Parallel development of orientation maps and spatial frequency selectivity in cat visual cortex

In an early stage of the postnatal development of cats, orientation maps mature and spatial frequency selectivity is consolidated. To investigate the time course of orientation map maturation associated with the consolidation of spatial frequency selectivity, we performed optical imaging of intrinsic signals in areas 17 and 18 of cats under the stimulation of drifting square‐wave gratings with different orientations and spatial frequencies. First, orientation maps for lower spatial frequencies emerged in the entire part of the lateral gyrus, which includes areas 17 and 18, and then these orientation maps in the posterior part of the lateral gyrus disappeared as orientation maps for higher spatial frequencies matured. Independent of age, an anteroposterior gradient of response strengths from lower to higher spatial frequencies was observed. This indicates that the regional distribution of spatial frequencies is innately determined. The size of iso‐orientation domains tended to decrease as the stimulus spatial frequency increased at every age examined. In contrast, orientation representation bias changed with age. In cats younger than 3 months, the cardinal (vertical and horizontal) orientations were represented predominantly over the oblique orientations. However, in young adult cats from 3 to 9 months old, the representation bias switched to predominantly oblique orientations. These age‐dependent changes in the orientation representation bias imply that orientation maps continue to elaborate within postnatal 1 year with the consolidation of spatial frequency selectivity. We conclude that both intrinsic and mutual factors lead to the development of orientation maps and spatial frequency selectivity.

[1]  D. Tolhurst,et al.  On the variety of spatial frequency selectivities shown by neurons in area 17 of the cat , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  Jérôme Ribot,et al.  Preservation of functional architecture in visual cortex of cats with experimentally induced hydrocephalus , 2006, The European journal of neuroscience.

[3]  M. Sur,et al.  Stability of Cortical Responses and the Statistics of Natural Scenes , 2001, Neuron.

[4]  Xiangmin Xu,et al.  How do functional maps in primary visual cortex vary with eccentricity? , 2007, The Journal of comparative neurology.

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

[6]  M. Stryker,et al.  Quantitative study of cortical orientation selectivity in visually inexperienced kitten. , 1976, Journal of neurophysiology.

[7]  J. Mazziotta,et al.  Brain Mapping: The Methods , 2002 .

[8]  Jeffrey A. Sloan,et al.  Spatial frequency analysis of the visual environment: Anisotropy and the carpentered environment hypothesis , 1978, Vision Research.

[9]  M. Silverman,et al.  Spatial frequency columns in primary visual cortex. , 1981, Science.

[10]  A. Grinvald,et al.  Spatio–temporal frequency domains and their relation to cytochrome oxidase staining in cat visual cortex , 1997, Nature.

[11]  S. Jacobson,et al.  Behavioural studies of spatial vision in cats reared with convergent squint: Is amblyopia due to arrest of development? , 1979, Experimental Brain Research.

[12]  Edward A. Essock,et al.  Oblique stimuli are seen best (not worst!) in naturalistic broad-band stimuli: a horizontal effect , 2003, Vision Research.

[13]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[14]  C. Hung,et al.  Building surfaces from borders in Areas 17 and 18 of the cat , 2001, Vision Research.

[15]  A. L. Humphrey,et al.  Termination patterns of individual X‐ and Y‐cell axons in the visual cortex of the cat: Projections to area 18, to the 17/18 border region, and to both areas 17 and 18 , 1985, The Journal of comparative neurology.

[16]  L. Sirovich,et al.  The organization of orientation and spatial frequency in primary visual cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[17]  A. Fuchs,et al.  The development of spatial‐frequency selectivity in kitten striate cortex. , 1981, The Journal of physiology.

[18]  N. Issa,et al.  The organization of spatial frequency maps measured by cortical flavoprotein autofluorescence , 2008, Vision Research.

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

[20]  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.

[21]  Y Matsuda,et al.  Arrangement of orientation pinwheel centers around area 17/18 transition zone in cat visual cortex. , 2000, Cerebral cortex.

[22]  G. Blasdel,et al.  Orientation selectivity, preference, and continuity in monkey striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  C. Gilbert,et al.  Laminar patterns of geniculocortical projection in the cat , 1976, Brain Research.

[24]  L. Palmer,et al.  Retinotopic organization of areas 18 and 19 in the cat , 1979, The Journal of comparative neurology.

[25]  C. Blakemore,et al.  The organization and post‐natal development of area 18 of the cat's visual cortex. , 1987, The Journal of physiology.

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

[27]  B W Knight,et al.  Representation of spatial frequency and orientation in the visual cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[28]  A. Grinvald,et al.  Spatio–temporal frequency domains and their relation to cytochrome oxidase staining in cat visual cortex , 1997, Nature.

[29]  Leonard E White,et al.  Visual experience promotes the isotropic representation of orientation preference , 2004, Visual Neuroscience.

[30]  L. Sirovich,et al.  An Optimization Approach to Signal Extraction from Noisy Multivariate Data , 2001, NeuroImage.

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

[32]  Shigeru Tanaka,et al.  A Postnatal Critical Period for Orientation Plasticity in the Cat Visual Cortex , 2009, PloS one.

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

[34]  M. Stryker,et al.  Spatial Frequency Maps in Cat Visual Cortex , 2000, The Journal of Neuroscience.

[35]  P. Buisseret,et al.  Comparative development of cell properties in cortical Area 18 of normal and dark-reared kittens , 2004, Experimental Brain Research.

[36]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. , 1978, The Journal of physiology.

[37]  J. Pettigrew,et al.  The effect of visual experience on the development of stimulus specificity by kitten cortical neurones , 1974, The Journal of physiology.

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

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

[40]  Jérôme Ribot,et al.  Anisotropy in the representation of direction preferences in cat area 18 , 2008, The European journal of neuroscience.

[41]  D Purves,et al.  The distribution of oriented contours in the real world. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Fred Wolf,et al.  Interareal coordination of columnar architectures during visual cortical development , 2008, Proceedings of the National Academy of Sciences.

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

[44]  Frances Wilkinson,et al.  Visual resolution in young kittens , 1976, Vision Research.

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

[46]  A. Derrington Development of spatial frequency selectivity in striate cortex of vision-deprived cats , 2004, Experimental Brain Research.

[47]  Siegrid Löwel,et al.  Postnatal growth and column spacing in cat primary visual cortex , 2003, Experimental Brain Research.

[48]  D. Fitzpatrick,et al.  Unequal representation of cardinal and oblique contours in ferret visual cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[49]  A. Grinvald,et al.  Optical Imaging of the Layout of Functional Domains in Area 17 and Across the Area 17/18 Border in Cat Visual Cortex , 1995, The European journal of neuroscience.

[50]  Krishan Rana,et al.  An Optimization Approach , 2004 .

[51]  A. Grinvald,et al.  The layout of iso-orientation domains in area 18 of cat visual cortex: optical imaging reveals a pinwheel-like organization , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  S. Appelle Perception and discrimination as a function of stimulus orientation: the "oblique effect" in man and animals. , 1972, Psychological bulletin.

[53]  M. Friedlander,et al.  Postnatal development of the spatial contrast sensitivity of X- and Y- cells in the kitten retinogeniculate pathway , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  Gang Wang,et al.  Difference in the representation of cardinal and oblique contours in cat visual cortex , 2003, Neuroscience Letters.

[55]  T. Bonhoeffer,et al.  Overrepresentation of horizontal and vertical orientation preferences in developing ferret area 17. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[56]  L. Cohen Changes in neuron structure during action potential propagation and synaptic transmission. , 1973, Physiological reviews.

[57]  Y. Yamane,et al.  Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns , 2001, Nature Neuroscience.