Total number and volume of Von Economo neurons in the cerebral cortex of cetaceans

Von Economo neurons (VENs) are a type of large, layer V spindle‐shaped neurons that were previously described in humans, great apes, elephants, and some large‐brained cetaceans. Here we report the presence of Von Economo neurons in the anterior cingulate (ACC), anterior insular (AI), and frontopolar (FP) cortices of small odontocetes, including the bottlenose dolphin (Tursiops truncatus), the Risso's dolphin (Grampus griseus), and the beluga whale (Delphinapterus leucas). The total number and volume of VENs and the volume of neighboring layer V pyramidal neurons and layer VI fusiform neurons were obtained by using a design‐based stereologic approach. Two humpback whale (Megaptera novaeangliae) brains were investigated for comparative purposes as representatives of the suborder Mysticeti. Our results show that the distribution of VENs in these cetacean species is comparable to that reported in humans, great apes, and elephants. The number of VENs in these cetaceans is also comparable to data available from great apes, and stereologic estimates indicate that VEN volume follows in these cetacean species a pattern similar to that in hominids, the VENs being larger than neighboring layer V pyramidal cells and conspicuously larger than fusiform neurons of layer VI. The fact that VENs are found in species representative of both cetacean suborders in addition to hominids and elephants suggests that these particular neurons have appeared convergently in phylogenetically unrelated groups of mammals possibly under the influence of comparable selective pressures that influenced specifically the evolution of cortical domains involved in complex cognitive and social/emotional processes. J. Comp. Neurol. 515:243–259, 2009. © 2009 Wiley‐Liss, Inc.

[1]  Soyoung Q. Park,et al.  The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans , 2010, Brain Structure and Function.

[2]  Patrick R Hof,et al.  Von Economo Neurons in the Elephant Brain , 2009, Anatomical record.

[3]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[4]  L. Lefebvre,et al.  A claim in search of evidence: reply to Manger’s thermogenesis hypothesis of cetacean brain structure , 2008, Biological reviews of the Cambridge Philosophical Society.

[5]  J. Allman,et al.  Selective reduction of Von Economo neuron number in agenesis of the corpus callosum , 2008, Acta Neuropathologica.

[6]  I. Agnarsson,et al.  The phylogeny of Cetartiodactyla: the importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies. , 2008, Molecular phylogenetics and evolution.

[7]  M. Casanova,et al.  Von Economo neurons are present in the dorsolateral (dysgranular) prefrontal cortex of humans , 2008, Neuroscience Letters.

[8]  Helen Barbas,et al.  Sequence of information processing for emotions through pathways linking temporal and insular cortices with the amygdala , 2008, NeuroImage.

[9]  Patrick R Hof,et al.  Functional Trade-Offs in White Matter Axonal Scaling , 2008, The Journal of Neuroscience.

[10]  J. Poole,et al.  Elephant sociality and complexity : the scientific evidence , 2008 .

[11]  Michael D Greicius,et al.  Divergent Social Functioning in Behavioral Variant Frontotemporal Dementia and Alzheimer Disease: Reciprocal Networks and Neuronal Evolution , 2007, Alzheimer disease and associated disorders.

[12]  Lori Marino,et al.  Cetacean brains: How aquatic are they? , 2007, Anatomical record.

[13]  L. Lefebvre,et al.  Cetaceans Have Complex Brains for Complex Cognition , 2007, PLoS biology.

[14]  B. Pakkenberg,et al.  Total neocortical cell number in the mysticete brain , 2007, Anatomical record.

[15]  Patrick R Hof,et al.  Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae) , 2007, Anatomical record.

[16]  J. Allman,et al.  Dendritic architecture of the von Economo neurons , 2006, Neuroscience.

[17]  J. Allman,et al.  Early frontotemporal dementia targets neurons unique to apes and humans , 2006, Annals of neurology.

[18]  Diana Reiss,et al.  Self-recognition in an Asian elephant , 2006, Proceedings of the National Academy of Sciences.

[19]  D. Lusseau Evidence for social role in a dolphin social network , 2006, Evolutionary Ecology.

[20]  P. Manger An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain , 2006, Biological reviews of the Cambridge Philosophical Society.

[21]  P. R. Hof,et al.  Design-based stereology in neuroscience , 2005, Neuroscience.

[22]  Patrick R Hof,et al.  Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[23]  P. Hof,et al.  Animal Studies Repository Animal Studies Repository Cortical Complexity in Cetacean Brains , 2022 .

[24]  O. Güntürkün,et al.  Neuron numbers in sensory cortices of five delphinids compared to a physeterid, the pygmy sperm whale , 2005, Brain Research Bulletin.

[25]  J. Allman,et al.  Intuition and autism: a possible role for Von Economo neurons , 2005, Trends in Cognitive Sciences.

[26]  J. Mann,et al.  Cultural transmission of tool use in bottlenose dolphins. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[27]  G. Roth,et al.  Evolution of the brain and intelligence , 2005, Trends in Cognitive Sciences.

[28]  M. Brunet,et al.  The position of Hippopotamidae within Cetartiodactyla. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  D. McShea,et al.  Origin and evolution of large brains in toothed whales. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[30]  A. D. Craig,et al.  Human feelings: why are some more aware than others? , 2004, Trends in Cognitive Sciences.

[31]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[32]  H. Stephan,et al.  Quantitative neuroanatomy of the brain of the La Plata dolphin, Pontoporia blainvillei , 2004, Anatomy and Embryology.

[33]  H. Barbas,et al.  Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression , 2003, BMC Neuroscience.

[34]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

[35]  P. Hof,et al.  Stereologic characterization and spatial distribution patterns of Betz cells in the human primary motor cortex. , 2003, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[36]  Chet C. Sherwood,et al.  Evolution of Specialized Pyramidal Neurons in Primate Visual and Motor Cortex , 2003, Brain, Behavior and Evolution.

[37]  Patrick R Hof,et al.  Altered spatial arrangement of layer V pyramidal cells in the mouse brain following prenatal low-dose X-irradiation. A stereological study using a novel three-dimensional analysis method to estimate the nearest neighbor distance distributions of cells in thick sections. , 2002, Cerebral cortex.

[38]  R. Dolan,et al.  An fMRI study of intentional and unintentional (embarrassing) violations of social norms. , 2002, Brain : a journal of neurology.

[39]  J. Allman,et al.  Book Review: Two Phylogenetic Specializations in the Human Brain , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[40]  L. Marino Convergence of Complex Cognitive Abilities in Cetaceans and Primates , 2002, Brain, Behavior and Evolution.

[41]  Philip D. Gingerich,et al.  Origin of Whales from Early Artiodactyls: Hands and Feet of Eocene Protocetidae from Pakistan , 2001, Science.

[42]  D. Reiss,et al.  Mirror self-recognition in the bottlenose dolphin: A case of cognitive convergence , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Bernd Würsig,et al.  Encyclopedia of Marine Mammals , 2001 .

[44]  Christoph Schmitz,et al.  Use of cryostat sections from snap-frozen nervous tissue for combining stereological estimates with histological, cellular, or molecular analyses on adjacent sections , 2000, Journal of Chemical Neuroanatomy.

[45]  N. Alpert,et al.  Activation of anterior paralimbic structures during guilt-related script-driven imagery , 2000, Biological Psychiatry.

[46]  J. Morrison,et al.  Numbers of Meynert and layer IVB cells in area V1: A stereologic analysis in young and aged macaque monkeys , 2000, The Journal of comparative neurology.

[47]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[48]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[49]  J. Allman,et al.  A neuronal morphologic type unique to humans and great apes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Phillips,et al.  Growing up with dinosaurs: molecular dates and the mammalian radiation. , 1999, Trends in ecology & evolution.

[51]  N. M. Brooke,et al.  A molecular timescale for vertebrate evolution , 1998, Nature.

[52]  Lori Marino,et al.  A Comparison of Encephalization between Odontocete Cetaceans and Anthropoid Primates , 1998, Brain, Behavior and Evolution.

[53]  L. Krubitzer,et al.  Modular Subdivisions of Dolphin Insular Cortex: Does Evolutionary History Repeat Itself? , 1998, Journal of Cognitive Neuroscience.

[54]  P. Gingerich,et al.  Likelihood estimation of the time of origin of Cetacea and the time of divergence of Cetacea and Artiodactyla , 1998 .

[55]  M. Bushnell,et al.  Pain affect encoded in human anterior cingulate but not somatosensory cortex. , 1997, Science.

[56]  H. Gundersen,et al.  The optical rotator , 1997, Journal of microscopy.

[57]  J. Gatesy More DNA support for a Cetacea/Hippopotamidae clade: the blood-clotting protein gene gamma-fibrinogen. , 1997, Molecular biology and evolution.

[58]  Alan C. Evans,et al.  Functional imaging of an illusion of pain , 1996, Nature.

[59]  J. Morrison,et al.  Spindle neurons of the human anterior cingul. Ate cortex , 1995, The Journal of comparative neurology.

[60]  L. Barnes,et al.  The Evolutionary History of Whales and Dolphins , 1994 .

[61]  L M Herman,et al.  Responses to anomalous gestural sequences by a language-trained dolphin: evidence for processing of semantic relations and syntactic information. , 1993, Journal of experimental psychology. General.

[62]  G. Behrmann Cytoarchitectonic studies of the cerebral cortex of the harbour porpoise, Phocoena Phocoena (Linné, 1758) , 1993 .

[63]  R. Connor,et al.  Two levels of alliance formation among male bottlenose dolphins (Tursiops sp.). , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[64]  H. Gundersen,et al.  Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator , 1991, The Anatomical record.

[65]  P. Morgane,et al.  Ultrastructure of synapses and golgi analysis of neurons in neocortex of the lateral gyrus (visual cortex) of the dolphin and pilot whale , 1990, Brain Research Bulletin.

[66]  H J Gundersen,et al.  The nucleator , 1988, Journal of microscopy.

[67]  P. Morgane,et al.  Visual cortex of the dolphin: An image analysis study , 1988, The Journal of comparative neurology.

[68]  H Haug,et al.  Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). , 1987, The American journal of anatomy.

[69]  G. Leuba,et al.  A quantitative study of neuronal and glial numerical density in the visual cortex of the bottlenose dolphin: Evidence for a specialized subarea and changes with age , 1986, The Journal of comparative neurology.

[70]  Natal'ja L. Krušinskaja The behaviour of cetaceans , 1986 .

[71]  A. Galaburda,et al.  The insular formations of the dolphin brain: Quantitative cytoarchitectonic studies of the insular component of the limbic lobe , 1984, The Journal of comparative neurology.

[72]  L. Herman,et al.  Comprehension of sentences by bottlenosed dolphins , 1984, Cognition.

[73]  P. Morgane,et al.  The limbic lobe of the dolphin brain: a quantitative cytoarchitectonic study. , 1982, Journal fur Hirnforschung.

[74]  Myron S. Jacobs,et al.  The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Surface configurations of the telencephalon of the bottlenose dolphin with comparative anatomical observations in four other cetacean species , 1980, Brain Research Bulletin.

[75]  The anatomy of the brain of the bottlenose dolphin, (Tursiops truncatus). Rhinic lobe (rhinencephalon): The archicortex , 1980, Pharmacology Biochemistry and Behavior.

[76]  P. Morgane,et al.  The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Rhinic lobe (rhinencephalon): The archicortex , 1979, Brain Research Bulletin.

[77]  P. Morgane,et al.  The anatomy of the brain of the bottlenose dolphin (Tursiops truncates). Rhinic lobe (rhinencephalon). I. The paleocortex , 1971, The Journal of comparative neurology.

[78]  D. B. Tower,et al.  Structural and functional organization of mammalian cerebral cortex: The correlation of neurone density with brain size. Cortical neurone density in the fin whale (Balaenoptera Physalus L.) with a note on the cortical neurone density in the Indian elephant , 1954, The Journal of comparative neurology.

[79]  I. Bertrand Techniques histologiques de neuropathologie , 1930 .

[80]  C. Economo,et al.  Eine neue art spezialzellen des lobus cinguli und lobus insulae , 1926 .