenarthra and Afrotheria: implications for brain evolution in mammals. Brain Struct Funct 213, 301–328 (2009). https://doi.org/10.1007/s00429-008-0198-9

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