Foci of orientation plasticity in visual cortex

Cortical areas are generally assumed to be uniform in their capacity for adaptive changes or plasticity. Here we demonstrate, however, that neurons in the cat striate cortex (V1) show pronounced adaptation-induced short-term plasticity of orientation tuning primarily at specific foci. V1 neurons are clustered according to their orientation preference in iso-orientation domains that converge at singularities or pinwheel centres. Although neurons in pinwheel centres have similar orientation tuning and responses to those in iso-orientation domains, we find that they differ markedly in their capacity for adaptive changes. Adaptation with an oriented drifting grating stimulus alters responses of neurons located at and near pinwheel centres to a broad range of orientations, causing repulsive shifts in orientation preference and changes in response magnitude. In contrast, neurons located in iso-orientation domains show minimal changes in their tuning properties after adaptation. The anisotropy of adaptation-induced orientation plasticity is probably mediated by inhomogeneities in local intracortical interactions that are overlaid on the map of orientation preference in V1.

[1]  “Why the Air at the Equator is not Hotter in January than in July”—Freezing of the Neva , 1880, Nature.

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

[3]  D. Hubel,et al.  Sequence regularity and geometry of orientation columns in the monkey striate cortex , 1974, The Journal of comparative neurology.

[4]  A. Saul,et al.  Adaptation in single units in visual cortex: The tuning of aftereffects in the spatial domain , 1989, Visual Neuroscience.

[5]  P. Hammond,et al.  Neural motion after-effects in the cat's striate cortex: Orientation selectivity , 1989, Vision Research.

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

[8]  G. Blasdel,et al.  Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[10]  D. Fitzpatrick,et al.  Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns , 1995, Neuron.

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

[12]  Xiaoqin Wang,et al.  Remodelling of hand representation in adult cortex determined by timing of tactile stimulation , 1995, Nature.

[13]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[15]  T Bonhoeffer,et al.  Orientation selectivity in pinwheel centers in cat striate cortex. , 1997, Science.

[16]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

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

[18]  U. Eysel,et al.  Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat. , 1997, Cerebral cortex.

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

[20]  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.

[21]  C. Gilbert,et al.  Topography of contextual modulations mediated by short-range interactions in primary visual cortex , 1999, Nature.

[22]  U. Eysel,et al.  Increased receptive field size in the surround of chronic lesions in the adult cat visual cortex. , 1999, Cerebral cortex.

[23]  P. Lennie,et al.  Rapid adaptation in visual cortex to the structure of images. , 1999, Science.

[24]  Y. Frégnac,et al.  Activity-dependent regulation of receptive field properties of cat area 17 by supervised Hebbian learning. , 1999, Journal of neurobiology.

[25]  M. Sur,et al.  Adaptation-Induced Plasticity of Orientation Tuning in Adult Visual Cortex , 2000, Neuron.

[26]  Maria V. Sanchez-Vives,et al.  Membrane Mechanisms Underlying Contrast Adaptation in Cat Area 17In Vivo , 2000, The Journal of Neuroscience.

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

[28]  M. Sur,et al.  Dynamic properties of recurrent inhibition in primary visual cortex: contrast and orientation dependence of contextual effects. , 2000, Journal of neurophysiology.