Horizontal interactions between visual cortical neurones studied by cross‐correlation analysis in the cat.

1. To explore the functional significance of horizontal neural connections in the extent of a ‘hypercolumn’ of the cat visual cortex, we carried out cross‐correlation analysis of spike trains recorded simultaneously from a pair of neurones separated horizontally by less than 1 mm. 2. Significantly correlated firings, which were found in sixty‐eight pairs of cells among 327 pairs analysed, were classified into three types on the basis of their functional implications: (1) excitatory interactions, (2) inhibitory interactions and (3) common inputs to both neurones of a pair from other sources. 3. Of these three types, common inputs were encountered most frequently. Excitatory interactions were always accompanied by common inputs. Inhibitory interactions were observed least frequently. 4. The proportion of cell pairs with correlated firings was high in pairs with a horizontal separation of less than 200 microns and decreased markedly with a horizontal separation of more than 400 microns. 5. Regarding laminar locations of cells, common inputs and excitatory interactions were often observed in layers II + III and V, whereas laminar bias was not seen in inhibitory interactions. 6. With respect to difference in orientation preference between two cells, all the three types of correlations were observed, mostly in cell pairs with a difference of less than 45 deg. In particular, common inputs and excitatory interactions were often seen in cell pairs with matched orientation preferences, but inhibitory interactions were found mostly in those with slightly different orientation preferences. In addition, common inputs and excitatory interactions tended to be found between cells with the same eye preference. 7. These results suggest that horizontal functional interactions exist mainly in a range of up to 400 microns as far as the extent of a hypercolumn of the visual cortex is concerned, and these interactions operate effectively between cortical cells with similar receptive field properties except for inhibitory interactions.

[1]  D. Hubel,et al.  Integrative action in the cat's lateral geniculate body , 1961, The Journal of physiology.

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

[3]  W. Levick,et al.  Maintained activity of lateral geniculate neurones in darkness , 1964, The Journal of physiology.

[4]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[5]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[6]  G. P. Moore,et al.  Statistical signs of synaptic interaction in neurons. , 1970, Biophysical journal.

[7]  W. Levick,et al.  Sustained and transient neurones in the cat's retina and lateral geniculate nucleus , 1971, The Journal of physiology.

[8]  D. D. Michaels Ocular dominance. , 1972, Survey of ophthalmology.

[9]  H. L. Bryant,et al.  Correlations of neuronal spike discharges produced by monosynaptic connections and by common inputs. , 1973, Journal of neurophysiology.

[10]  D H Hubel,et al.  Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport. , 1974, Brain research.

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

[12]  G L Gerstein,et al.  Interactions between neurons in auditory cortex of the cat. , 1974, Journal of neurophysiology.

[13]  T. Powell,et al.  The intrinsic, association and commissural connections of area 17 on the visual cortex. , 1975, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[14]  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.

[15]  G. Gerstein,et al.  Interactions between cat lateral geniculate neurons. , 1976, Journal of neurophysiology.

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

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

[18]  M. Stryker,et al.  Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. , 1978, The Journal of physiology.

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

[20]  G. Henry,et al.  Laminar distribution of first-order neurons and afferent terminals in cat striate cortex. , 1979, Journal of neurophysiology.

[21]  A. L. Humphrey,et al.  Topographic organization of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). I. Microelectrode recording , 1980, The Journal of comparative neurology.

[22]  K. Tanaka,et al.  Organization of cat visual cortex as investigated by cross-correlation technique. , 1981, Journal of neurophysiology.

[23]  M. Stryker,et al.  Physiological evidence that the 2-deoxyglucose method reveals orientation columns in cat visual cortex , 1981, Nature.

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

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

[26]  N. Swindale,et al.  A model for the formation of orientation columns , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[27]  C. Gilbert Microcircuitry of the visual cortex. , 1983, Annual review of neuroscience.

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

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

[30]  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.

[31]  B. Gustafsson,et al.  Influence of stretch‐evoked synaptic potentials on firing probability of cat spinal motoneurones. , 1984, The Journal of physiology.

[32]  A. Aertsen,et al.  Evaluation of neuronal connectivity: Sensitivity of cross-correlation , 1985, Brain Research.

[33]  D. Whitteridge,et al.  Synaptic connections of intracellularly filled clutch cells: A type of small basket cell in the visual cortex of the cat , 1985, The Journal of comparative neurology.

[34]  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.

[35]  A. Shosaku,et al.  Cross-correlation analysis of a recurrent inhibitory circuit in the rat thalamus. , 1986, Journal of neurophysiology.

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

[37]  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.

[38]  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.

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

[40]  M. Cynader,et al.  Anatomical properties and physiological correlates of the intrinsic connections in cat area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  J. Krüger,et al.  Multimicroelectrode investigation of monkey striate cortex: spike train correlations in the infragranular layers. , 1988, Journal of neurophysiology.

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

[43]  Charles D. Gilbert,et al.  The Role of Horizontal Connections in Generating Long Receptive Fields in the Cat Visual Cortex , 1989, The European journal of neuroscience.

[44]  T. Wiesel,et al.  Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Tadaharu Tsumoto,et al.  Excitatory amino acid transmitters and their receptors in neural circuits of the cerebral neocortex , 1990, Neuroscience Research.

[47]  W. Singer,et al.  Horizontal Interactions in Cat Striate Cortex: II. A Current Source‐Density Analysis , 1990, The European journal of neuroscience.