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The influence of input from the lower cortical layers on the orientation tuning of upper layer V1 cells in a primate

Published online by Cambridge University Press:  02 June 2009

John D. Allison ,
Vivien A. Casagrande  and
A.B. Bonds
John D. Allison
Affiliation:
Department of Cell Biology, Vanderbilt University, Nashville
Vivien A. Casagrande
Affiliation:
Department of Cell Biology, Vanderbilt University, Nashville Department of Psychology, Vanderbilt University, Nashville
A.B. Bonds
Affiliation:
Department of Electrical and Biomedical Engineering, Vanderbilt University, Nashville
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Abstract

The receptive fields of cells in the primary visual cortex (area 17 or V1) show clear orientation selectivity, unlike those of the lateral geniculate nucleus (LGN) cells which provide their visual input. The intrinsic circuitry of V1 cells is believed to be partly responsible for this selectivity. We investigated the influence of ascending projections from neurons in the lower layers (5 and 6) of V1 on the orientation selectivity of single neurons in the upper layers (2, 3, and 4) by reversibly inactivating (“blocking”) lower layer neural activity with iontophoretic application of γ-aminobutyric acid (GABA) while recording from upper layer cells in the prosimian primate, Galago crassicaudatus. During lower layer blocking, the majority (20/28 = 71.4%) of upper layer neurons exhibited a change in the orientation of their preferred stimulus, a reduction in their orientation tuning, and/or an increase in their response amplitude. Twelve (42.9%) neurons exhibited shifts in their preferred orientation averaging 11 (±4) deg. These neurons were located, on average, 272 (±120) μm tangential from the vertical axis of the pipette center. Eleven neurons (39.2%) exhibited an average reduced orientation tuning of 52.5%. Their average location was 230 ± (115) ftm away from the vertical axis of the pipette. Five (17.9%) neurons with average location 145 (±75) firn from the vertical axis exhibited both effects. Two (7.1%) neurons that exhibited significant increases in response amplitude to stimulus angles within 10 deg of the peak excitatory stimulus without changes in orientation selectivity or tuning were located less than 100 μm from the vertical axis. The effects on the orientation tuning of cells were restricted in all cases to within ±30 deg of the preferred stimulus orientation. This suggests that layer blocking affects cells with preferred stimulus orientations similar to those of the recorded neurons. Only cells located within 500 μm tangential to the vertical axis of the injection site exhibited these effects. These results suggest that cells within layers 5 and 6 provide organized, orientation-tuned inhibition that sharpens the orientation tuning of cells in the upper cortical layers within the same, or closely neighboring, cell columns.

Keywords

Visual cortexOrientation tuningLayer blockingIntracortical inhibitionGABA
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 2 , March 1995 , pp. 309 - 320
Copyright
Copyright © Cambridge University Press 1995

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References

Albrecht, D.G. & Geisler, W.S. (1991). Motion sensitivity and the contrast-response function of simple cells in the visual cortex. Visual Neuroscience 7, 531–546.CrossRefGoogle ScholarPubMed
Allison, J.D. & Bonds, A.B. (1994). Inactivation of the infragranular striate cortex broadens orientation tuning of supragranular visual neurons in the cat. Experimental Brain Research 101, 415–426.CrossRefGoogle ScholarPubMed
Berman, N.E.J., Payne, B.R., Labar, D.R. & Murphy, E.H. (1982). Functional organization of neurons in cat striate cortex: Variations in ocular dominance and receptive field type with cortical laminae and location in visual field. Journal of Neurophysiology 48, 162–177.CrossRefGoogle ScholarPubMed
Berman, N.E.J., Wilkes, M.E. & Payne, B.R. (1987). Organization of orientation and direction selectivity in area 17 and 18 of cat cerebral cortex. Journal of Neurophysiology 58, 676–699.CrossRefGoogle ScholarPubMed
Blasdel, G.G., Lund, J.S. & Fitzpatrick, D. (1985). Intrinsic connections of macaque striate cortex: Axonal projections of cells outside lamina 4C. Journal of Neuroscience 5, 3350–3369.CrossRefGoogle ScholarPubMed
Bolz, J. & Gilbert, C.D. (1986). Generation of end-inhibition in the visual cortex via interlaminar connections. Nature 320, 362–365.CrossRefGoogle ScholarPubMed
Bonds, A.B. & DeBruyn, E.J. (1985). Inhibition and spatial selectivity in the visual cortex: The cooperative neuronal network revisited. In Models of the Visual Cortex, ed. Rose, D. & Dobson, G., pp. 292–300, New York: John Wiley & Sons.Google Scholar
Brodmann, K. (1909). Vergleichende lokalisationlehre der grosshirn-rinde in ihren Prinzipien dargestellt aufgrunddes zellenbaues, pp. 324. Leipzig, Germany: J.A. Barth.Google Scholar
Casagrande, V.A. & Kaas, J.H. (1994). The afferent, intrinsic, and efferent connections of primary visual cortex in primates. In Cerebral Cortex, Vol. 10, ed. Peters, A. & Rockland, K.S., pp. 201–259, New York: Plenum Press.Google Scholar
Creutzfeldt, O.D., Innocenti, G.M. & Brooks, D. (1974 a). Vertical organization in the visual cortex (area 17). Experimental Brain Research 21, 315–336.CrossRefGoogle ScholarPubMed
Creutzfeldt, O.D., Kuhnt, U. & Benevento, L.A. (1974 b). An intracellular analysis of visual cortical neurons to moving stimuli: Responses in a cooperative neuronal network. Experimental Brain Research 21, 251–274.CrossRefGoogle Scholar
DeBruyn, E.J. & Bonds, A.B. (1986). Contrast adaptation in cat visual cortex is not mediated by GABA. Brain Research 383, 339–342.CrossRefGoogle Scholar
DeBruyn, E.J., Casagrande, V.A., Peck, P.D. & Bonds, A.B. (1993). Visual resolution and sensitivity of single cells in the primary visual cortex (VI) of a nocturnal primate (Bush Baby): Correlation with cortical layers and cytochrome-oxidase patterns. Journal of Neurophysiology 69, 3–18.CrossRefGoogle ScholarPubMed
Eysel, U.T. (1992). Lateral inhibitory interactions in area 17 and 18 of the cat visual cortex. Progress in Brain Research 90, 407–423.CrossRefGoogle Scholar
Ferster, D. (1986). Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. Journal of Neuroscience 6, 1284–1301.CrossRefGoogle ScholarPubMed
Ferster, D. (1987). Origin of orientation-selective EPSPs in simple cells of cat visual cortex. Journal of Neuroscience 7, 1780–1791.CrossRefGoogle ScholarPubMed
Ferster, D. (1988). Spatially opponent excitation and inhibition in simple cells of the cat visual cortex. Journal of Neuroscience 8, 1172–1180.CrossRefGoogle ScholarPubMed
Ferster, D. & Koch, C. (1987). Neuronal connections underlying orientation selectivity in cat visual cortex. Trends in Neuroscience 10, 487–492.CrossRefGoogle Scholar
Ferster, D. & Lindström, S. (1983). An intracellular analysis of geniculocortical connectivity in area 17 of the cat. Journal of Physiology (London) 342, 181–215.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Lund, J.S. & Blasdel, G.G. (1985). Intrinsic connections of macaque striate cortex: Afferent and efferent connections of lamina 4C. Journal of Neuroscience 5, 3329–3349.CrossRefGoogle ScholarPubMed
Gilbert, C.D. & Wiesel, T.N. (1990). The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat. Vision Research 30, 1689–1701.CrossRefGoogle ScholarPubMed
Hässler, R. (1967). Comparative anatomy of central visual systems in day-and night-active primates. In Evolution of the Forebrain, ed. Hässler, R. and Stephan, H., pp. 419–434. New York: Plenum Press.Google Scholar
Heeger, D. J. (1992). Normalization of cell responses in cat striate cortex. Visual Neuroscience 9, 181–197.CrossRefGoogle ScholarPubMed
Henry, G.H., Dreher, B. & Bishop, P.O. (1973). Orientation specificity of cells in cat striate cortex. Journal of Neurophysiology 37, 1394–1409.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106–154.CrossRefGoogle ScholarPubMed
Jones, J.P. & Palmer, L.A. (1987). An evaluation of the two-dimensional gabor filter model of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1233–1258.CrossRefGoogle ScholarPubMed
Kabara, J.F., Snider, R.K., Allison, J.D. & Bonds, A.B. (1994). Compound stimuli modify receptive field spatial tuning in cat cortical cells. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1469.Google Scholar
Lachica, H.A., Beck, P.D. & Casagrande, V.A. (1992). Parallel pathways in macaque monkey striate cortex: Anatomically defined columns in layer III. Proceeding of the National Academy of Sciences of the U.S.A. 89, 3566–3570.CrossRefGoogle ScholarPubMed
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1993). Intrinsic connections of layer III of striate cortex in squirrel monkey and bush baby: Correlations with patterns of cytochrome oxidase. Journal of Comparative Neurology 329, 163–187.CrossRefGoogle ScholarPubMed
Levick, W.R. (1972). Another tungsten microelectrode. Medical and Biological Engineering 10, 510–515.CrossRefGoogle ScholarPubMed
Lund, J.S. (1988). Anatomical organization of macaque monkey striate visual cortex. Annual Review of Neuroscience 11, 253–288.CrossRefGoogle ScholarPubMed
Sillito, A.M. (1975). The contribution of inhibitory mechanisms to the receptive-field properties of neurones in the striate cortex of the cat. Journal of Physiology 250, 305–329.CrossRefGoogle Scholar
Skottun, B., DeValois, R.L., Grosof, D.H., Movshon, J.A., Albrecht, D.O. & Bonds, A.B. (1991). Classifying simple and complex cells on the basis of response modulation. Vision Research 31, 1079–1086.CrossRefGoogle ScholarPubMed
Volgushev, M., Pei, X., Vidyasagar, T.R. & Creutzfeldt, O.D. (1993). Excitation and inhibition in orientation selectivity of cat visual cortex neurons revealed by whole-cell recordings in vivo. Visual Neu-roscience 10, 1151–1155.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome-oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Wörgötter, F. & Koch, C. (1991). A detailed model of the primary visual pathway in the cat: Comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity. Journal of Neuroscience 11, 1959–1979.CrossRefGoogle ScholarPubMed