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Neuroanatomy of the killer whale (Orcinus orca): a magnetic resonance imaging investigation of structure with insights on function and evolution

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Abstract

The evolutionary process of adaptation to an obligatory aquatic existence dramatically modified cetacean brain structure and function. The brain of the killer whale (Orcinus orca) may be the largest of all taxa supporting a panoply of cognitive, sensory, and sensorimotor abilities. Despite this, examination of the O. orca brain has been limited in scope resulting in significant deficits in knowledge concerning its structure and function. The present study aims to describe the neural organization and potential function of the O. orca brain while linking these traits to potential evolutionary drivers. Magnetic resonance imaging was used for volumetric analysis and three-dimensional reconstruction of an in situ postmortem O. orca brain. Measurements were determined for cortical gray and cerebral white matter, subcortical nuclei, cerebellar gray and white matter, corpus callosum, hippocampi, superior and inferior colliculi, and neuroendocrine structures. With cerebral volume comprising 81.51 % of the total brain volume, this O. orca brain is one of the most corticalized mammalian brains studied to date. O. orca and other delphinoid cetaceans exhibit isometric scaling of cerebral white matter with increasing brain size, a trait that violates an otherwise evolutionarily conserved cerebral scaling law. Using comparative neurobiology, it is argued that the divergent cerebral morphology of delphinoid cetaceans compared to other mammalian taxa may have evolved in response to the sensorimotor demands of the aquatic environment. Furthermore, selective pressures associated with the evolution of echolocation and unihemispheric sleep are implicated in substructure morphology and function. This neuroanatomical dataset, heretofore absent from the literature, provides important quantitative data to test hypotheses regarding brain structure, function, and evolution within Cetacea and across Mammalia.

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Acknowledgments

The authors sincerely thank Erika Nilson for preparation of the specimen, Sharon Birzer for illustration, and Paul Ponganis for valuable manuscript feedback. The authors also thank Hauke Bartsch for improved visualization of MR images (Fig. 2 and Online Resource 1) through MR image preprocessing to remove intensity non-uniformity using the Non-parametric Non-uniform intensity Normalization (N3) algorithm as implemented in ITK (http://github.com/HaukeBartsch/itkN3). AW was supported by the National Science Foundation Graduate Research Fellowship Program. The funder had no role in the study design, data collection, analysis, or interpretation, preparation of the manuscript, or decision to publish.

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Authors and Affiliations

  1. Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA, 92093, USA

    Alexandra Wright

  2. Center for Functional MRI, Department of Radiology, University of California, San Diego, La Jolla, CA, 92093, USA

    Miriam Scadeng, Dominik Stec & Rebecca Dubowitz

  3. National Marine Mammal Foundation, San Diego, CA, 92106, USA

    Sam Ridgway

  4. SeaWorld San Diego, 500 SeaWorld Drive, San Diego, CA, 92109, USA

    Judy St. Leger

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  1. Alexandra Wright
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Correspondence to Alexandra Wright.

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AW, MS, DS, RD, and SR declare that they have no conflict of interest. JSL is a paid employee of SeaWorld Parks and Entertainment. No live animals were used for this study. The O. orca specimen was examined opportunistically during postmortem investigation.

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429_2016_1225_MOESM1_ESM.pdf

Online Resource 1. Annotated frontal, horizontal, and sagittal MR images of the O. orca brain. Anatomical directions: A (anterior), P (posterior), D (dorsal), V (ventral), R (right), and L (left) (PDF 2358 kb)

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Wright, A., Scadeng, M., Stec, D. et al. Neuroanatomy of the killer whale (Orcinus orca): a magnetic resonance imaging investigation of structure with insights on function and evolution. Brain Struct Funct 222, 417–436 (2017). https://doi.org/10.1007/s00429-016-1225-x

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