How Does Connectivity Between Cortical Areas Depend on Brain Size? Implications for Efficient Computation

A formula for an average connectivity between cortical areas in mammals is derived. Based on comparative neuroanatomical data, it is found, surprisingly, that this connectivity is either only weakly dependent or independent of brain size. It is discussed how this formula can be used to estimate the average length of axons in white matter. Other allometric relations, such as cortical patches and area sizes vs. brain size, are also provided. Finally, some functional implications, with an emphasis on efficient cortical computation, are discussed as well.

[1]  S. Laughlin,et al.  An Energy Budget for Signaling in the Grey Matter of the Brain , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

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

[3]  R. Douglas,et al.  Opening the grey box , 1991, Trends in Neurosciences.

[4]  J L Ringo,et al.  Neuronal interconnection as a function of brain size. , 1991, Brain, behavior and evolution.

[5]  G Tononi,et al.  Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. , 2000, Cerebral cortex.

[6]  Daniel P. F. Sturdy,et al.  The connectivity of the brain: multi-level quantitative analysis , 1995, Biological Cybernetics.

[7]  C. Blakemore,et al.  Analysis of connectivity in the cat cerebral cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  Braitenberg,et al.  Cortical architectonics: General and areal , 1978 .

[9]  A. L. Humphrey,et al.  Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis) , 1982, The Journal of comparative neurology.

[10]  Valentino Braitenberg,et al.  Brain Size and Number of Neurons: An Exercise in Synthetic Neuroanatomy , 2004, Journal of Computational Neuroscience.

[11]  C. Cherniak Neural component placement , 1995, Trends in Neurosciences.

[12]  Charles F. Stevens,et al.  How Cortical Interconnectedness Varies with Network Size , 1989, Neural Computation.

[13]  G. Mitchison Axonal trees and cortical architecture , 1992, Trends in Neurosciences.

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

[15]  Jan Karbowski Optimal wiring in the cortex and neuronal degree of separation , 2002, Neurocomputing.

[16]  J. B. HURSHl CONDUCTION VELOCITY AND DIAMETER OF NERVE FIBERS , 2004 .

[17]  H. J. Jerison Brain size and the evolution of mind , 1991 .

[18]  Mark A. Changizi,et al.  Principles underlying mammalian neocortical scaling , 2001, Biological Cybernetics.

[19]  D. Pandya,et al.  Architecture and Connections of Cortical Association Areas , 1985 .

[20]  M. Young The organization of neural systems in the primate cerebral cortex , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[21]  A. Pestronk Histology of the Nervous System of Man and Vertebrates , 1997, Neurology.

[22]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[23]  M. Wong-Riley Cytochrome oxidase: an endogenous metabolic marker for neuronal activity , 1989, Trends in Neurosciences.

[24]  W. Singer,et al.  Development of horizontal intrinsic connections in cat striate cortex , 2004, Experimental Brain Research.

[25]  J. Karbowski Optimal wiring principle and plateaus in the degree of separation for cortical neurons. , 2001, Physical review letters.

[26]  Francisco Aboitiz,et al.  Species Differences and Similarities in the Fine Structure of the Mammalian Corpus callosum , 2001, Brain, Behavior and Evolution.

[27]  J. Kaas,et al.  The evolution of isocortex. , 1995, Brain, behavior and evolution.

[28]  Leah Krubitzer,et al.  Organization of sensory cortex in a Madagascan insectivore, the tenrec (Echinops telfairi) , 1997, The Journal of comparative neurology.

[29]  William B. Levy,et al.  Energy Efficient Neural Codes , 1996, Neural Computation.

[30]  R. Malach,et al.  Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex , 1993, The Journal of comparative neurology.

[31]  A. Burkhalter,et al.  Organization of corticocortical connections in human visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Lund,et al.  Intra- and inter-areal connections between the primary visual cortex V1 and the area immediately surrounding V1 in the rat , 2001, Neuroscience.

[33]  W. Rushton A theory of the effects of fibre size in medullated nerve , 1951, The Journal of physiology.

[34]  R. Shulman,et al.  Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Prof. Dr. Dr. Valentino Braitenberg,et al.  Cortex: Statistics and Geometry of Neuronal Connectivity , 1998, Springer Berlin Heidelberg.

[36]  H. Frahm,et al.  Comparison of brain structure volumes in Insectivora and Primates. I. Neocortex. , 1982, Journal fur Hirnforschung.

[37]  Jack W Scannell,et al.  The connectional organization of neural systems in the cat cerebral cortex , 1993, Current Biology.

[38]  J. Sundsten,et al.  Folding of the Cerebral Cortex in Mammals , 1984 .

[39]  T. Sejnowski,et al.  A universal scaling law between gray matter and white matter of cerebral cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Peter T. Fox,et al.  Mosaic evolution of brain structure in mammals , 2022 .

[41]  J. Kaas The organization of neocortex in mammals: implications for theories of brain function. , 1987, Annual review of psychology.

[42]  Rob R. de Ruyter van Steveninck,et al.  The metabolic cost of neural information , 1998, Nature Neuroscience.

[43]  V. Caviness Architectonic map of neocortex of the normal mouse , 1975, The Journal of comparative neurology.

[44]  Malcolm P. Young,et al.  Objective analysis of the topological organization of the primate cortical visual system , 1992, Nature.

[45]  S. Shipp,et al.  The functional logic of cortical connections , 1988, Nature.

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

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

[48]  R G Shulman,et al.  Interpreting functional imaging studies in terms of neurotransmitter cycling. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Almut Schüz Patterns of cortico-cortical connections in the mouse , 2001 .

[50]  Jon H. Kaas,et al.  Why is Brain Size so Important:Design Problems and Solutions as Neocortex Gets Biggeror Smaller , 2000 .

[51]  H. Frahm,et al.  New and revised data on volumes of brain structures in insectivores and primates. , 1981, Folia primatologica; international journal of primatology.

[52]  Dmitri B. Chklovskii,et al.  Wiring Optimization in the Brain , 1999, NIPS.

[53]  Leah Krubitzer,et al.  Arealization of the Neocortex in Mammals: Genetic and Epigenetic Contributions to the Phenotype , 2000, Brain, Behavior and Evolution.

[54]  Patrice Y. Simard,et al.  Time is of the essence: a conjecture that hemispheric specialization arises from interhemispheric conduction delay. , 1994, Cerebral cortex.

[55]  M. Hofman Energy Metabolism, Brain Size and Longevity in Mammals , 1983, The Quarterly Review of Biology.

[56]  A. Schüz,et al.  Basic Connectivity of the Cerebral Cortex and some Considerations on the Corpus Callosum , 1996, Neuroscience & Biobehavioral Reviews.

[57]  Jon H Kaas,et al.  The organization of sensory cortex , 2001, Current Opinion in Neurobiology.

[58]  M. Hofman Size and shape of the cerebral cortex in mammals. I. The cortical surface. , 1985, Brain, behavior and evolution.

[59]  Gully A. P. C. Burns,et al.  The Analysis of Cortical Connectivity , 1995 .

[60]  A. Schüz,et al.  Constancy and variability in cortical structure. A study on synapses and dendritic spines in hedgehog and monkey. , 1995, Journal fur Hirnforschung.