Cortical heterogeneity: Implications for visual processing and polysensory integration

Recent studies have revealed substantial variation in pyramidal cell structure in different cortical areas. Moreover, cell morphology has been shown to vary in a systematic fashion such that cells in visual association areas are larger and more spinous than those in the primary visual area. Various aspects of these structural differences appear to be important in influencing neuronal function. At the cellular level, differences in the branching patterns in the dendritic arbour may allow for varying degrees of non-linear compartmentalisation. Differences in total dendritic length and spine number may determine the number of inputs integrated by individual cells. Variations in spine density and geometry may affect cooperativity of inputs and shunting inhibition, and the tangential dimension of the dendritic arbours may determine sampling strategies within cortex. At the systems level, regional variation in pyramidal cell structure may determine thedegree of recurrent excitation through reentrant circuits influencing the discharge properties of individual neurones and the functional signature of the circuits they compose. The ability of pyramidal neurones in visual areas of the parietal and temporal lobes to integrate large numbers of excitatory inputs may also facilitate cortical binding. Here I summarise what I consider to be among the most salient, and testable, aspects of an inter-relationship between morphological and functional heterogeneity in visual cortex.

[1]  Todd M. Preuss,et al.  Evolutionary Anatomy of the Primate Cerebral Cortex: The discovery of cerebral diversity: an unwelcome scientific revolution , 2001 .

[2]  J. Szentágothai The ‘module-concept’ in cerebral cortex architecture , 1975, Brain Research.

[3]  Kazuo Hikosaka,et al.  Tolerances of responses to visual patterns in neurons of the posterior inferotemporal cortex in the macaque against changing stimulus size and orientation, and deleting patterns , 1999, Behavioural Brain Research.

[4]  D. Ts'o,et al.  The organization of chromatic and spatial interactions in the primate striate cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  J. Kaas,et al.  The evolution of complex sensory systems in mammals. , 1989, The Journal of experimental biology.

[6]  H. Tamura,et al.  Contribution of GABAergic inhibition to receptive field structures of monkey inferior temporal neurons. , 2002, Cerebral cortex.

[7]  I. Fujita,et al.  Contrasting forms of synaptic plasticity in monkey inferotemporal and primary visual cortices , 1997, Neuroreport.

[8]  A. Cowey,et al.  Patterns of inter- and intralaminar GABAergic connections distinguish striate (V1) and extrastriate (V2, V4) visual cortices and their functionally specialized subdivisions in the rhesus monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[10]  U. Eysel,et al.  Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17) , 1992, Neuroscience.

[11]  U. Eysel,et al.  Network of GABAergic large basket cells in cat visual cortex (area 18): Implication for lateral disinhibition , 1993, The Journal of comparative neurology.

[12]  P. Lennie Single Units and Visual Cortical Organization , 1998, Perception.

[13]  R. Desimone,et al.  Inferior temporal mechanisms for invariant object recognition. , 1994, Cerebral cortex.

[14]  V. Mountcastle The evolution of ideas concerning the function of the neocortex. , 1995, Cerebral cortex.

[15]  K. Rockland,et al.  Bistratified distribution of terminal arbors of individual axons projecting from area V1 to middle temporal area (MT) in the macaque monkey , 1989, Visual Neuroscience.

[16]  T. Sejnowski,et al.  [Letters to nature] , 1996, Nature.

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

[18]  P. Somogyi,et al.  Targets and Quantitative Distribution of GABAergic Synapses in the Visual Cortex of the Cat , 1990, The European journal of neuroscience.

[19]  A. Cowey,et al.  Vertical organization of neurones accumulating 3H-GABA in visual cortex of rhesus monkey , 1981, Nature.

[20]  D. Whitteridge,et al.  Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex , 2004, Experimental Brain Research.

[21]  Karl Zilles,et al.  Architecture, Connectivity, and Transmitter Receptors of Human Extrastriate Visual Cortex , 1997 .

[22]  K. Rockland,et al.  The pyramidal cell of the sensorimotor cortex of the macaque monkey: phenotypic variation. , 2002, Cerebral cortex.

[23]  T. Wiesel,et al.  Clustered intrinsic connections in cat visual cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Jon H. Kaas,et al.  12 – The Organization of Sensory and Motor Cortex in Owl Monkeys , 1994 .

[25]  J. Morrison,et al.  Chapter II Neurochemical organization of the primate visual cortex , 1998 .

[26]  G. Elston Pyramidal cell heterogeneity in the visual cortex of the nocturnal new world owl monkey (aotus trivirgatus) , 2003, Neuroscience.

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

[28]  J. Lund,et al.  Widespread periodic intrinsic connections in the tree shrew visual cortex. , 1982, Science.

[29]  G. Elston The pyramidal neuron in occipital, temporal and prefrontal cortex of the owl monkey (Aotus trivirgatus): regional specialization in cell structure , 2003, The European journal of neuroscience.

[30]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

[31]  Bartlett W. Mel Synaptic integration in an excitable dendritic tree. , 1993, Journal of neurophysiology.

[32]  D. Prince,et al.  Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features , 1990, The Journal of comparative neurology.

[33]  J. Ringo,et al.  Investigation of long term recognition and association memory in unit responses from inferotemporal cortex , 1993, Experimental Brain Research.

[34]  L A Krubitzer,et al.  How does evolution build a complex brain? , 2000, Novartis Foundation symposium.

[35]  W Rall,et al.  Matching dendritic neuron models to experimental data. , 1992, Physiological reviews.

[36]  Alan Cowey,et al.  The neurobiology of blindsight , 1991, Trends in Neurosciences.

[37]  G. Elston Comparative studies of pyramidal neurons in visual cortex of monkeys , 2004 .

[38]  Leslie G. Ungerleider,et al.  Visual topography of area TEO in the macaque , 1991, The Journal of comparative neurology.

[39]  V. Mountcastle,et al.  Visual input to the visuomotor mechanisms of the monkey's parietal lobe. , 1977, Science.

[40]  J. Kaas Plasticity of sensory and motor maps in adult mammals. , 1991, Annual review of neuroscience.

[41]  E. G. Jones,et al.  Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

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

[44]  R. Weller Two cortical visual systems in Old World and New World primates. , 1988, Progress in brain research.

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

[46]  M G Rosa,et al.  Cellular heterogeneity in cerebral cortex: A study of the morphology of pyramidal neurones in visual areas of the marmoset monkey , 1999, The Journal of comparative neurology.

[47]  M. Colonnier Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. , 1968, Brain research.

[48]  G. Elston,et al.  PYRAMIDAL NEURONES IN MACAQUE VISUAL CORTEX: INTERAREAL PHENOTYPIC VARIATION OF DENDRITIC BRANCHING PATTERNS , 2001 .

[49]  W. B. Spatz,et al.  Morphology and connections of neurons in area 17 projecting to the extrastriate areas mt and 19DM and to the superior colliculus in the monkey Callithrix jacchus , 1995, The Journal of comparative neurology.

[50]  W. Taylor,et al.  Direction selectivity in the retina , 2002, Current Opinion in Neurobiology.

[51]  M. Colonnier,et al.  A laminar analysis of the number of round‐asymmetrical and flat‐symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat , 1985, The Journal of comparative neurology.

[52]  Jon H. Kaas,et al.  The emergence and evolution of mammalian neocortex , 1995, Trends in Neurosciences.

[53]  A. Peters,et al.  Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. III. Origins and frequency of occurrence of the terminals , 1992, Journal of neurocytology.

[54]  Christof Koch,et al.  Biophysics of Computation: Information Processing in Single Neurons (Computational Neuroscience Series) , 1998 .

[55]  G. Elston Pyramidal Cells of the Frontal Lobe: All the More Spinous to Think With , 2000, The Journal of Neuroscience.

[56]  John H. R. Maunsell,et al.  The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: Asymmetries, areal boundaries, and patchy connections , 1986, The Journal of comparative neurology.

[57]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[58]  Bob Jacobs,et al.  Regional Dendritic Variation in Primate Cortical Pyramidal Cells , 2002 .

[59]  D. B. Bender,et al.  Visual Receptive Fields of Neurons in Inferotemporal Cortex of the Monkey , 1969, Science.

[60]  Bartlett W. Mel NMDA-Based Pattern Discrimination in a Modeled Cortical Neuron , 1992, Neural Computation.

[61]  J. DeFelipe,et al.  The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs , 1992, Progress in Neurobiology.

[62]  W H Calvin,et al.  Fast and slow pyramidal tract neurons: an intracellular analysis of their contrasting repetitive firing properties in the cat. , 1976, Journal of neurophysiology.

[63]  H. Barbas,et al.  The laminar pattern of connections between prefrontal and anterior temporal cortices in the Rhesus monkey is related to cortical structure and function. , 2000, Cerebral cortex.

[64]  A. Larkman,et al.  Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions , 1991, The Journal of comparative neurology.

[65]  B. C. Motter,et al.  Functional properties of parietal visual neurons: mechanisms of directionality along a single axis , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[67]  J. Lund,et al.  Anatomical organization of primate visual cortex area VII , 1981, The Journal of comparative neurology.

[68]  W. R. Taylor,et al.  Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina , 2002, The Journal of Neuroscience.

[69]  J. DeFelipe Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex , 1997, Journal of Chemical Neuroanatomy.

[70]  G. Elston,et al.  Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey , 1999, The Journal of comparative neurology.

[71]  W. Rall Branching dendritic trees and motoneuron membrane resistivity. , 1959, Experimental neurology.

[72]  A. Grinvald,et al.  Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[73]  G. Elston,et al.  Cortical integration in the visual system of the macaque monkey: large-scale morphological differences in the pyramidal neurons in the occipital, parietal and temporal lobes , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[74]  G. Elston,et al.  Interlaminar differences in the pyramidal cell phenotype in cortical areas 7m and STP (the superior temporal polysensory area) of the macaque monkey , 2001, Experimental Brain Research.

[75]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[77]  J. Kaas,et al.  Evidence from V1 connections for both dorsal and ventral subdivisions of V3 in three species of new world monkeys , 2002, The Journal of comparative neurology.

[78]  J. B. Levitt,et al.  Cells and circuits contributing to functional properties in area V1 of macaque monkey cerebral cortex: bases for neuroanatomically realistic models. , 1995, Journal of anatomy.

[79]  J. Kaas The Segregation of Function in the Nervous System , 1995 .

[80]  P. Somogyi,et al.  Salient features of synaptic organisation in the cerebral cortex 1 Published on the World Wide Web on 3 March 1998. 1 , 1998, Brain Research Reviews.

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

[82]  M. Livingstone,et al.  Mechanisms of Direction Selectivity in Macaque V1 , 1998, Neuron.

[83]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[84]  C. Gilbert Adult cortical dynamics. , 1998, Physiological reviews.

[85]  J. B. Levitt,et al.  Anatomical origins of the classical receptive field and modulatory surround field of single neurons in macaque visual cortical area V1. , 2002, Progress in brain research.

[86]  A Grinvald,et al.  Optical imaging reveals the functional architecture of neurons processing shape and motion in owl monkey area MT , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[87]  J. Morrison,et al.  Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis , 1995, The Journal of comparative neurology.

[88]  D. Chklovskii,et al.  Geometry and Structural Plasticity of Synaptic Connectivity , 2002, Neuron.

[89]  T. Wiesel,et al.  Targets of horizontal connections in macaque primary visual cortex , 1991, The Journal of comparative neurology.

[90]  K. Rockland,et al.  Configuration, in serial reconstruction, of individual axons projecting from area V2 to V4 in the macaque monkey. , 1992, Cerebral cortex.

[91]  M. Cynader,et al.  Intrinsic projections within visual cortex: evidence for orientation-specific local connections. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[92]  G. Innocenti General Organization of Callosal Connections in the Cerebral Cortex , 1986 .

[93]  G. Elston,et al.  Dendritic branching patterns of pyramidal cells in the visual cortex of the new world marmoset monkey, with comparative notes on the old world macaque monkey , 2001 .

[94]  Bartlett W. Mel,et al.  Impact of Active Dendrites and Structural Plasticity on the Memory Capacity of Neural Tissue , 2001, Neuron.

[95]  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.

[96]  J. Kaas,et al.  Connectional and Architectonic Evidence for Dorsal and Ventral V3, and Dorsomedial Area in Marmoset Monkeys , 2001, The Journal of Neuroscience.

[97]  P. Hof,et al.  Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns , 1999, Journal of Chemical Neuroanatomy.

[98]  D. Ferster,et al.  Neural mechanisms of orientation selectivity in the visual cortex. , 2000, Annual review of neuroscience.

[99]  Vivien A. Casagrande,et al.  The Afferent, Intrinsic, and Efferent Connections of Primary Visual Cortex in Primates , 1994 .

[100]  P. H. Schiller On the specificity of neurons and visual areas , 1996, Behavioural Brain Research.

[101]  T. Voigt,et al.  Morphology of the cells within the inferior temporal gyrus that project to the prefrontal cortex in the macaque monkey , 1990, The Journal of comparative neurology.

[102]  A. J. Mistlin,et al.  Neurones responsive to faces in the temporal cortex: studies of functional organization, sensitivity to identity and relation to perception. , 1984, Human neurobiology.

[103]  Keiji Tanaka,et al.  Polysensory properties of neurons in the anterior bank of the caudal superior temporal sulcus of the macaque monkey. , 1988, Journal of neurophysiology.

[104]  Kisou Kubota,et al.  Morphological differences between fast and slow pyramidal tract neurons in the monkey motor cortex as revealed by intracellular injection of horseradish peroxidase by pressure , 1981, Neuroscience Letters.

[105]  A. Cowey,et al.  Retrograde transport of gamma-amino[3H]butyric acid reveals specific interlaminar connections in the striate cortex of monkey. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[106]  G. Elston,et al.  The Pyramidal Cell in Cognition: A Comparative Study in Human and Monkey , 2001, The Journal of Neuroscience.

[107]  I. Fujita,et al.  Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex , 2000, Nature Neuroscience.

[108]  David J. Calkins,et al.  Neuronal chemistry and functional organization in the primate visual system , 1998, Trends in Neurosciences.

[109]  G. Elston,et al.  Variation in the spatial relationship between parvalbumin immunoreactive interneurones and pyramidal neurones in rat somatosensory cortex. , 1999, NeuroReport.

[110]  J. Fuster Cortical dynamics of memory. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[111]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[113]  Keiji Tanaka,et al.  Neurochemical gradients along monkey sensory cortical pathways: calbindin‐immunoreactive pyramidal neurons in layers II and III , 1999, The European journal of neuroscience.

[114]  DH Hubel,et al.  Segregation of form, color, and stereopsis in primate area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[115]  R. Malach Cortical columns as devices for maximizing neuronal diversity , 1994, Trends in Neurosciences.

[116]  Kevan A. C. Martin,et al.  A Canonical Microcircuit for Neocortex , 1989, Neural Computation.

[117]  S. Zeki,et al.  The Organization of Connections between Areas V5 and V1 in Macaque Monkey Visual Cortex , 1989, The European journal of neuroscience.

[118]  K. Rockland,et al.  Specific and columnar projection from area TEO to TE in the macaque inferotemporal cortex. , 1993, Cerebral cortex.

[119]  Michael B. Calford,et al.  Dynamic representational plasticity in sensory cortex , 2002, Neuroscience.

[120]  K. Nakamura,et al.  Mnemonic firing of neurons in the monkey temporal pole during a visual recognition memory task. , 1995, Journal of neurophysiology.

[121]  Karl J. Friston Book Review: Brain Function, Nonlinear Coupling, and Neuronal Transients , 2001 .

[122]  M. Cynader,et al.  Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). , 1992, Cerebral cortex.

[123]  J. Kaas Why Does the Brain Have So Many Visual Areas? , 1989, Journal of Cognitive Neuroscience.

[124]  Robert B. Nelson,et al.  Gradients of protein kinase C substrate phosphorylation in primate visual system peak in visual memory storage areas , 1987, Brain Research.

[125]  E. Geijo-Barrientos,et al.  Laminar Localization, Morphology, and Physiological Properties of Pyramidal Neurons that Have the Low-Threshold Calcium Current in the Guinea-Pig Medial Frontal Cortex , 1996, The Journal of Neuroscience.

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

[127]  R. Weinberg,et al.  Glutamate in terminals of thalamocortical fibers in rat somatic sensory cortex , 1993, Neuroscience Letters.

[128]  J. Fuster,et al.  Occipital and inferotemporal responses to visual signals in the monkey , 1985, Experimental Neurology.

[129]  B. Walmsley,et al.  The time course of synaptic potentials evoked in cat spinal motoneurones at identified group Ia synapses. , 1983, The Journal of physiology.

[130]  G. Elston,et al.  The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. , 1997, Cerebral cortex.

[131]  J. Lund,et al.  Intrinsic laminar lattice connections in primate visual cortex , 1983, The Journal of comparative neurology.

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

[133]  Neurons in the temporal cortex changed their preferred direction of motion dependent on shape. , 1999, Neuroreport.

[134]  K. Rockland,et al.  Morphology of individual axons projecting from area V2 to MT in the macaque , 1995, The Journal of comparative neurology.

[135]  G. Elston,et al.  Parvalbumin-, Calbindin-, and Calretinin-Immunoreactive Neurons in the Prefrontal Cortex of the Owl Monkey (Aotus trivirgatus): A Standardized Quantitative Comparison with Sensory and Motor Areas , 2003, Brain, Behavior and Evolution.

[136]  I Fujita,et al.  Intrinsic connections in the macaque inferior temporal cortex , 1996, The Journal of comparative neurology.

[137]  P. Goldman-Rakic,et al.  Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey , 1995, The Journal of comparative neurology.

[138]  C D Gilbert,et al.  Circuitry, architecture, and functional dynamics of visual cortex. , 1993, Cerebral cortex.

[139]  T. Wiesel,et al.  Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex , 1979, Nature.

[140]  Bevil R. Conway,et al.  Color contrast in macaque V1. , 2002, Cerebral cortex.

[141]  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.

[142]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[143]  B. Seltzer,et al.  Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: Evidence for subdivisions of superior temporal polysensory cortex , 1995, The Journal of comparative neurology.

[144]  Andreas Burkhalter,et al.  Microcircuitry of forward and feedback connections within rat visual cortex , 1996, The Journal of comparative neurology.

[145]  G. Elston,et al.  Complex dendritic fields of pyramidal cells in the frontal eye field of the macaque monkey: comparison with parietal areas 7a and LIP , 1998, Neuroreport.

[146]  T. Wiesel,et al.  Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[147]  Otto D. Creutzfeldt,et al.  Generality of the functional structure of the neocortex , 1977, Naturwissenschaften.

[148]  Kenji Kawano,et al.  Global and fine information coded by single neurons in the temporal visual cortex , 1999, Nature.

[149]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[150]  D. Whitteridge,et al.  Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. , 1984, The Journal of physiology.

[151]  Jean Bullier,et al.  The Role of Area 17 in the Transfer of Information to Extrastriate Visual Cortex , 1994 .

[152]  K. Rockland,et al.  Organization of individual cortical axons projecting from area V1 (area 17) to V2 (area 18) in the macaque monkey , 1990, Visual Neuroscience.

[153]  M G Rosa,et al.  Comparison of dendritic fields of layer III pyramidal neurons in striate and extrastriate visual areas of the marmoset: a Lucifer yellow intracellular injection. , 1996, Cerebral cortex.

[154]  K. Rockland,et al.  A reticular pattern of intrinsic connections in primate area V2 (area 18) , 1985, The Journal of comparative neurology.

[155]  J. DeFelipe,et al.  Demonstration of glutamate-positive axon terminals forming asymmetric synapses in cat neocortex , 1988, Brain Research.

[156]  G. Elston,et al.  Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. , 1998, Cerebral cortex.

[157]  T. Poggio,et al.  Retinal ganglion cells: a functional interpretation of dendritic morphology. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[158]  D. Hubel,et al.  Anatomy and physiology of a color system in the primate visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[159]  Alan Peters,et al.  THE SMALL PYRAMIDAL NEURON OF THE RAT CEREBRAL CORTEX , 1968, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

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

[161]  J. Jacobs,et al.  Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. , 2001, Cerebral cortex.

[162]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[163]  E. Callaway,et al.  Convergence of magno- and parvocellular pathways in layer 4B of macaque primary visual cortex , 1996, Nature.

[164]  M. Rosa Visuotopic Organization of Primate Extrastriate Cortex , 1997 .

[165]  E. G. Jones,et al.  Vertical organization of gamma-aminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[166]  M. Descheˆnes,et al.  Morphological characterization of slow and fast pyramidal tract cells in the cat , 1979, Brain Research.

[167]  Idan Segev,et al.  Excitable dendrites and spines: earlier theoretical insights elucidate recent direct observations , 1998, Trends in Neurosciences.

[168]  G. Mitchison,et al.  Long axons within the striate cortex: their distribution, orientation, and patterns of connection. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[169]  J. C. Anderson,et al.  The Connection from Cortical Area V1 to V5: A Light and Electron Microscopic Study , 1998, The Journal of Neuroscience.