Anatomical properties and physiological correlates of the intrinsic connections in cat area 18

After making a map of response properties of neurons in a roughly 3 X 4 mm region of area 18 in the cat, we injected wheat-germ agglutinin horseradish peroxidase (WGA-HRP) and succinylated concanavalin A (Con A) into physiologically identified regions of the map. We observed up to 10 patches of retrogradely labeled cells surrounding each injection site. The majority of the patches occurred within 1.4 mm of the center of the injection site, but rare patches were found as far as 3.4 mm from the injection site. The mean center-to-center spacing of the intrinsic patches was about 1 mm, while the mean distance between the center of the injection site and the nearest patches was less than 1 mm. The labeled cells included both nonpyramidal and pyramidal types and were found in all layers, although they were usually most dense in layers II-IV. Between 2% and 9% of the cells within a cortical column were labeled after a single injection of WGA-HRP or Con A into area 18. Injections of different tracers into 2 neighboring areas resulted in a uniform and less patchy distribution of labeled cells, which suggests that the patches observed after a single injection were only a portion of a continuous horizontal system of interconnections. The patterns and positions of the intrinsic patches were compared to the distribution of the following receptive-field properties: preferred orientation, receptive-field location, and eye preference. The preferred orientations of the recording sites within the injected and labeled areas were different and, most frequently, orthogonal to each other. This is a highly specific projection, since regions with orientation values like those of the injection site were “within range,” yet not labeled. We were unable to detect any relationship between the ocular preferences of the injected and labeled cell regions. Injections into areas predominantly driven by the contralateral eye resulted in labeled regions exhibiting varied eye preference distributions. In some animals they were like the injection site and in others there were equal numbers of contra- and ipsilateral eye-dominated regions. The overall distribution of the patches around the injection site was elongated along the anterior-posterior cortical axis of the brain. The patches extended further in the posterior than the anterior direction. These observations appear to be related to the finding that the cortical magnification factor is greater along the anterior-posterior than the medial-lateral axis of area 18.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  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.

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

[3]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[4]  D. Hubel,et al.  The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain , 1975, The Journal of comparative neurology.

[5]  J. DeFelipe,et al.  A type of basket cell in superficial layers of the cat visual cortex. A Golgi-electron microscope study , 1982, Brain Research.

[6]  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.

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

[8]  M. Colonnier,et al.  An anterograde degeneration study of the tangential spread of axons in cortical areas 17 and 18 of the squirrel monkey (Saimiri Sciureus) , 1978, The Journal of comparative neurology.

[9]  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.

[10]  R. Freeman,et al.  A comparison of inhibition in orientation and spatial frequency selectivity of cat visual cortex , 1986, Nature.

[11]  K. Rockland,et al.  A reticular pattern of intrinsic connections in primate area V2 (area 18) , 1985, The Journal of comparative neurology.

[12]  A. Rosenquist,et al.  Laminar origins of visual corticocortical connections in the cat , 1984, The Journal of comparative neurology.

[13]  A. L. Humphrey,et al.  Termination patterns of individual X‐ and Y‐cell axons in the visual cortex of the cat: Projections to area 18, to the 17/18 border region, and to both areas 17 and 18 , 1985, The Journal of comparative neurology.

[14]  L. Palmer,et al.  Retinotopic organization of areas 18 and 19 in the cat , 1979, The Journal of comparative neurology.

[15]  M. Cynader,et al.  Functional topography in cat area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  W. Nauta,et al.  Columnar distribution of cortico-cortical fibers in the frontal association, limbic, and motor cortex of the developing rhesus monkey , 1977, Brain Research.

[17]  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.

[18]  K. Albus,et al.  Second and third visual areas of the cat: interindividual variability in retinotopic arrangement and cortical location , 1980, The Journal of physiology.

[19]  J. Lund,et al.  Intrinsic laminar lattice connections in primate visual cortex , 1983, The Journal of comparative neurology.

[20]  P. Heggelund,et al.  The depth distribution of optimal stimulus orientations for neurones in cat area 17 , 1977, Experimental Brain Research.

[21]  Laminar distribution of GABA-immunoreactive neurons and processes in area 18 of the cat , 1987, Brain Research Bulletin.

[22]  D. Hubel,et al.  Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. L. Humphrey,et al.  Background and stimulus-induced patterns of high metabolic activity in the visual cortex (area 17) of the squirrel and macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  D J Price,et al.  The postnatal development of clustered intrinsic connections in area 18 of the visual cortex in kittens. , 1986, Brain research.

[25]  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.

[26]  T. Imig,et al.  Sources and terminations of callosal axons related to binaural and frequency maps in primary auditory cortex of the cat , 1978, The Journal of comparative neurology.

[27]  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.

[28]  Alan Peters,et al.  A reassessment of the forms of nonpyramidal neurons in area 17 of cat visual cortex , 1981, The Journal of comparative neurology.

[29]  K. Rockland Anatomical organization of primary visual cortex (area 17) in the ferret , 1985, The Journal of comparative neurology.

[30]  A. Harvey The afferent connexions and laminar distribution of cells in area 18 of the cat. , 1980, The Journal of physiology.

[31]  O. Creutzfeldt,et al.  The distribution of degenerating axons after small lesions in the intact and isolated visual cortex of the cat , 1977, Experimental Brain Research.

[32]  E. G. Jones,et al.  Varieties and distribution of non‐pyramidal cells in the somatic sensory cortex of the squirrel monkey , 1975, The Journal of comparative neurology.

[33]  B. R. Moore,et al.  A modification of the Rayleigh test for vector data , 1980 .

[34]  D. Hubel,et al.  Laminar and columnar distribution of geniculo‐cortical fibers in the macaque monkey , 1972, The Journal of comparative neurology.

[35]  P. Goldman-Rakic,et al.  Interdigitation of contralateral and ipsilateral columnar projections to frontal association cortex in primates. , 1982, Science.

[36]  J. Kaas,et al.  Cortical connections of area 17 in tree shrews , 1984, The Journal of comparative neurology.

[37]  A. L. Humphrey,et al.  Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis) , 1982, The Journal of comparative neurology.

[38]  B. Heller Circular Statistics in Biology, Edward Batschelet. Academic Press, London & New York (1981), 371, Price $69.50 , 1983 .

[39]  M. Colonnier THE TANGENTIAL ORGANIZATION OF THE VISUAL CORTEX. , 1964, Journal of anatomy.

[40]  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.

[41]  D. Hubel,et al.  Orientation columns in macaque monkey visual cortex demonstrated by the 2-deoxyglucose autoradiographic technique , 1977, Nature.

[42]  D. J. Price,et al.  Patterns of cytochrome oxidase activity in areas 17, 18 and 19 of the visual cortex of cats and kittens , 2004, Experimental Brain Research.

[43]  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.

[44]  A L Humphrey,et al.  Topographic organization of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). II. Deoxyglucose mapping , 1980, The Journal of comparative neurology.

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

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

[47]  B. Wainer,et al.  Stabilization of the tetramethylbenzidine (TMB) reaction product: application for retrograde and anterograde tracing, and combination with immunohistochemistry. , 1984, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

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

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

[50]  P. O. Bishop,et al.  Binocular interaction on monocularly discharged lateral geniculate and striate neurons in the cat. , 1981, Journal of neurophysiology.

[51]  D. Hubel,et al.  Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey , 1981, Nature.

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

[53]  J Bullier,et al.  Branching and laminar origin of projections between visual cortical areas in the cat , 1984, The Journal of comparative neurology.

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

[55]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.