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Spatial and temporal coherence in cortico-cortical connections: A cross-correlation study in areas 17 and 18 in the cat

Published online by Cambridge University Press:  02 June 2009

J. I. Nelson ,
P. A. Salin ,
M. H.-J. Munk ,
M. Arzi  and
J. Bullier
J. I. Nelson
Affiliation:
Working Group in Biophysics, Philipps University, 3550 Marburg, Germany
P. A. Salin
Affiliation:
Vision et Motricité, INSERM Unité 94, 69500 Bron, France
M. H.-J. Munk
Affiliation:
Working Group in Biophysics, Philipps University, 3550 Marburg, Germany
M. Arzi
Affiliation:
Vision et Motricité, INSERM Unité 94, 69500 Bron, France
J. Bullier
Affiliation:
Vision et Motricité, INSERM Unité 94, 69500 Bron, France
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Abstract

Visual cortical areas are richly but selectively connected by “patchy” projections. We characterized these connections physiologically with cross-correlograms (CCHs), calculated for neuron pairs or small groups located one each in visual areas 17 and 18 of the cat. The CCHs were then compared to the visuotopic and orientation match of the neurons' receptive fields (RFs).

For both spontaneous and visually driven activity, most non-flat correlograms were centered; i.e. the most likely temporal relationship between spikes in the two areas is a synchronous one. Although spikes are most likely to occur simultaneously, area 17 spikes may occur before area 18 or vice versa, giving the cross-correlogram peak a finite width (temporal dispersion). Cross-correlograms fell into one of three groups according to their full-width at half peak height: 1–8 ms (modal width, 3 ms), 15–65 ms (modal width 30 ms), or 100–1000 ms (modal width 400 ms). These classificatory groups are nonoverlapping; the three types of coupling appeared singly and in combination.

Neurons whose receptive fields (RFs) are nonoverlapping or cross-oriented may yet be coupled, but the coupling is more likely to be the broadest type of coupling than the medium-dispersed type. The sharpest type of coupling is found exclusively between neurons with at least partially overlapping RFs and mostly between neurons whose stimulus orientation preferences matched to within 22.5 deg. The maximum spatial dispersion observed in the RFs of coupled neurons compares well with the maximum divergence seen anatomically in the A18/A17 projection system.

We suggest three different mechanisms to produce each of the three different degrees of observed spatial and temporal coherence. All mechanisms use common input of cortical origin. For medium and broad coupling, this common input arises from cell assemblies split between both sides of the 17/18 projection system, but acting synchronously. Such distributed common-input cell assemblies are a means of overcoming sparse connectivity and achieving synaptic transmission in the pyramidal network.

Keywords

Cross-correlationExtrinsic projectionsVisual pathwaysTemporal synchronizationVisual cortex
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 1 , July 1992 , pp. 21 - 37
Copyright
Copyright © Cambridge University Press 1992

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References

Allman, J., Miezin, F. & McGuinness, E. (1985). Direction- and velocity-specific responses from beyond the classical receptive field in the middle temporal visual area (MT). Perception 14, 105–126.Google Scholar
Ball, G.J., Gloor, P. & Thompson, C.J. (1977). Computed unit-EEG correlations and laminar profiles of spindle waves in the electroencephalogram of cats. EEG Clinical Neurophysiology 43, 330–345.Google Scholar
Birnbacher, D. & Albus, K. (1987). Divergence of single axons in afferent projections to the cat's visual cortical areas 17, 18, and 19: A parametric study. Journal of Comparative Neurology 261, 543–561.CrossRefGoogle Scholar
Braitenberg, V. & SchÜZ, A. (1989). Cortex: Hohe Ordnung Oder GrÖBtmÖGliches Durcheinander? Spektrum der Wissenschaft May, 74–86.Google Scholar
Bullier, J., Kennedy, H. & Salinger, W. (1984a). Bifurcation of sub-cortical afferents to visual areas 17, 18 and 19 in cat cortex. Journal of Comparative Neurology 228, 309–328.Google Scholar
Bullier, J., Kennedy, H. & Salinger, W. (1984b). Branching and laminar origin of projections between visual cortical areas in the cat. Journal of Comparative Neurology 228, 329–341.Google Scholar
Bullier, J., McCourt, M.E. & Henry, G.H. (1988). Physiological studies on the feedback connection to the striate cortex from cortical areas 18 and 19 of the cat. Experimental Brain Research 70, 90–98.Google Scholar
Cope, T.C., Fetz, E.E. & Matsumura, M. (1987). Cross-correlation assessment of synaptic strength of single la fibre connections with triceps surae motoneurones in cats. Journal of Physiology (London) 390, 161–188.CrossRefGoogle Scholar
Creutzfeldt, O.D., Watanabe, S. & Lux, H.D. (1966). Relations between EEG phenomena and potentials of single cortical cells. II. Spontaneous and convulsoid activity. EEG Clinical Neurophysiology 20, 19–37.CrossRefGoogle ScholarPubMed
Cusick, C.G. & Kaas, J.H. (1986). Interhemispheric connections of cortical sensory and motor representations in primates. In Two Hemispheres—One Brain, Functions of the Corpus Callosum, ed. LeporÉ, F., Ptito, M., Jasper, H.H., pp. 83–102. New York: Alan R. Liss.Google Scholar
De Lima, A.D., Voigt, T. & Morrison, J.H. (1990). Morphology of the cells within the inferior temporal gyrus that project to the prefrontal cortex in the macaque monkey. Journal of Comparative Neurology 296, 159–172.CrossRefGoogle Scholar
Donaldson, I.M.L. & Nash, J.R.G. (1975). The effect of a chronic lesion in cortical area 17 on the visual responses of units in area 18 of the cat. Journal of Physiology (London) 245, 325–332.Google Scholar
Douglas, R.J. & Martin, K.A.C. (1991). Opening the grey box. Trends in Neuroscience 14, 286–293.CrossRefGoogle ScholarPubMed
Dreher, B. & Cottee, L.J. (1975). Visual receptive-field properties of cells in area 18 of cat's cerebral cortex before and after acute lesions in area 17. Journal of Neurophysiology 38, 735–750.Google Scholar
Eckhorn, R., Bauer, R. & Reitboeck, H.J. (1989). Discontinuities in visual cortex and possible functional implications: Relating cortical structure and function with multielectrode/correlation techniques. In Springer Series in Brain Dynamics, vol. 2, ed. Basar, E. & Bullock, T.H., pp. 267–278. Berlin: Springer.Google Scholar
Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M. & Reitboeck, H.J. (1988). Coherent Oscillations: A Mechanism Of Feature Linking In The Visual Cortex? Multiple Electrode And Correlation Analyses In The Cat. Biological Cybernetics 60, 121–130.Google Scholar
Einstein, G. & Fitzpatrick, D. (1991). Distribution and morphology of area 17 neurons that project to the cat's extrastriate cortex. Journal of Comparative Neurology 303, 132–149.Google Scholar
Engel, A.K., König, P., Gray, C.M. & Singer, W. (1990). Stimulus-dependent neuronal oscillations in cat visual cortex: Inter-columnar interaction as determined by cross-correlation analysis. European Journal of Neuroscience 2, 588–606.Google Scholar
Engel, A.K., Kreiter, A.K., König, P. & Singer, W. (1991). Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. Proceedings National Academy of Science of the U.S.A. 88, 6048–6052.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van essen, D.C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1, 1–47.Google Scholar
Fernald, R. & Chase, R. (1971). An improved method for plotting retinal landmarks and focusing the eyes. Vision Research 11, 95–96.Google Scholar
Freeman, R.D. & Ohzawa, I. (1990). On the neurophysiological organization of binocular vision. Vision Research 30, 1661–1676.Google Scholar
Gabbott, P.L.A., Martin, K.A.C. & Whitteridge, D. (1987). Connections between pyramidal neurons in layer 5 of cat visual cortex (area 17). Journal of Comparative Neurology 259, 364–381.Google Scholar
Geisert, E.E. Jr, (1980). Cortical projections of the lateral geniculate nucleus in the cat. Journal of Comparative Neurology 190, 793–812.CrossRefGoogle ScholarPubMed
Gilbert, C.D. & Wiesel, T.N. (1989). Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. Journal of Neuroscience 9, 2432–2442.Google Scholar
Girard, P. & Bullier, J. (1989). Visual activity in area V2 during reversible inactivation of area 17 in the Macaque monkey. Journal of Neurophysiology 62, 1287–1302.Google Scholar
Gochin, P.M., Miller, E.K., Gross, C.G. & Gerstein, G.L. (1991). Functional Interactions Among Neurons In Inferior Temporal Cortex Of The Awake Macaque. Experimental Brain Research 84, 505–516.CrossRefGoogle ScholarPubMed
Gray, C.M., König, P., Engel, A.K. & Singer, W. (1989). Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334–337.CrossRefGoogle ScholarPubMed
Gray, C. & Singer, W. (1987). Stimulus-dependent neuronal oscillations in the cat visual cortex area 17. Neuroscience, an International Journal Under the Editorial Direction oflBRO (Suppl.) 22, S434.Google Scholar
Gulyas, B., Orban, G.A., Duysens, J. & Maes, H. (1987). The suppressive influence of moving textured backgrounds on responses of cat striate neurons to moving bars. Journal of Neurophysiology 57, 1767–1791.CrossRefGoogle ScholarPubMed
Henry, G.H., Salin, P. & Bullier, J. (1991). Projections from area-18 and area-19 to cat striate cortex: Divergence and laminar specificity. European Journal of Neuroscience 3, 186–200.CrossRefGoogle ScholarPubMed
Jones, E.G., Coulter, J.D. & Hendry, S.H.C. (1978). Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. Journal of Comparative Neurology 181, 291–348.Google Scholar
Jones, E.G. & Wise, S.P. (1977). Size, laminar and columnar distribution of efferent cells in the sensory motor cortex of monkeys. Journal of Comparative Neurology 175, 391–438.CrossRefGoogle ScholarPubMed
Kennedy, H., Meissirel, C. & Dehay, C. (1991). Callosal pathways and their compliancy to general rules governing the organization of cortico cortical connectivity. In Neuroanatomy of the Visual Pathways and Their Development, ed. Dreher, B. & Robinson, S.R., pp. 324–359. New York: Macmillan.Google Scholar
Kisvarday, Z.F., Martin, K.A.C., Freund, T.F., Magloczky, Z., Whitteridge, D. & Somogyi, P. (1986). Synaptic targets of HRPfilled layer III pyramidal cells in the cat striate cortex. Experimental Brain Research 64, 541–552.Google Scholar
Krause, F., Eckhorn, R. & Habbel, C. (1984). Two types of direction selective mechanisms in simple units revealed by receptive field cinematograms. Pfluegers Archive—European Journal of Physiology 402, R51.Google Scholar
KrÜGer, J. & Aiple, F. (1988). Multimicroelectrode investigation of monkey striate cortex: Spike train correlations in the infragranular layers. Journal of Neurophysiology 60, 798–828.CrossRefGoogle ScholarPubMed
Levay, S. (1988). The patchy intrinsic projections of visual-cortex. Progress in Brain Research 75, 147–161.Google Scholar
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Llinas, R.R. (1988). The intrinsic electrophysiological properties of mammalian neurons: Insights into central nervous system function. Science 242, 1654–1664.Google Scholar
Maunsell, J.H.R. & Newsome, W.T. (1987). Visual processing in monkey extrastriate cortex. Annual Review of Neuroscience 10, 363–401.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Van Essen, D.C. (1983). The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 2563–2586.Google Scholar
McLean, J. & Palmer, L.A. (1989). Contribution of linear spatiotemporal receptive field structure to velocity selectivity of simple cells in area 17 of cat. Vision Research 29, 675–679.Google Scholar
Melssen, W.J. & Epping, W.J. (1987). Detection and estimation of neural connectivity based on cross-correlation analysis. Biological Cybernetics 57, 403–414.Google Scholar
Merrill, E.G. & Ainsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrodes. Medical and Biological Engineering 10, 662–672.Google Scholar
Mlchalski, A., Gerstein, G.L., Czarkowska, J. & Tarnecki, R. (1983). Interactions between cat striate cortex neurons. Experimental Brain Research 51, 97–107.Google Scholar
Mignard, M. & Malpeli, J.G. (1991). Paths of information flow through visual cortex. Science 251, 1249–1251.Google Scholar
Mitchison, G. & Crick, F. (1982). Long axons within the striate cortex: Their distribution, orientation, and patterns of connection. Proceedings National Academy of Science of the U.S.A. 79, 3661–3665.Google Scholar
Montero, V.M. (1981). Topography of the cortico-cortical connections from the striate cortex in the cat. Brain, Behavior and Evolution 18, 194–218.CrossRefGoogle ScholarPubMed
Nelson, J.I. (1975). Globality and stereoscopic fusion in binocular vision. Journal of Theoretical Biology 49, 1–88.CrossRefGoogle ScholarPubMed
Nelson, J.I. (1985). The cellular basis of perception. In Models of the Visual Cortex, ed. Rose, D. & DOBSON, V., pp. 108–122. New York: Wiley.Google Scholar
Nelson, J.I., Bullier, J., Salin, P.A. & Munk, M.H.-J. (1990). Three kinds of functional coupling between cat areas A17 and A18 revealed by cross-correlation. Society for Neuroscience Abstracts 16(2), 1136.Google Scholar
Nelson, J.I. & Frost, B.J. (1978). Orientation-selective inhibition from beyond the classic visual receptive field. Brain Research 139, 359–365.Google Scholar
Nelson, J.I. & Frost, B.J. (1985). Intracortical facilitation among co-oriented, co-axially aligned simple cells in cat striate cortex. Experimental Brain Research 61, 54–61.Google Scholar
Nelson, J.I., Munk, M.H.-J., Bullier, J. & Eckhorn, R. (1989). Functional connectivity revealed in and outside of receptive field overlap by 3 cross-correlation techniques. Society for Neuroscience Abstracts 15, 1057.Google Scholar
Nikara, T., Bishop, P.O. & Pettigrew, J.D. (1968). Analysis of retinal correspondence by studying receptive fields of binocular single units in cat striate cortex. Experimental Brain Research 6, 353–372.CrossRefGoogle ScholarPubMed
Noda, H. & Adey, W.R. (1970). Firing of neuron pairs in cat association cortex during sleep and wakefulness. Journal of Neurophysiology 33, 672–684.Google Scholar
Patel, I.M. & Chapin, J.K. (1990). Ketamine effects on somatosensory cortical single neurons and on behavior in rats. Anesthesia and Analgesia 70, 635–644.CrossRefGoogle ScholarPubMed
Pettigrew, J.D., Cooper, M.L. & Lasdel, G.G. (1979). Improved use of tapetal reflection for eye-position monitoring. Investigative Ophthalmology and Visual Science 18, 490–495.Google ScholarPubMed
Reitboeck, H.J. & Werner, G. (1983). Multi-electrode recording system for the study of spatio-temporal activity patterns of neurons in the central nervous system. Experientia 39, 339–341.Google Scholar
Rockland, K.S. & Pandya, D.N. (1979). Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Research 179, 3–20.Google Scholar
Rockland, K.S. & Virga, A. (1989). Terminal arbors of individual “feedback” axons projecting from area V2 to V1 in the macaque monkey: A study using immunohistochemistry of anterogradely transported Phaseolus vulgaris-leucoagglutinin. Journal of Comparative Neurology 285, 54–72.CrossRefGoogle ScholarPubMed
Salin, P.A. (1988). Etude de I'organisation topographique des afférents à I'aire striée du chat adulte par une methode de double marquage. Thèse de médecine, Université Claude Bernard, Lyon I.Google Scholar
Salin, P.A. (1991). Organisation géometrique et fonctionelle des connexions entre les aires 17 et 18 du cortex visuel du chat. Thése de doctorat, Université Claude Bernard, Lyon I.Google Scholar
Salin, P.A., Bullier, J. & Kennedy, H. (1989). Convergence and divergence in the afferent projections to cat area 17. Journal of Comparative Neurology 283, 486–512.CrossRefGoogle ScholarPubMed
Salin, P.A., Girard, P., Kennedy, H. & Bullier, J. (1992). The visuotopic organization of cortìcocortical connections in the visual system of the cat. Journal of Comparative Neurology (in press).CrossRefGoogle Scholar
Sandell, J.H. & Schiller, P.H. (1982). Effect of cooling area 18 on striate cortex cells in the squirrel monkey. Journal of Neurophysiology 48, 38–48.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1977). The effect of striate cortex cooling on area 18 cells in the monkey. Brain Research 126, 366–369.CrossRefGoogle ScholarPubMed
SchÜZ, A. & Palm, G. (1989). Density of neurons and synapses in the cerebral cortex of the mouse. Journal of Comparative Neurology 286, 442–455.Google Scholar
Sherk, H. (1978). Area 18 cell responses in cat during reversible inactivation of area 17. Journal of Neurophysiology 41, 204–215.Google Scholar
Sporns, O., Gally, J.A., Reeke, G.N.JR., & Edelman, G.M. (1989). Reentrant signaling among simulated neuronal groups leads to coherency in their oscillatory activity. Proceedings National Academy of Science of the U.S.A. 86, 7265–7269.Google Scholar
Stevens, C.F. (1989). How cortical interconnectedness varies with network size. Neural Computation 1, 473–479.CrossRefGoogle Scholar
Symonds, L.L. & Rosenquist, A.C. (1984). Laminar origins of visual cortico-cortical connections in the cat. Journal of Comparative Neurology 229, 39–47.CrossRefGoogle Scholar
Tigges, J., Tigges, M. & Perachio, A.A. (1977). Complementary laminar terminations of afferents to area 17 originating in area 18 and the lateral geniculate nucleus in squirrel monkey. Journal of Comparative Neurology 176, 87–100.CrossRefGoogle ScholarPubMed
Ts'O, D.Y., Gilbert, C.D. & Wiesel, T.N. (1986). Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. Journal of Neuroscience 6, 1160–1170.CrossRefGoogle ScholarPubMed
Vakkur, G.J., Bishop, P.O. & Kozak, W. (1963). Visual optics in the cat, including posterior nodal distance and retinal landmarks. Vision Research 3, 289–314.CrossRefGoogle Scholar
Van Essen, D.C. (1985). Functional organization of primate visual cortex. In Cerebral Cortex, Vol. 3, ed. Peters, A. & Jones, E.G., pp. 259–329. New York, London: Plenum.Google Scholar
Van Essen, D.C., Newsome, W.T. & Bixby, J.L. (1982). The pattern of interhemispheric connections and its relationship to extrastriate visual areas in the macaque monkey. Journal of Neuroscience 2, 265–283.Google Scholar
Van Hulle, M.M. & Orban, G.A. (1989). Entropy driven artificial neuronal networks and sensorial representation: A proposal. Journal of Parallel and Distributed Computing 6, 264–290.Google Scholar