The Role of Horizontal Connections in Generating Long Receptive Fields in the Cat Visual Cortex

The cells in the primary visual cortex possess numerous functional properties that are more complex and varied than those seen in the cortical input. These properties result from the network of intrinsic cortical connections running across the cortical layers and between cortical columns. In the current study we relate the long receptive fields that are characteristic of layer 6 cells to the input that these cells receive from layer 5. The axons of layer 5 pyramidal cells project over long distances within layer 6, enabling layer 6 cells to collect input from regions of cortex representing large parts of the visual field. When layer 5 was locally inactivated by injection of the inhibitory transmitter GABA, layer 6 cells lost sensitivity over the portion of their receptive fields corresponding to the inactivated region of layer 5. This suggests that the extensive convergence in the projection from layer 5 to layer 6 is responsible for generating the long receptive fields characteristic of the layer 6 cells.

[1]  L. Palmer,et al.  Visual receptive fields of single striate corical units projecting to the superior colliculus in the cat. , 1974, Brain research.

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

[3]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

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

[5]  C. Gilbert Laminar differences in receptive field properties of cells in cat primary visual cortex , 1977, The Journal of physiology.

[6]  C. Blakemore,et al.  The neural mechanism of binocular depth discrimination , 1967, The Journal of physiology.

[7]  A. L. Humphrey,et al.  Projection patterns of individual X‐ and Y‐cell axons from the lateral geniculate nucleus to cortical area 17 in the cat , 1985, The Journal of comparative neurology.

[8]  G. Henry,et al.  The afferent connections and laminar distribution of cells in the cat striate cortex , 1979, The Journal of comparative neurology.

[9]  J. O'leary,et al.  Structure of the area striata of the cat , 1941 .

[10]  F. Wörgötter,et al.  Lateral interactions at direction‐selective striate neurones in the cat demonstrated by local cortical inactivation. , 1988, The Journal of physiology.

[11]  C. Gilbert Horizontal integration in the neocortex , 1985, Trends in Neurosciences.

[12]  G. Blasdel,et al.  Voltage-sensitive dyes reveal a modular organization in monkey striate cortex , 1986, Nature.

[13]  D. Whitteridge,et al.  Connections between pyramidal neurons in layer 5 of cat visual cortex (area 17) , 1987, The Journal of comparative neurology.

[14]  T. Wiesel,et al.  The Sharpey-Schafer lecture. Morphological basis of visual cortical function. , 1983, Quarterly journal of experimental physiology.

[15]  M S Loop,et al.  Merging of modalities in the optic tectum: infrared and visual integration in rattlesnakes. , 1978, Science.

[16]  G. Henry,et al.  Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey , 1979, The Journal of comparative neurology.

[17]  T. Wiesel,et al.  Patterns of synaptic input to layer 4 of cat striate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[20]  D. Whitteridge,et al.  Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. , 1984, The Journal of physiology.

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

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

[23]  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.

[24]  D. Ferster,et al.  The axonal arborizations of lateral geniculate neurons in the striate cortex of the cat , 1978, The Journal of comparative neurology.

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

[26]  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.

[27]  B. R. Payne,et al.  Organization of direction preferences in cat visual cortex , 1981, Brain Research.

[28]  J. Lund Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta) , 1973, The Journal of comparative neurology.

[29]  L C Katz,et al.  Local circuitry of identified projection neurons in cat visual cortex brain slices , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  L. Benevento,et al.  Auditory-visual interaction in single cells in the cortex of the superior temporal sulcus and the orbital frontal cortex of the macaque monkey , 1977, Experimental Neurology.