Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species

The mammalian cerebral cortex is composed of individual layers characterized by the cell types they contain and their afferent and efferent connections. The current study examined the raw, and size-normalized, laminar thicknesses in three cortical regions (somatosensory, motor, and premotor) of fourteen species from three orders of mammals: primates, carnivores, and rodents. The proportional size of the pyramidal cell layers (supra- and infragranular) varied between orders but was similar within orders despite wide variance in absolute cortical thickness. Further, supragranular layer thickness was largest in primates (46 +/- 3 percent), followed by carnivores (36 +/- 3 percent), and then rodents (19 +/- 4 percent), suggesting a distinct difference in the proportion of cortex devoted to corticocortical connectivity across these orders. Although measures of supragranular layer thickness are highly correlated with measures of overall brain size, such associations are not present when independent contrasts are used to control for phylogenetic inertia. Interestingly, neurogenesis time span remains strongly associated with supragranular layer thickness despite size normalization and controlling for phylogenetic inertia. Such layering differences between orders, and similarities amongst species within an order, suggest that supragranular layer expansion may have occurred early in mammalian evolution and may be related to ontogenetic variables such as neurogenesis time span rather than measures of overall size.

[1]  D. L. Adams,et al.  Capricious expression of cortical columns in the primate brain , 2003, Nature Neuroscience.

[2]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[3]  T. Sawaguchi,et al.  A hypothesis on the primate neocortex evolution: column-multiplication hypothesis. , 1986, The International journal of neuroscience.

[4]  B. Finlay,et al.  Neural development in metatherian and eutherian mammals: Variation and constraint , 1999, The Journal of comparative neurology.

[5]  Andrew Rambaut,et al.  Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data , 1995, Comput. Appl. Biosci..

[6]  L. Krubitzer The organization of neocortex in mammals: are species differences really so different? , 1995, Trends in Neurosciences.

[7]  M. Pagel,et al.  The comparative method in evolutionary biology , 1991 .

[8]  Matthew H. Nitecki,et al.  Some Other Books of Interest. (Book Reviews: Extinctions; Orders and Families of Recent Mammals of the World) , 1985 .

[9]  Vernon B Mountcastle,et al.  Introduction. Computation in cortical columns. , 2003, Cerebral cortex.

[10]  David W. Macdonald,et al.  The Encyclopedia of Mammals , 1984 .

[11]  D. Morris The Mammals: A Guide to the Living Species , 1965 .

[12]  Lockard Bi The forebrain of the ferret. , 1985 .

[13]  R. Nowak,et al.  Walker's mammals of the world , 1968 .

[14]  O. S. Adrianov,et al.  Atlas of the Canine Brain , 1964 .

[15]  J F Fulton,et al.  Physiology of the Nervous System , 1939, Science.

[16]  K. Laland,et al.  Social intelligence, innovation, and enhanced brain size in primates , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[17]  H. Plotkin,et al.  Brain, Behaviour, and Evolution , 1979 .

[18]  M Litaker,et al.  Morphological differences between minicolumns in human and nonhuman primate cortex. , 2001, American journal of physical anthropology.

[19]  F. O. Schmitt,et al.  The Organization of the Cerebral Cortex. , 1982 .

[20]  Lynn Nadel,et al.  Encyclopedia of Cognitive Science , 2003 .

[21]  R. Sidman,et al.  Atlas of the Mouse Brain and Spinal Cord , 1971 .

[22]  M. Carpenter A Stereotaxic Atlas of the Chimpanzee Brain. , 1965 .

[23]  M. Carpenter The cerebral cortex , 1976 .

[24]  S. Cajal New Ideas on the Structure of the Nervous System in Man and Vertebrates , 1990 .

[25]  D. Buxhoeveden,et al.  The minicolumn hypothesis in neuroscience. , 2002, Brain : a journal of neurology.

[26]  H. Supèr,et al.  The early differentiation of the neocortex: a hypothesis on neocortical evolution. , 2001, Cerebral cortex.

[27]  Andrew E. Switala,et al.  Quantitative analysis of cell columns in the cerebral cortex , 2000, Journal of Neuroscience Methods.

[28]  B. Finlay,et al.  Translating developmental time across mammalian species , 2001, Neuroscience.

[29]  Alan Peters,et al.  Comparative Structure and Evolution of Cerebral Cortex, Part I , 1990, Cerebral Cortex.

[30]  B. Finlay,et al.  Linked regularities in the development and evolution of mammalian brains. , 1995, Science.

[31]  Andy Purvis,et al.  Comparative methods for explaining adaptations , 1991, Nature.

[32]  H. J. Jerison,et al.  Evolution of the Brain and Intelligence , 1973 .

[33]  Larry W. Swanson,et al.  Photographic Atlas of the Rat Brain: The Cell and Fiber Architecture Illustrated in Three Planes with Stereotaxic Coordinates , 1995 .

[34]  P. Rakic Specification of cerebral cortical areas. , 1988, Science.

[35]  T. Powell,et al.  The basic uniformity in structure of the neocortex. , 1980, Brain : a journal of neurology.

[36]  R. Guillery Histology of the Nervous System by Santiago Ramón y Cajal. Translated into English from the French edition by Neely Swanson and Larry W. Swanson, Oxford University Press, 1995. $195.00 (1672 pp) ISBN 0 19 507 4017 , 1996, Trends in Neurosciences.

[37]  C. Beaulieu,et al.  Numerical data on neocortical neurons in adult rat, with special reference to the GABA population , 1993, Brain Research.

[38]  S. Cajal Cajal on the cerebral cortex , 1988 .

[39]  J. J. Flynn,et al.  Phylogeny of the Carnivora (Mammalia): congruence vs incompatibility among multiple data sets. , 1998, Molecular phylogenetics and evolution.

[40]  J. Fuster Cortex and Mind , 2002 .

[41]  Ray S. Snider,et al.  A stereotaxic atlas of the cat brain , 1987 .

[42]  G. Elston,et al.  Pyramidal Cells, Patches, and Cortical Columns: a Comparative Study of Infragranular Neurons in TEO, TE, and the Superior Temporal Polysensory Area of the Macaque Monkey , 2000, The Journal of Neuroscience.

[43]  Prof. Dr. Heiko Braak,et al.  Architectonics of the Human Telencephalic Cortex , 1980, Studies of Brain Function.

[44]  R. Pascher,et al.  Heterogeneity in the columnar number of neurons in different neocortical areas in the rat , 1996, Neuroscience Letters.

[45]  K Zilles,et al.  Limbic frontal cortex in hominoids: a comparative study of area 13. , 1998, American journal of physical anthropology.

[46]  Joaquín M. Fuster Neurobiology of Cortical Networks , 2005 .

[47]  Functional neuroimaging in child psychiatry: Brain development and evolution , 2000 .

[48]  M Marín-Padilla,et al.  Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: A unifying theory , 1992, The Journal of comparative neurology.

[49]  P. Rakić,et al.  Changes in cell-cycle kinetics during the development and evolution of primate neocortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[50]  M. Carpenter,et al.  A Stereotaxic Atlas of the Brain of the Squirrel Monkey. , 1963 .

[51]  W. Welker,et al.  Comparisons between brains of a large and a small hystricomorph rodent: capybara, Hydrochoerus and guinea pig, Cavia; neocortical projection regions and measurements of brain subdivisions. , 1976, Brain, behavior and evolution.

[52]  G. Edelman,et al.  The Mindful Brain: Cortical Organization and the Group-Selective Theory of Higher Brain Function , 1978 .

[53]  J. Hill,et al.  A world list of mammalian species , 1980 .

[54]  A. Hopf,et al.  The Yakovlev Collection. A unique resource for brain research and the basis for a multinational data bank. , 1982, Journal fur Hirnforschung.

[55]  Miguel Marín-Padilla,et al.  Cajal–Retzius cells and the development of the neocortex , 1998, Trends in Neurosciences.

[56]  G. Bonin,et al.  The isocortex of man , 1951 .

[57]  M. Hofman On the evolution and geometry of the brain in mammals , 1989, Progress in Neurobiology.

[58]  T. Preuss Taking the Measure of Diversity: Comparative Alternatives to the Model-Animal Paradigm in Cortical Neuroscience , 2000, Brain, Behavior and Evolution.

[59]  P. Rakic,et al.  Radial unit hypothesis of neocortical expansion. , 2000, Novartis Foundation symposium.

[60]  B. Finlay,et al.  The course of human events: predicting the timing of primate neural development , 2000 .

[61]  S. Gould,et al.  Ontogeny and Phylogeny , 1978 .

[62]  T. Preuss Preface: From Basic Uniformity to Diversity in Cortical Organization , 2000, Brain, Behavior and Evolution.

[63]  W. Luckett,et al.  Monophyly or polyphyly of the order Rodentia: Possible conflict between morphological and molecular interpretations , 1993, Journal of Mammalian Evolution.

[64]  B. Weir Introduction to rodents , 1987 .

[65]  R. Galuske,et al.  Hemispheric asymmetries in cerebral cortical networks , 2003, Trends in Neurosciences.

[66]  P. Rakic A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution , 1995, Trends in Neurosciences.

[67]  Pasko Rakic,et al.  Developmental and evolutionary adaptations of cortical radial glia. , 2003, Cerebral cortex.

[68]  V. Caviness,et al.  Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model , 1995, Trends in Neurosciences.

[69]  P. Rakic Progress: Neurogenesis in adult primate neocortex: an evaluation of the evidence , 2002, Nature Reviews Neuroscience.

[70]  H. Kennedy,et al.  Non-uniformity of neocortex: areal heterogeneity of NADPH-diaphorase reactive neurons in adult macaque monkeys. , 2000, Cerebral cortex.

[71]  B. Dreher,et al.  The visual pathways of eutherian mammals and marsupials develop according to a common timetable. , 1990, Brain, behavior and evolution.

[72]  A. Purvis A composite estimate of primate phylogeny. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[73]  E. G. Jones,et al.  Microcolumns in the cerebral cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[74]  G. Elston Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. , 2003, Cerebral cortex.

[75]  E. Macphail Brain and Intelligence in Vertebrates , 1982 .

[76]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[77]  Alan Peters,et al.  Comparative structure and evolution of cerebral cortex , 1990 .

[78]  M. Ernst,et al.  Functional neuroimaging in child psychiatry , 2001, Current psychiatry reports.

[79]  P. Rakić,et al.  Genetic control of cortical development. , 1999, Cerebral cortex.