Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-26T11:10:16.061Z Has data issue: false hasContentIssue false
  • English
  • Français

Temporal-frequency tuning of direction selectivity in cat visual cortex

Published online by Cambridge University Press:  02 June 2009

Alan B. Saul  and
Allen L. Humphrey
Alan B. Saul
Affiliation:
Department of Neurobiology, Anatomy, and Cell Science, University of Pittsburgh School of Medicine, Pittsburgh
Allen L. Humphrey
Affiliation:
Department of Neurobiology, Anatomy, and Cell Science, University of Pittsburgh School of Medicine, Pittsburgh
Get access Rights & Permissions [Opens in a new window]

Abstract

Responses of 71 cells in areas 17 and 18 of the cat visual cortex were recorded extracellularly while stimulating with gratings drifting in each direction across the receptive field at a series of temporal frequencies. Direction selectivity was most prominent at temporal frequencies of 1–2 Hz. In about 20% of the total population, the response in the nonpreferred direction increased at temporal frequencies of around 4 Hz and direction selectivity was diminished or lost. In a few cells the preferred direction reversed.

One consequence of this behavior was a tendency for the preferred direction to have lower optimal temporal frequencies than the nonpreferred direction. Across the population, the preferred direction was tuned almost an octave lower. In spite of this, temporal resolution was similar in the two directions. It appeared that responses in the nonpreferred direction were suppressed at low frequencies, then recovered at higher frequencies.

This phenomenon might reflect the convergence in visual cortex of lagged and nonlagged inputs from the lateral geniculate nucleus. These afferents fire about a quarter-cycle apart (i.e. are in temporal quadrature) at low temporal frequencies, but their phase difference increases to a half-cycle by about 4 Hz. Such timing differences could underlie the prevalence of direction-selective cortical responses at 1 and 2 Hz and the loss of direction selectivity in many cells by 4 or 8 Hz.

Keywords

Temporal frequencyDirection selectivityVisual cortexLateral geniculate nucleusLagged cells
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 4 , April 1992 , pp. 365 - 372
Copyright
Copyright © Cambridge University Press 1992

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

Adelson, E.H. & Bergen, J.R. (1985). Spatiotemporal energy models for the perception of motion. Journal of the Optical Society of America 2, 284–299.CrossRefGoogle ScholarPubMed
BakerC.L., Jr. C.L., Jr. & Cynader, M.S. (1986). Spatial receptive-field properties of direction-selective neurons in cat striate cortex. Journal of Neurophysiology 55, 1136–1152.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in rabbit's retina. Journal of Physiology 178, 477–504.CrossRefGoogle ScholarPubMed
Bonds, A.B. (1991). Temporal dynamics of contrast gain in single cells of the cat striate cortex. Visual Neuroscience 6, 239–255.CrossRefGoogle ScholarPubMed
De Valois, R.L., Albrecht, D.G. & Thorell, L.G. (1982). Spatial-frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545–559.CrossRefGoogle ScholarPubMed
Duysens, J., Maes, H. & Orban, G.A. (1987). The velocity dependence of direction selectivity of visual cortical neurones in the cat. Journal of Physiology 387, 95–113.CrossRefGoogle ScholarPubMed
Emerson, R.C. & Gerstein, G.L. (1977). Simple striate neurons in the cat. II. Mechanisms underlying directional asymmetry and directional selectivity. Journal of Neurophysiology 40, 136–155.CrossRefGoogle ScholarPubMed
Eysel, U.T., Worgotter, F. & Pape, H.-C. (1987). Local cortical lesions abolish lateral inhibition at direction-selective cells in cat visual cortex. Experimental Brain Research 68, 606–612.CrossRefGoogle ScholarPubMed
Eysel, U.T., Muche, T. & Worgotter, F. (1988). Lateral interactions at direction-selective striate neurones in the cat demonstrated by local cortical inactivation. Journal of Physiology 399, 657–675.CrossRefGoogle ScholarPubMed
Goodwin, A.W., Henry, G.H. & Bishop, P.O. (1975). Direction selectivity of simple striate cells: properties and mechanism. Journal of Neurophysiology 38, 1500–1523.CrossRefGoogle ScholarPubMed
Goodwin, A.W. & Henry, G.H. (1978). The influence of stimulus velocity on the responses of single neurons in the striate cortex. Journal of Physiology 277, 467–482.CrossRefGoogle ScholarPubMed
Holub, R.A. & Morton-Gibson, M. (1981). Response of visual cortical neurons of the cat to moving sinusoidal gratings: response-contrast functions and spatiotemporal interactions. Journal of Neurophysiology 46, 1244–1259.CrossRefGoogle ScholarPubMed
Humphrey, A.L., Sur, M., Uhlrich, D.J. & Sherman, S.M. (1985). Projection patterns of individual X- and Y-cell axons from the lateral geniculate nucleus to cortical area 17 in the cat. Journal of Comparative Neurology 233, 159–189.CrossRefGoogle ScholarPubMed
Humphrey, A.L. & Weller, R.E. (1988a). Functionally distinct groups of X-cells in the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 268, 429–447.CrossRefGoogle ScholarPubMed
Humphrey, A.L. & Weller, R.E. (1988b). Structural correlates of functionally distinct X-cells in the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 268, 448–468.CrossRefGoogle ScholarPubMed
Maddess, T., Mccourt, M.E., Blakeslee, B. & Cunningham, R.B. (1988). Factors governing the adaptation of cells in area 17 of the cat visual cortex. Biological Cybernetics 59, 229–236.CrossRefGoogle ScholarPubMed
Mastronarde, D.N. (1987). Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells. Journal of Neurophysiology 57, 357–380.CrossRefGoogle ScholarPubMed
Mastronarde, D.N., Saul, A.B. & Humphrey, A.L. (1991). Lagged Y cells in the cat lateral geniculate nucleus. Visual Neuroscience 7, 191–200.CrossRefGoogle ScholarPubMed
Mclean, J. & Palmer, L. (1989). Contribution of linear spatiotemporal receptive-field structure to velocity selectivity of simple cells in area 17 of cat. Vision Research 29, 675–679.CrossRefGoogle ScholarPubMed
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978). Spatial summation in the receptive fields of simple cell in the cat's striate cortex. Journal of Physiology 283, 53–77.CrossRefGoogle ScholarPubMed
Mullikin, W.H., Jones, J.P. & Palmer, L.A. (1984). Receptive-field properties and laminar distribution of X-like and Y-like simple cells in cat area 17. Journal of Neurophysiology 52, 350–371.CrossRefGoogle ScholarPubMed
Nelson, S.B. (1991). Temporal interactions in the cat visual system. I. Orientation-selective suppression in the visual cortex. Journal of Neuroscience 11, 344–356.CrossRefGoogle ScholarPubMed
Orban, G.A., Kennedy, H. & Maes, H. (1981). Response to movement of neurons in areas 17 and 18 of the cat: direction selectivity. Journal of Neurophysiology 45, 1059–1073.CrossRefGoogle ScholarPubMed
Orban, G.A., Hoffman, K.-P. & Duysens, J. (1985). Velocity selectivity in the cat visual system. 1. Responses of LGN cells to moving bar stimuli: a comparison with cortical areas 17 and 18. Journal of Neurophysiology 54, 1026–1049.CrossRefGoogle Scholar
Press, W.H., Flannery, B.P., Teukolsky, S.A. & Vetterling, W.T. (1986). Numerical Recipes: The Art of Scientific Computing. Cambridge, UK: Cambridge University Press.Google Scholar
Reid, R.C. (1988). Directional selectivity and the spatiotemporal structure of the receptive fields of simple cells in cat striate cortex. Ph.D. Dissertation, Rockefeller University.Google Scholar
Reid, R.C., Soodak, R.E. & Shapley, R.M. (1987). Linear mechanisms of directional selectivity in simple cells of cat striate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 84, 8740–8744.CrossRefGoogle ScholarPubMed
Reid, R.C., Soodak, R.E. & Shapley, R.M. (1991). Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. Journal of Neurophysiology 66, 505–529.CrossRefGoogle ScholarPubMed
Saul, A.B. & Cynader, M.S. (1989). Adaptation in single units in visual cortex: the tuning of aftereffects in the temporal domain. Visual Neuroscience 2, 609–620.CrossRefGoogle ScholarPubMed
Saul, A.B. & Humphrey, A.L. (1989). Phase differences in the cat LGN and cortical direction selectivity. Society for Neuroscience Abstracts 15, 1394.Google Scholar
Saul, A.B. & Humphrey, A.L. (1990a). Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. Journal of Neurophysiology 64, 206–224.CrossRefGoogle ScholarPubMed
Saul, A.B. & Humphrey, A.L. (1990b). Evidence of lagged-type geniculate input to visual cortex. Society for Neuroscience Abstracts 16, 1218.Google Scholar
Saul, A.B. & Humphrey, A.L. (1991). Cortical direction selectivity as a function of temporal frequency. Society for Neuroscience Abstracts 17, 1015.Google Scholar
Shadlen, M. & Carney, T. (1986). Mechanisms of human motion perception revealed by a new cyclopean illusion. Science 232, 95–97.CrossRefGoogle ScholarPubMed
Tolhurst, D.J. & Doan, A.F. (1991). Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex. Visual Neuroscience 6, 421–428.CrossRefGoogle ScholarPubMed
Van Santen, J.P.H. & Sperling, G. (1985). Elaborated Reichardt detectors. Journal of the Optical Society of America 2, 300–321.CrossRefGoogle ScholarPubMed
Watson, A.B. & AhumadaA.J., Jr. A.J., Jr. (1983). A look at motion in the frequency domain. In Motion: Perception and Representation, ed. Tsotsos, J.K., pp. 1–10. New York: Association for Computing Machinery.Google Scholar
Watson, A.B. & AhumadaA.J., Jr. A.J., Jr. (1985). Model of human visual-motion sensing. Journal of the Optical Society of America 2, 322–342.CrossRefGoogle ScholarPubMed