Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-17T19:59:51.314Z Has data issue: false hasContentIssue false
  • English
  • Français

Heterogeneity in local distributions of orientation-selective neurons in the cat primary visual cortex

Published online by Cambridge University Press:  02 June 2009

Pedro E. Maldonado  and
Charles M. Gray
Pedro E. Maldonado
Affiliation:
Center For Neuroscience, University of California, Davis
Charles M. Gray
Affiliation:
Center For Neuroscience, University of California, Davis Seclion of Neurobiology, Physiology, and Behavior, University of California, Davis
Get access Rights & Permissions [Opens in a new window]

Abstract

We have employed the tetrode technique, which allows accurate discrimination of individual neuronal spike trains from multiunit recordings, in order to examine the variation of orientation selectivity among local groups of neurons. We recorded a total of 321 cells from 62 sites in area 17 of halothane-anesthetized cats; each site contained between three to ten neurons that were estimated to be less than 65 μm away from the tetrode tip. For each cell, we determined the orientation tuning in response to moving bars. Of the cells tested, 8.4% were unresponsive, 22.7% had no preferential response to any particular orientation, while 68.8% were tuned. The average difference in preferred orientation between cell pairs recorded at the same site was 10.7 deg, but the variance in preferred orientation differences differed significantly among sites. Some clusters of cells exhibited the same or nearly the same orientation preference, while others had orientation preferences that differed by as much as 90 deg. Our data demonstrate that the tuning for orientation is more heterogeneously distributed at a local level than previous studies have suggested.

Keywords

Orientation selectivityVisual cortexCatsTetrodes
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 3 , May 1996 , pp. 509 - 516
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abeles, M. & Goldstein, M.H. (1977). Multispike train analysis. Proceedings of IEEE 65, 762–773.CrossRefGoogle Scholar
Albus, K. (1975). A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat. II. The spatial organization of the orientation domain. Experimental Brain Research 24, 159–179.CrossRefGoogle ScholarPubMed
Bauer, R. (1982). A high probability of an orientation shift between layers 4 and 5 in central parts of the cat striate cortex. Experimental Brain Research 48, 245–255.CrossRefGoogle ScholarPubMed
Bauer, R. & Fischer, W.H. (1987). Continuity or incontinuity of orientation columns in visual cortex: A critical evaluation of published and unpublished data. Neuroscience 22, 841–847.CrossRefGoogle ScholarPubMed
Bishop, P.O., Coombs, J.S., & Henry, G.H. (1971). Interaction effects of visual contours on the discharge frequency of simple striate neurons. Journal of Physiology 219, 659–687.CrossRefGoogle Scholar
Blasdel, G.G. & Salama, G. (1986). Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579–585.CrossRefGoogle ScholarPubMed
Bonhoeffer, T. & Grinvald, A. (1993). The layout of iso-orientation domains in area 18 of cat visual cortex: Optical imaging reveals a pinwheel-like organization. Journal of Neuroscience 13, 4157–4180CrossRefGoogle ScholarPubMed
Braitenberg, V. & Braitenberg, C. (1976). Geometry of orientation columns in the visual cortex. Biological Cybernetics 33, 179–186.CrossRefGoogle Scholar
Britten, K.H., Shadlen, M.N., Newsome, W.T., & Movshon, J.A. (1992). The analysis of visual motion: A comparison of neuronal and psychophysical performance. Journal of Neuroscience 12, 4745–4765.CrossRefGoogle Scholar
Chapman, B., Zahs, K.R., & Stryker, M.P. (1991). Relation of cortical orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. Journal of Neuroscience 11, 1347–1358.CrossRefGoogle ScholarPubMed
Creutzfeldt, O.D., Innocenti, C.M., & Brooks, D. (1974). Vertical organization in the visual cortex (area 17) of the cat. Experimental Brain Research 21, 315–336.CrossRefGoogle ScholarPubMed
Crook, J.M., Eysel, U.T., & Machemer, H.F. (1991). Influence of GABA-induced remote inactivation on the orienation tuning of cells of area 18 of feline visual cortex: A comparison with area 17. Neuroscience 40, 1–12.CrossRefGoogle Scholar
Donaldson, I.M. & Nash, J.R (1975). variability of the relative preference for stimulus orientation and direction of movement in some units of the cat visual cortex (areas 17 and 18). Journal of Physiology (London) 245, 305–324.CrossRefGoogle Scholar
Eysel, U.T., Crook, J.M., & Machemer, H.F. (1990). GABA-induced remote inactivation reveals cross-orientation inhibition in the cat stri-ate cortex. Experimental Brain Research 80, 626–630.CrossRefGoogle ScholarPubMed
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
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.CrossRefGoogle ScholarPubMed
Gray, C.M., Maldonado, P.E., Wilson, M.A., & Mcnaughton, B.L. (1995). Tetrodes markedly improve the reliability and yield of multiple single unit isolation from multiunit recordings in cat striate cortex. Journal of Neuroscience Methods 63, 43–54.CrossRefGoogle ScholarPubMed
Heogelund, P. & Albus, K. (1978). Response variability and orientation discrimination of single cells in striate cortex of cat. Experimental Brain Research 32, 197–211.Google Scholar
Henry, G.H., Dreher, B., & Bishop, P.O. (1974). Orientation specificity of cells in cat striate cortex. Journal of Neurophysiology 34, 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
Hubel, D.H. & Wiesel, T.N. (1963). Shape and arrangement of columns in cat's striate cortex. Journal of Physiology 165, 559–568.CrossRefGoogle ScholarPubMed
Kisvarday, Z.F., Kim, D.S., Eysel, U.T., & Bonhoeffer, T. (1994). Relationship between lateral inhibitory connections and the topography of the orientation maps in the cat visual cortex. European Journal of Neuroscience 6, 1619–1632.CrossRefGoogle ScholarPubMed
Lee, B.B., Albus, K., Heggelund, P., Hulme, M.J., & Creutzfeldt, O.D. (1977). The depth distribution of optimal stimulus orientation for neurons in cat area 17. Experimental Brain Research 27, 301–314.Google ScholarPubMed
Le Vay, S. & Nelson, S.B. (1991). Columnar organization of the visual cortex. In The Neural Basis of Visual Function, ed. Leventhal, A., pp. 266–315. Boca Raton, Florida: MacMillan. CRC Press.Google Scholar
Löwel, S., Freeman, B. & Singer, W. (1987). Topographic organization of the orientation column system in large flat-mounts of the cat visual cortex: A 2-deoxyglucose study. Journal of Comparative Neurology 255, 401–415.CrossRefGoogle ScholarPubMed
Matsubara, J.A., Cynader, M.S., & Swindale, N.V. (1987). Anatomical properties and physiological correlates of the intrinsic connections in cat area 18. Journal of Neuroscience 7, 1428–1446.CrossRefGoogle ScholarPubMed
Mountcastle, V.B. (1957). Modality and topographic properties of single neurons of cat's somatosensory cortex. Journal of Neurophysiology 20, 408–434.CrossRefGoogle Scholar
Murphy, P.C. & Sillito, A.M. (1986). Continuity of orientation columns between superficial and deep laminae of the cat primary visual cortex. Journal of Physiology 381, 95–110.CrossRefGoogle ScholarPubMed
Nelson, S., Toth, L., Sheth, B., & Sur, M. (1994). Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science 265, 174–117.CrossRefGoogle ScholarPubMed
Obermayer, K. & Blasdel, G.G. (1993). Geometry of orientation and ocular dominance columns in monkey striate cortex. Journal of Neuroscience 13, 4114–4129.CrossRefGoogle ScholarPubMed
O'Keefe, J.O. & Reece, M.L. (1993). Phase relationship between hip-pocampal place units and the EEC theta rhythm. Hippocampus 3, 317–330.CrossRefGoogle Scholar
Payne, B.R. & Berman, N. (1983). Functional organization of neurons in the cat striate cortex: Variations in preferred orientation and orientation selectivity with receptive-field type, ocular dominance, and location in the visual field map. Journal of Neurophysiology 49, 1051–1072.CrossRefGoogle ScholarPubMed
Pei, X., Vidyasagar, T.R., Volgushev, M., & Creutzfeldt, O.D. (1994). Receptive field analysis and orientation selectivity of post-synaptic potentials of simple cells in cat visual cortex. Journal of Neuroscience 14, 7130–7140.CrossRefGoogle Scholar
Pettigrew, J.D., Cooper, M.L., & Blasdel, G.G. (1979). Improved use of tapetal reflection for eye-position monitoring. Association Research Vision Ophthalmology 18, 490–495.Google ScholarPubMed
Schoppmann, A. & Stryker, M.P. (1981). Physiological evidence that the 2-deoxyglucose method reveals orientation columns in cat visual cortex. Nature 293, 574–576.CrossRefGoogle ScholarPubMed
Sillito, A.M., Kemp, J.A., Milson, J.A., & Berardi, N. (1980). A re-evaluation of the mechanisms underlying simple cell orientation selectivity. Brain Research 194, 517–520.CrossRefGoogle ScholarPubMed
Singer, W. (1981). Topographic organization of orientation columns in the cat visual cortex. Experimental Brain Research 44, 431–436.CrossRefGoogle ScholarPubMed
Swindale, N.V., Matsubara, J.A., & Cynader, M.S. (1987). Surface organization of orientation and direction selectivity in cat area 18. Journal of Neuroscience 7, 1414–1427.CrossRefGoogle ScholarPubMed
Vidyasagar, T.R. & Henry, G.H., (1990). Relationship between preferred orientation and ordinal position in neurones of cat striate cortex. Visual Neuroscience 5, 565–569.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 Neuroscience 10, 1151–1155.CrossRefGoogle ScholarPubMed
Wilson, M.A. & McNaughton, B.L. (1993). Dynamics of the hippocampal ensemble code for space. Science 261, 1055–1058.CrossRefGoogle ScholarPubMed