Matching the modules: cortical maps and long-range intrinsic connections in visual cortex during development.

Visual cortical neurons exhibit a high degree of response selectivity and are grouped into small columns according to their response preferences. The columns are located at regularly spaced intervals covering the whole cortical representation of the visual field with a modular system of feature-selective neurons. The selectivity of these cells and their modular arrangement is thought to emerge from interactions in the network of specific intracortical and thalamocortical connections. Understanding the ontogenesis of this complex structure and contributions of intrinsic and extrinsic, experience-dependent mechanisms during cortical development can provide new insights into the way the visual cortex processes information about the environment. Available data about the development of connections and response properties in the visual cortex suggest that maturation proceeds in two distinct steps. In the first phase, mechanisms inherent to the cortex establish a crude framework of interconnected neural modules which exhibit the basic but still immature traits of the adult state. Relevant mechanisms in this phase are assumed to consist of molecular cues and patterns of spontaneous neural activity in cortical and corticothalamic interconnections. In a second phase, the primordial layout becomes refined under the control of visual experience establishing a fine-tuned network of connections and mature response properties.

[1]  M. Imbert,et al.  Visual cortical cells: their developmental properties in normal and dark reared kittens. , 1976, The Journal of physiology.

[2]  C. Blakemore,et al.  Development of orientation columns in cat striate cortex revealed by 2-deoxyglucose autoradiography , 1983, Nature.

[3]  D. Mitchell,et al.  A physiological and behavioural study in cats of the effect of early visual experience with contours of a single orientation. , 1977, The Journal of physiology.

[4]  W. Singer,et al.  Functional Specificity of Long-Range Intrinsic and Interhemispheric Connections in the Visual Cortex of Strabismic Cats , 1997, The Journal of Neuroscience.

[5]  A. Antonini,et al.  Pioneer neurons and target selection in cerebral cortical development. , 1990, Cold Spring Harbor symposia on quantitative biology.

[6]  H. Tamura,et al.  Horizontal interactions between visual cortical neurones studied by cross‐correlation analysis in the cat. , 1991, The Journal of physiology.

[7]  E. Callaway,et al.  Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[8]  W. Singer,et al.  Topographic organization of the orientation column system in large flat‐mounts of the cat visual cortex: A 2‐deoxyglucose study , 1987, The Journal of comparative neurology.

[9]  M P Stryker,et al.  Rapid remodeling of axonal arbors in the visual cortex. , 1993, Science.

[10]  P. Huttenlocher,et al.  Development of cortical neuronal activity in the neonatal cat. , 1967, Experimental neurology.

[11]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[12]  T. Wiesel,et al.  The distribution of afferents representing the right and left eyes in the cat's visual cortex , 1977, Brain Research.

[13]  M. Stryker,et al.  Morphology of Single Geniculocortical Afferents and Functional Recovery of the Visual Cortex after Reverse Monocular Deprivation in the Kitten , 1998, The Journal of Neuroscience.

[14]  W. Singer,et al.  The origin and topography of long-range intrinsic projections in cat visual cortex: a developmental study. , 1996, Cerebral cortex.

[15]  D. Fitzpatrick,et al.  Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex , 1997, The Journal of Neuroscience.

[16]  C. Shatz,et al.  Neurogenesis of the cat's primary visual cortex , 1985, The Journal of comparative neurology.

[17]  A. Grinvald,et al.  Relationships between orientation-preference pinwheels, cytochrome oxidase blobs, and ocular-dominance columns in primate striate cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[18]  D. Ferster,et al.  Orientation selectivity of thalamic input to simple cells of cat visual cortex , 1996, Nature.

[19]  D. Hubel,et al.  The period of susceptibility to the physiological effects of unilateral eye closure in kittens , 1970, The Journal of physiology.

[20]  R. Reid,et al.  Specificity of monosynaptic connections from thalamus to visual cortex , 1995, Nature.

[21]  W Singer,et al.  Monocularly Induced 2‐Deoxyglucose Patterns in the Visual Cortex and Lateral Geniculate Nucleus of the Cat: II. Awake Animals and Strabismic Animals , 1993, The European journal of neuroscience.

[22]  W Singer,et al.  Monocularly Induced 2‐Deoxyglucose Patterns in the Visual Cortex and Lateral Geniculate Nucleus of the Cat: I. Anaesthetized and Paralysed Animals , 1993, The European journal of neuroscience.

[23]  Tobias Bonhoeffer,et al.  Reverse occlusion leads to a precise restoration of orientation preference maps in visual cortex , 1994, Nature.

[24]  M. Stryker,et al.  Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  D. Fitzpatrick The functional organization of local circuits in visual cortex: insights from the study of tree shrew striate cortex. , 1996, Cerebral cortex.

[26]  D. Hubel,et al.  Orientation columns in macaque monkey visual cortex demonstrated by the 2-deoxyglucose autoradiographic technique , 1977, Nature.

[27]  P. Heggelund,et al.  Development of spatial receptive-field organization and orientation selectivity in kitten striate cortex. , 1985, Journal of neurophysiology.

[28]  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.

[29]  C. Blakemore,et al.  Reversal of the physiological effects of monocular deprivation in kittens: further evidence for a sensitive period , 1974, The Journal of physiology.

[30]  D. Mitchell,et al.  Monocular astigmatism effects on kitten visual cortex development , 1977, Nature.

[31]  Fred Wolf,et al.  The layout of orientation and ocular dominance domains in area 17 of strabismic cats , 1998, The European journal of neuroscience.

[32]  David G. Jones,et al.  Analysis of the postnatal growth of visual cortex , 1998, Visual Neuroscience.

[33]  C. Shatz,et al.  Segregation of geniculocortical afferents during the critical period: a role for subplate neurons , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  T. Wiesel,et al.  Functional architecture of cortex revealed by optical imaging of intrinsic signals , 1986, Nature.

[35]  K. Obermayer,et al.  Geometry of orientation and ocular dominance columns in monkey striate cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  W. Singer,et al.  Changes in the circuitry of the kitten visual cortex are gated by postsynaptic activity , 1979, Nature.

[37]  J. Horton Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. , 1997, Survey of ophthalmology.

[38]  W Singer,et al.  The Perceptual Grouping Criterion of Colinearity is Reflected by Anisotropies of Connections in the Primary Visual Cortex , 1997, The European journal of neuroscience.

[39]  H. Hirsch,et al.  Physiological consequences for the cat's visual cortex of effectively restricting early visual experience with oriented contours. , 1978, Journal of neurophysiology.

[40]  W. Singer,et al.  The effects of early visual experience on the cat's visual cortex and their possible explanation by Hebb synapses. , 1981, The Journal of physiology.

[41]  D. Hubel,et al.  Laminar and columnar distribution of geniculo‐cortical fibers in the macaque monkey , 1972, The Journal of comparative neurology.

[42]  W. Singer,et al.  Development of Orientation Preference Maps in Area 18 of Kitten Visual Cortex , 1997, The European journal of neuroscience.

[43]  Y. Frégnac,et al.  Development of neuronal selectivity in primary visual cortex of cat. , 1984, Physiological reviews.

[44]  Y. Frégnac,et al.  Early development of visual cortical cells in normal and dark‐reared kittens: relationship between orientation selectivity and ocular dominance. , 1978, The Journal of physiology.

[45]  R. Malach,et al.  Relationship between orientation domains, cytochrome oxidase stripes, and intrinsic horizontal connections in squirrel monkey area V2. , 1994, Cerebral cortex.

[46]  Amiram Grinvald,et al.  Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns , 1991, Nature.

[47]  D. Hubel,et al.  Anatomical demonstration of orientation columns in macaque monkey , 1978, The Journal of comparative neurology.

[48]  W Singer,et al.  Chronic recordings from single sites of kitten striate cortex during experience-dependent modifications of receptive-field properties. , 1989, Journal of neurophysiology.

[49]  M Imbert,et al.  Plasticity in the kitten's visual cortex: effects of the suppression of visual experience upon the orientational properties of visual cortical cells. , 1982, Brain research.

[50]  M. Reivich,et al.  THE [14C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT 1 , 1977, Journal of neurochemistry.

[51]  M. Stryker,et al.  Development of Orientation Preference Maps in Ferret Primary Visual Cortex , 1996, The Journal of Neuroscience.

[52]  C. Blakemore,et al.  Innate and environmental factors in the development of the kitten's visual cortex. , 1975, The Journal of physiology.

[53]  D. Hubel,et al.  RECEPTIVE FIELDS OF CELLS IN STRIATE CORTEX OF VERY YOUNG, VISUALLY INEXPERIENCED KITTENS. , 1963, Journal of neurophysiology.

[54]  G. Henry,et al.  The nature and origin of orientation specificity in neurons of the visual pathways , 1994, Progress in Neurobiology.

[55]  H. Hirsch,et al.  Receptive-field properties of different classes of neurons in visual cortex of normal and dark-reared cats. , 1980, Journal of neurophysiology.

[56]  D. Hubel,et al.  Binocular interaction in striate cortex of kittens reared with artificial squint. , 1965, Journal of neurophysiology.

[57]  M. Stryker,et al.  The role of visual experience in the development of columns in cat visual cortex. , 1998, Science.

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

[59]  A L Humphrey,et al.  Topographic organization of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). II. Deoxyglucose mapping , 1980, The Journal of comparative neurology.

[60]  D. Baylor,et al.  Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. , 1991, Science.

[61]  W. Singer,et al.  Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. , 1992, Science.

[62]  K. Albus,et al.  Early post‐natal development of neuronal function in the kitten's visual cortex: a laminar analysis. , 1984, The Journal of physiology.

[63]  L C Katz,et al.  Development of horizontal projections in layer 2/3 of ferret visual cortex. , 1996, Cerebral cortex.

[64]  William Prinzmetal,et al.  Visual Feature Integration in a World of Objects , 1995 .

[65]  Frank H. Duffy,et al.  Comparison of the effects of dark rearing and binocular suture on development and plasticity of cat visual cortex , 1981, Brain Research.

[66]  H. Hirsch,et al.  Cortical effect of early selective exposure to diagonal lines , 1975, Science.

[67]  F. Sengpiel,et al.  Intrinsic and environmental factors in the development of functional maps in cat visual cortex , 1998, Neuropharmacology.

[68]  Tobias Bonhoeffer,et al.  Development of identical orientation maps for two eyes without common visual experience , 1996, Nature.

[69]  M. Stryker,et al.  The Role of Activity in the Development of Long-Range Horizontal Connections in Area 17 of the Ferret , 1996, The Journal of Neuroscience.

[70]  H. J. Luhmann,et al.  Horizontal Interactions in Cat Striate Cortex: I. Anatomical Substrate and Postnatal Development , 1990, The European journal of neuroscience.

[71]  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.

[72]  C. Shatz,et al.  The relationship between the geniculocortical afferents and their cortical target cells during development of the cat's primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  A. Grinvald,et al.  Spatial Relationships among Three Columnar Systems in Cat Area 17 , 1997, The Journal of Neuroscience.

[74]  M. Stryker,et al.  Development of orientation selectivity in ferret visual cortex and effects of deprivation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[75]  E. Callaway,et al.  Emergence and refinement of clustered horizontal connections in cat striate cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[76]  P. Coleman,et al.  Demonstration of orientation columns with [14C]2-deoxyglucose in a cat reared in a striped environment , 1979, Brain Research.

[77]  M. Stryker,et al.  Ocular dominance peaks at pinwheel center singularities of the orientation map in cat visual cortex. , 1997, Journal of neurophysiology.

[78]  K Albus,et al.  Rapid rearrangement of intrinsic tangential connections in the striate cortex of normal and dark‐reared kittens: Lack of exuberance beyond the second postnatal week , 1992, The Journal of comparative neurology.

[79]  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.

[80]  J. Bolz,et al.  Functional specificity of a long-range horizontal connection in cat visual cortex: a cross-correlation study , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[81]  M. Weliky,et al.  Disruption of orientation tuning visual cortex by artificially correlated neuronal activity , 1997, Nature.

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