The neocortex of cetartiodactyls: I. A comparative Golgi analysis of neuronal morphology in the bottlenose dolphin (Tursiops truncatus), the minke whale (Balaenoptera acutorostrata), and the humpback whale (Megaptera novaeangliae)

Abstract

The present study documents the morphology of neurons in several regions of the neocortex from the bottlenose dolphin (Tursiops truncatus), the North Atlantic minke whale (Balaenoptera acutorostrata), and the humpback whale (Megaptera novaeangliae). Golgi-stained neurons (n = 210) were analyzed in the frontal and temporal neocortex as well as in the primary visual and primary motor areas. Qualitatively, all three species exhibited a diversity of neuronal morphologies, with spiny neurons including typical pyramidal types, similar to those observed in primates and rodents, as well as other spiny neuron types that had more variable morphology and/or orientation. Five neuron types, with a vertical apical dendrite, approximated the general pyramidal neuron morphology (i.e., typical pyramidal, extraverted, magnopyramidal, multiapical, and bitufted neurons), with a predominance of typical and extraverted pyramidal neurons. In what may represent a cetacean morphological apomorphy, both typical pyramidal and magnopyramidal neurons frequently exhibited a tri-tufted variant. In the humpback whale, there were also large, star-like neurons with no discernable apical dendrite. Aspiny bipolar and multipolar interneurons were morphologically consistent with those reported previously in other mammals. Quantitative analyses showed that neuronal size and dendritic extent increased in association with body size and brain mass (bottlenose dolphin < minke whale < humpback whale). The present data thus suggest that certain spiny neuron morphologies may be apomorphies in the neocortex of cetaceans as compared to other mammals and that neuronal dendritic extent covaries with brain and body size.

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Acknowledgments

Partial support for this work was provided by Colorado College’s divisional research funds (B.J.), the James S. McDonnell Foundation (Grants 22002078 to C.C.S. and P.R.H., and 220020293 to C.C.S.), and the National Science Foundation (Grants BCS-0515484 and BCS-0824531 to C.C.S.). The authors wish to thank Ms. Kimberly Durham, Mr. Robert DiGiovanni, Ms. Julika N. Wocial, and The Riverhead Foundation for Marine Research and Preservation for precious help during samples collection under MMHSRP’s MMPA/ESA Enhancement and Scientific Research Permit NMFS Permit No. 932-1905/MA-009526, and the National Marine Fisheries Service (NOAA Fisheries) for permission to collect samples from stranded specimens to Dr. Joy Reidenberg.

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Butti, C., Janeway, C.M., Townshend, C. et al. The neocortex of cetartiodactyls: I. A comparative Golgi analysis of neuronal morphology in the bottlenose dolphin (Tursiops truncatus), the minke whale (Balaenoptera acutorostrata), and the humpback whale (Megaptera novaeangliae). Brain Struct Funct 220, 3339–3368 (2015). https://doi.org/10.1007/s00429-014-0860-3

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Keywords

  • Cetacean neocortex
  • Neuronal morphology
  • Golgi method
  • Brain evolution