Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat.

The topography of lateral excitatory and lateral inhibitory connections was studied in relation to orientation maps obtained in areas 17 and 18. Small iontophoretic injections of biocytin were delivered to the superficial layers in regions where orientation selectivity had been mapped using electrode recordings of single- and multi-unit activity from various cortical depths. Biocytin revealed extensive patchy axonal projections of up to 3.5 mm in both areas while labelled somata occurred chiefly at the injection site, indicating that the labelling was primarily anterograde. Two types of boutons could be clearly distinguished: (i) putative excitatory boutons either en passant or having a short stalk and (ii) inhibitory boutons which were invariably of the basket-type. Three-dimensional reconstructions of all labelled boutons showed that the excitatory and the inhibitory networks had a distinctively different relationship to orientation maps. The overall distribution of connections showed that 53-59% of excitatory and 46-48% of inhibitory connections were at iso-orientation, +/-30 degrees; oblique-orientation, +/-(30-60) degrees, was shown by 30% of excitatory and 28-39% of inhibitory connections; cross-orientation was shown by 11-17% of excitatory and 15-24% of inhibitory connections. Although excitatory patches occupied mainly iso-orientation locations, interpatch regions representing chiefly non-iso-orientations (oblique + cross orientation) were also innervated. There was considerable overlap between the excitatory and inhibitory network. Nonetheless, inhibitory connections were more common than excitatory connections with non-iso-orientation locations. There was no significant difference between the orientation topography of area 17 and area 18 projections. The results suggest that in general the lateral connectivity system is not orientation specific, but shows a moderate iso-orientation preference for excitation and an even weaker iso-orientation preference for inhibition. The broad orientation spectrum of lateral connections could provide the basis for mechanisms that requiring different orientations, as for example in detecting orientation discontinuities.

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

[2]  D. Hubel,et al.  Shape and arrangement of columns in cat's striate cortex , 1963, The Journal of physiology.

[3]  G. Mitchison,et al.  Long axons within the striate cortex: their distribution, orientation, and patterns of connection. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[6]  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.

[7]  D. Hubel,et al.  Specificity of intrinsic connections in primate primary visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  M. Cynader,et al.  Intrinsic projections within visual cortex: evidence for orientation-specific local connections. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[9]  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.

[10]  M. Cynader,et al.  Surface organization of orientation and direction selectivity in cat area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[12]  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.

[13]  S. Levay,et al.  Patchy intrinsic projections in visual cortex, area 18, of the cat: Morphological and immunocytochemical evidence for an excitatory function , 1988, The Journal of comparative neurology.

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

[15]  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.

[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]  H. Tamura,et al.  Horizontal interactions between visual cortical neurones studied by cross‐correlation analysis in the cat. , 1991, The Journal of physiology.

[18]  C. Koch,et al.  Isotropic connections generate functional asymmetrical behavior in visual cortical cells. , 1991, Journal of neurophysiology.

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

[20]  T. Sejnowski,et al.  Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. , 1991, Journal of neurophysiology.

[21]  J. Boyd,et al.  Intrinsic connections in cat visual cortex: a combined anterograde and retrograde tracing study , 1991, Brain Research.

[22]  U. Eysel,et al.  Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17) , 1992, Neuroscience.

[23]  J. Boyd,et al.  Presence of GABA-immunoreactive neurons within intracortical patches in area 18 of the cat , 1992, Brain Research.

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

[25]  Klaus Albus,et al.  Lack of Exuberance in Clustered Intrinsic Connections in the Striate Cortex of One‐month‐old Kitten , 1992, The European journal of neuroscience.

[26]  A. Cowey,et al.  Patterns of inter- and intralaminar GABAergic connections distinguish striate (V1) and extrastriate (V2, V4) visual cortices and their functionally specialized subdivisions in the rhesus monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[28]  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.

[29]  U. Eysel,et al.  Network of GABAergic large basket cells in cat visual cortex (area 18): Implication for lateral disinhibition , 1993, The Journal of comparative neurology.

[30]  A. Grinvald,et al.  The layout of iso-orientation domains in area 18 of cat visual cortex: optical imaging reveals a pinwheel-like organization , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  A. Grinvald,et al.  Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[32]  U. Eysel,et al.  Functional and Structural Topography of Horizontal Inhibitory Connections in Cat Visual Cortex , 1993, The European journal of neuroscience.

[33]  A. Burkhalter,et al.  Organization of long-range inhibitory connections with rat visual cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  R. Frostig,et al.  Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  N. A. Lazareva,et al.  Double orientation tuning in the cat visual cortex units , 1994, Neuroscience.

[36]  R. Malach,et al.  Relationship between orientation domains, cytochrome oxidase stripes, and intrinsic horizontal connections in squirrel monkey area V2. , 1994, Cerebral cortex.

[37]  T. Bonhoeffer,et al.  Relationship Between Lateral Inhibitory Connections and the Topography of the Orientation Map in Cat Visual Cortex , 1994, The European journal of neuroscience.

[38]  K. Albus,et al.  The Topography of Tangential Inhibitory Connections in the Postnatally Developing and Mature Striate Cortex of the Cat , 1994, The European journal of neuroscience.

[39]  J. B. Levitt,et al.  Intrinsic cortical connections in macaque visual area V2: Evidence for interaction between different functional streams , 1994, The Journal of comparative neurology.

[40]  U. Eysel,et al.  Time‐slice analysis of inhibition in cat striate cortical neurones , 1994, Neuroreport.

[41]  H. Jones,et al.  Visual cortical mechanisms detecting focal orientation discontinuities , 1995, Nature.

[42]  R. V. Novikova,et al.  Sensitivity to cross-like figures in the cat striate neurons , 1995, Neuroscience.

[43]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[44]  P A Salin,et al.  Corticocortical connections in the visual system: structure and function. , 1995, Physiological reviews.

[45]  C. Gilbert,et al.  Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex , 1995, Nature.

[46]  R. Traub,et al.  A mechanism for generation of long-range synchronous fast oscillations in the cortex , 1996, Nature.

[47]  J. B. Levitt,et al.  Relation between patterns of intrinsic lateral connectivity, ocular dominance, and cytochrome oxidase-reactive regions in macaque monkey striate cortex. , 1996, Cerebral cortex.

[48]  U. Eysel,et al.  GABA-induced inactivation of functionally characterized sites in cat striate cortex: Effects on orientation tuning and direction selectivity , 1997, Visual Neuroscience.

[49]  K. Albus.  A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat , 1975, Experimental Brain Research.