Von Economo Neurons in the Brain of Cetaceans: Distribution and Quantification
Department of Neuroscience, Mount Sinai School of Medicine, New York, NY, USA
Abstract
The anterior cingulate, anterior insular and frontopolar cortices of cetaceans are characterized by the presence in layer V of a class of bipolar and large-sized projection neurons thought to play a crucial role in the neural circuitry responsible for social awareness and assessment of complex social situations: the Von Economo neurons (VENs).1,4 Von Economo neurons have been previously described in layer V of the anterior insular and anterior cingulate cortices of humans, great apes,7,8 and elephants,3 and in layer V of the dorsolateral prefrontal cortex of humans.2 The loss, morphological alteration or abnormal development and distribution of VENs in humans are known to be related to a wide spectrum of neuropsychiatric conditions such as frontotemporal dementia, schizophrenia and autism. The selective distribution of VENs in the cetacean brain is intriguing and consistent with the growing evidence of their sophisticated cognitive abilities and social lifestyles such as complex social structures, long-term bonds, higher-order alliances, cooperative networks, cultural transmission, tool use, and mirror self-recognition.5,6,9 In an attempt to understand the neuroanatomical basis of cognition in cetaceans, we used a stereological approach to obtain volume estimates and to perform an exhaustive count of the total number of VENs in the anterior cingulate, anterior insular and frontopolar cortices of representative taxa of the order Cetacea such as the bottlenose dolphin (Tursiops truncatus), the Risso's dolphin (Grampus griseus), the beluga whale (Delphinapterus leucas), and the humpback whale (Megaptera novaeangliae). Our results show that in the cetacean neocortex, similarly to what has been previously described in great apes, VENs have a larger volume than neighboring layer V pyramidal cell and fusiform neurons of layer VI and they are mainly concentrated at the crown of the gyri. The presence and the comparable distribution of VENs in unrelated taxa such as cetaceans, great apes and elephants provides support to the hypothesis that VENs may be the evolutionary selected adaptation necessary to permit, in large brains, fast information processing along highly specific network involved in complex social behaviors. In the specific case of cetaceans, the presence of VENs in both odontocetes and mysticetes may be the anatomical basis for the observed cognitive convergences that are widely recognized to be shared by primates and cetaceans.
Acknowledgements
The authors thank Drs. P.J. Morgane and I.I. Glezer for donation of the humpback whale and beluga whale brain specimens and the collections of histological slides, and the Mediterranean Marine Mammals Tissue Bank of the University of Padova for generous provision of material from the bottlenose and Risso's dolphins. Sponsored by The James S. McDonnell Foundation; Grant number: 22002078.
References
1. Allman J.M., K.K. Watson, N.A. Tetreault, and A.Y. Hakeem. 2005. Intuition and autism: a possible role for Von Economo neurons. Trends Cogn Sci 9: 367-373.
2. Fajardo C., M.I. Escobar, E. Buritica, G. Arteaga, J. Umbarila, M.F. Casanova, and H. Pimienta. 2008. Von Economo neurons are present in the dorsolateral (dysgranular) prefrontal cortex of humans. Neurosci Lett 435: 215-218.
3. Hakeem A.Y., C.C. Sherwood, C.J. Bonar, C. Butti, P.R. Hof, and J.M. Allman. 2009. Von Economo neurons in the elephant brain. Anat Rec (Hoboken) 292(2): 242-8.
4. Hof P.R., and E. Van der Gucht. 2007. Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anat Rec 290: 1-31.
5. Krushinskaya N.L. 1986. The behaviour of cetaceans. Invest Cetacea 19: 115-273.
6. Marino L., R.C. Connor, R.E. Fordyce, L.M. Herman, P.R. Hof, L. Lefebvre, D. Lusseau, B. McCowan, E.A. Nimchinsky, A.A. Pack, L. Rendell, J.S. Reidenberg, D. Reiss, M.D. Uhen, E. Van der Gucht, and H. Whitehead. 2007. Cetaceans have complex brains for complex cognition. PLoS Biol 5(5): e139.
7. Nimchinsky E.A., E. Gilissen, J.M. Allman, D.P. Perl, J.M. Erwin, and P.R. Hof. 1999. A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci USA 96: 5268-5273.
8. Nimchinsky, E.A., B.A. Vogt, J.J. Morrison, and P.R. Hof. 1995. Spindle neurons of the human anterior cingulate cortex. J Comp Neurol 355: 27-37.
9. Reiss D., and L. Marino. 2001. Mirror self-recognition in the bottlenose dolphin: a case of cognitive convergence. Proc Natl Acad Sci USA 98(10): 5937-5942.