Inactivation of the infragranular striate cortex broadens orientation tuning of supragranular visual neurons in the cat

Intracortical inhibition is believed to enhance the orientation tuning of striate cortical neurons, but the origin of this inhibition is unclear. To examine the possible influence of ascending inhibitory projections from the infragranular layers of striate cortex on the orientation selectivity of neurons in the supragranular layers, we measured the spatiotemporal response properties of 32 supragranular neurons in the cat before, during, and after neural activity in the infragranular layers beneath the recorded cells was inactivated by iontophoretic administration of GABA. During GABA iontophoresis, the orientation tuning bandwidth of 15 (46.9%) supragranular neurons broadened as a result of increases in response amplitude to stimuli oriented about ±20° away from the preferred stimulus angle. The mean (±SD) baseline orientation tuning bandwidth (half width at half height) of these neurons was 13.08±2.3°. Their mean tuning bandwidth during inactivation of the infragranular layers increased to 19.59±2.54°, an increase of 49.7%. The mean percentage increase in orientation tuning bandwidth of the individual neurons was 47.4%. Four neurons exhibited symmetrical changes in their orientation tuning functions, while 11 neurons displayed asymmetrical changes. The change in form of the orientation tuning functions appeared to depend on the relative vertical alignment of the recorded neuron and the infragranular region of inactivation. Neurons located in close vertical register with the inactivated infragranular tissue exhibited symmetric changes in their orientation tuning functions. The neurons exhibiting asymmetric changes in their orientation tuning functions were located just outside the vertical register. Eight of these 11 neurons also demonstrated a mean shift of 6.67±5.77° in their preferred stimulus orientation. The magnitude of change in the orientation tuning functions increased as the delivery of GABA was prolonged. Responses returned to normal approximately 30 min after the delivery of GABA was discontinued. We conclude that inhibitory projections from neurons within the infragranular layers of striate cortex in cats can enhance the orientation selectivity of supragranular striate cortical neurons.

[1]  Gerald Westhhmer,et al.  Simultaneous orientation contrast for lines in the human fovea , 1990, Vision Research.

[2]  T. Tsumoto,et al.  Excitatory amino acid transmitters in neuronal circuits of the cat visual cortex. , 1986, Journal of neurophysiology.

[3]  K. Tanaka,et al.  Cross-Correlation Analysis of Interneuronal Connectivity in cat visual cortex. , 1981, Journal of neurophysiology.

[4]  T. Tsumoto,et al.  Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition , 1979, Experimental Brain Research.

[5]  D. Burr,et al.  Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[6]  田中 啓治 Organization of Geniculate Inputs to Visual Cortical Cells in the Cat , 1986 .

[7]  C. Gilbert,et al.  Generation of end-inhibition in the visual cortex via interlaminar connections , 1986, Nature.

[8]  P. Somogyi,et al.  Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat , 1983, Neuroscience.

[9]  A. B. Bonds,et al.  Classifying simple and complex cells on the basis of response modulation , 1991, Vision Research.

[10]  P. O. Bishop,et al.  Orientation specificity of cells in cat striate cortex. , 1974, Journal of neurophysiology.

[11]  B. Payne,et al.  Functional organization of neurons in cat striate cortex: variations in ocular dominance and receptive-field type with cortical laminae and location in visual field. , 1982, Journal of neurophysiology.

[12]  Alan Peters,et al.  Smooth and sparsely‐spined stellate cells in the visual cortex of the rat: A study using a combined golgi‐electron microscope technique , 1978, The Journal of comparative neurology.

[13]  K. Albus,et al.  Phaclofen antagonizes baclofen-induced suppression of visually evoked responses in the cat's striate cortex , 1988, Brain Research.

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

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

[16]  T. Wiesel,et al.  The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat , 1990, Vision Research.

[17]  S. Tieman,et al.  Relay cells, not interneurons, of cat's lateral geniculate nucleus contain N‐acetylaspartylglutamate , 1993, The Journal of comparative neurology.

[18]  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.

[19]  T. Tsumoto,et al.  Actions of excitatory amino acid antagonists on geniculo-cortical transmission in the cat's visual cortex , 2004, Experimental Brain Research.

[20]  O. Creutzfeldt,et al.  Vertical organization in the visual cortex (area 17) in the cat , 2004, Experimental Brain Research.

[21]  C. Blakemore,et al.  Lateral Inhibition between Orientation Detectors in the Human Visual System , 1970, Nature.

[22]  M. Ito,et al.  Functional synaptic organization of primary visual cortex neurones in the cat , 2004, Experimental Brain Research.

[23]  W. R. Levick,et al.  Another tungsten microelectrode , 1972, Medical and biological engineering.

[24]  Z. Kisvárday,et al.  GABAergic networks of basket cells in the visual cortex. , 1992, Progress in brain research.

[25]  S. Levay,et al.  Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi Preparations , 1973, The Journal of comparative neurology.

[26]  P. Somogyi,et al.  Evidence for interlaminar inhibitory circuits in the striate cortex of the cat , 1987, The Journal of comparative neurology.

[27]  P. O. Bishop,et al.  Receptive fields of simple cells in the cat striate cortex , 1973, The Journal of physiology.

[28]  H. Tamura,et al.  Inhibition contributes to orientation selectivity in visual cortex of cat , 1988, Nature.

[29]  O. Creutzfeldt,et al.  An intracellular analysis of visual cortical neurones to moving stimuli: Responses in a co-operative neuronal network , 2004, Experimental Brain Research.

[30]  P. Somogyi,et al.  Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex , 1986, Neuroscience.

[31]  D. Ferster Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  F. Wörgötter,et al.  Topographical Aspects of Intracortical Excitation and Inhibition Contributing to Orientation Specificity in Area 17 of the Cat Visual Cortex , 1991, The European journal of neuroscience.

[33]  P. Heggelund Receptive field organization of complex cells in cat striate cortex , 2004, Experimental Brain Research.

[34]  U. Eysel,et al.  GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex , 2004, Experimental Brain Research.

[35]  B R Payne,et al.  Organization of orientation and direction selectivity in areas 17 and 18 of cat cerebral cortex. , 1987, Journal of neurophysiology.

[36]  Trichur Raman Vidyasagar,et al.  Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18 , 2004, Experimental Brain Research.

[37]  D. Whitteridge,et al.  Physiological and morphological properties of identified basket cells in the cat's visual cortex , 2004, Experimental Brain Research.

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

[39]  A. Sillito,et al.  A re-evaluation of the mechanisms underlying simple cell orientation selectivity , 1980, Brain Research.

[40]  A. Sillito The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

[41]  T. Powell,et al.  An experimental study of the termination of the lateral geniculo–cortical pathway in the cat and monkey , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[42]  Dennis M. Levi,et al.  Spatial scale shifts in peripheral vernier acuity , 1994, Vision Research.

[43]  P. Heggelund,et al.  Receptive field organization of simple cells in cat striate cortex , 1981, Experimental brain research.

[44]  A. Sillito Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex , 1977, The Journal of physiology.

[45]  G Westheimer,et al.  Simultaneous orientation contrast for lines in the human fovea. , 1990, Vision research.

[46]  R. Shapley,et al.  Linear mechanism of orientation tuning in the retina and lateral geniculate nucleus of the cat. , 1987, Journal of neurophysiology.

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

[48]  A. Sillito Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. , 1979, The Journal of physiology.