Orientation specificity of contrast adaptation in visual cortical pinwheel centres and iso‐orientation domains

Exposure to a high‐contrast visual stimulus causes adaptation, a psychophysical phenomenon that is quite selective for stimulus orientation. Its mechanism is largely cortical but the underlying circuitry is still not unambiguously resolved. It has been suggested that adaptation could be the result of integration of inputs from cells within a large local pool, effectively scaling their outputs with respect to local contrast. In this case, orientation selectivity of neuronal adaptation should depend on the location of neurons within the cortical map of orientation preference. We tested this hypothesis by quantifying adaptation to optimally oriented and to orthogonal‐to‐optimum gratings among neurons recorded either from iso‐orientation domains or orientation pinwheel centres, as identified by optical imaging of cat visual cortex. We did not find a significant difference in adaptation characteristics for these two populations of cells, implying that these characteristics do not depend on the local functional architecture. Surprisingly, however, we additionally observed that under isoflurane (but not halothane) anaesthesia, most neurons exhibited adaptation by cross‐oriented gratings, regardless of their location within the orientation map. It seems likely that, under isoflurane, inputs became visible that were masked by the commonly used, deeper halothane anaesthesia. For individual cells, the presence of these inputs was independent of their location within the cortical orientation map.

[1]  C. R. Ball Estimation and identification of thiols in rat spleen after cysteine or glutathione treatment: relevance to protection against nitrogen mustards. , 1966, Biochemical pharmacology.

[2]  A Pantle,et al.  A model for after-effects of seen movement. , 1967, Vision research.

[3]  C Blakemore,et al.  On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images , 1969, The Journal of physiology.

[4]  C. Blakemore,et al.  The orientation specificity of two visual after‐effects , 1971, The Journal of physiology.

[5]  L. Maffei,et al.  Neural Correlate of Perceptual Adaptation to Gratings , 1973, Science.

[6]  C. Blakemore,et al.  Stimulus specificity in the human visual system. , 1973, Vision research.

[7]  D. Tolhurst,et al.  Is spatial adaptation an after‐effect of prolonged inhibition? , 1974, The Journal of physiology.

[8]  Andrew E. Kertesz,et al.  The role of positional and orientational disparity cues in human fusional response , 1975, Vision Research.

[9]  R. Vautin,et al.  Responses of single cells in cat visual cortex to prolonged stimulus movement: neural correlates of visual aftereffects. , 1977, Journal of neurophysiology.

[10]  P. Lennie,et al.  Pattern-selective adaptation in visual cortical neurones , 1979, Nature.

[11]  I. Ohzawa,et al.  Contrast gain control in the cat visual cortex , 1982, Nature.

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

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

[14]  D. G. Albrecht,et al.  Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. , 1984, The Journal of physiology.

[15]  M A Georgeson,et al.  The effect of spatial adaptation on perceived contrast. , 1985, Spatial vision.

[16]  I. Ohzawa,et al.  Contrast gain control in the cat's visual system. , 1985, Journal of neurophysiology.

[17]  A. B. Bonds,et al.  Contrast adaptation in cat visual cortex is not mediated by GABA , 1986, Brain Research.

[18]  A. B. Bonds Role of Inhibition in the Specification of Orientation Selectivity of Cells in the Cat Striate Cortex , 1989, Visual Neuroscience.

[19]  Trichur Raman Vidyasagar Pattern adaptation in cat visual cortex is a co-operative phenomenon , 1990, Neuroscience.

[20]  M. Berkley Behavioral determination of the spatial selectivity of contrast adaptation in cats: Some evidence for a common plan in the mammmlian visual system , 1990, Visual Neuroscience.

[21]  F. Moroni,et al.  General anaesthetics inhibit the responses induced by glutamate receptor agonists in the mouse cortex , 1992, Neuroscience Letters.

[22]  U. Eysel,et al.  GABA-induced inactivation of functionally characterized sites in cat visual cortex (area 18): effects on orientation tuning , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  I. Ohzawa,et al.  Organization of suppression in receptive fields of neurons in cat visual cortex. , 1992, Journal of neurophysiology.

[24]  D. Heeger Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

[25]  Robert J. Snowden,et al.  Perceived contrast as a function of adaptation duration , 1994, Vision Research.

[26]  R S Aronstam,et al.  Volatile anesthetics and glutamate activation of N-methyl-D-aspartate receptors. , 1995, Biochemical pharmacology.

[27]  U. Eysel,et al.  GABA-induced inactivation of functionally characterized sites in cat visual cortex (area 18): effects on direction selectivity. , 1996, Journal of neurophysiology.

[28]  L. Palmer,et al.  Contrast adaptation and excitatory amino acid receptors in cat striate cortex , 1996, Visual Neuroscience.

[29]  J. Ross,et al.  Perceived contrast following adaptation to gratings of different orientations , 1996, Vision Research.

[30]  R. Snowden,et al.  Spatial frequency adaptation: Threshold elevation and perceived contrast , 1996, Vision Research.

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

[32]  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.

[33]  M. Carandini,et al.  A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. , 1997, Science.

[34]  C. Blakemore,et al.  Different mechanisms underlie three inhibitory phenomena in cat area 17 , 1998, Vision Research.

[35]  U. Eysel,et al.  Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques , 1998, The European journal of neuroscience.

[36]  Tobias Bonhoeffer,et al.  Orientation topography of layer 4 lateral networks revealed by optical imaging in cat visual cortex (area 18) , 1999, The European journal of neuroscience.

[37]  E. Puil,et al.  Mechanism of anesthesia revealed by shunting actions of isoflurane on thalamocortical neurons. , 1999, Journal of neurophysiology.

[38]  E. Puil,et al.  Ionic mechanism of isoflurane's actions on thalamocortical neurons. , 1999, Journal of Neurophysiology.

[39]  Maria V. Sanchez-Vives,et al.  Cellular Mechanisms of Long-Lasting Adaptation in Visual Cortical Neurons In Vitro , 2000, The Journal of Neuroscience.

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

[41]  U. Eysel,et al.  Topography of orientation centre connections in the primary visual cortex of the cat , 2001, Neuroreport.

[42]  M. Sur,et al.  Foci of orientation plasticity in visual cortex , 2001, Nature.

[43]  F. Wörgötter,et al.  Quantitative determination of orientational and directional components in the response of visual cortical cells to moving stimuli , 1987, Biological Cybernetics.