Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-25T05:19:49.591Z Has data issue: false hasContentIssue false
  • English
  • Français

Adaptation aftereffects in single neurons of cat visual cortex: Response timing is retarded by adapting

Published online by Cambridge University Press:  02 June 2009

Alan B. Saul
Alan B. Saul
Affiliation:
Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh
Get access Rights & Permissions [Opens in a new window]

Abstract

Extracellular single-unit recordings were made from simple cells in area 17 of anesthetized cats. Cells were tested with drifting gratings under control and adapted conditions. Response amplitude and phase were measured as a function of either contrast or temporal frequency. Adapting not only reduces amplitude, but also retards phase. Adaptation alters the responses of simple cells in a particular way: the onset of the response to each cycle of a sinusoidally modulated stimulus is delayed. Once cells start to respond during each cycle, however, they generally recover to control levels, and the offset of the response is unaffected by adapting. The timing aftereffects are independent of the amplitude aftereffects. Timing aftereffects are tuned around the adapting temporal frequency, with a bias toward lower temporal frequencies. Adaptation thus modifies cortical responses even more specifically then previously thought. Firing rates are depressed primarily at response onset, even after several stimulus cycles have occurred following the end of adapting. Because all cells appear to adapt in this way, the data offer an opportunity to theorize about cortical connectivity. One implication is that inhibition onto a simple cell arises from other simple cells with similar response properties that fire a half-cycle out of phase with the target cell.

Keywords

Adaptation aftereffectsVisual cortexSimple cellsResponse timingIntracortical inhibition
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 2 , March 1995 , pp. 191 - 205
Copyright
Copyright © Cambridge University Press 1995

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

Albrecht, D.G., Farrar, S.B. & Hamilton, D.B. (1984). Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. Journal of Physiology 347, 713–739.CrossRefGoogle ScholarPubMed
Blakemore, C. & Tobin, E.A. (1972). Lateral inhibition between orientation detectors in the cat's visual cortex. Experimental Brain Research 15, 439–440.Google Scholar
Bonds, A.B. (1991). Temporal dynamics of contrast gain in single cells of the cat striate cortex. Visual Neuroscience 6, 239–255.CrossRefGoogle ScholarPubMed
Carandini, M. & Heeger, D.J. (1994). Summation and division by neurons in primate visual cortex. Science 264, 1333–1336.Google Scholar
Dealy, R.S. & Tolhurst, D.J. (1974). Is spatial adaptation an aftereffect of prolonged inhibition? Journal of Physiology 241, 261–270.Google Scholar
Dean, A.F. (1983). Adaptation-induced alteration of the relation between response amplitude and contrast in cat striate cortex neurones. Vision Research 23, 249–256.CrossRefGoogle Scholar
Dean, A.F. & Tolhurst, D.J. (1986). Factors influencing the temporal phase of response to bar and grating stimuli for simple cells in the cat striate cortex. Experimental Brain Research 62, 143–151.Google Scholar
DeAngelis, G.C., Ohzawa, I. & Freeman, R.D. (1993). Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. Journal of Neurophysiology 69, 1091–1117.Google Scholar
DeBruyn, E.J. & Bonds, A.B. (1986). Contrast adaptation in cat visual cortex is not mediated by GABA. Brain Research 383, 339–342.Google Scholar
Ferster, D. (1986). Orientation selectivity of synaptic potentials in neurons of cat visual cortex. Journal of Neuroscience 6, 1284–1301.Google Scholar
Ferster, D. (1988). Spatially opponent excitation and inhibition in simple cells of the cat visual cortex. Journal of Neuroscience 8, 1172–1180.Google Scholar
Giaschi, D., Douglas, R., Marlin, S. & Cynader, M. (1993). The time course of direction-selective adaptation in simple and complex cells in cat striate cortex. Journal of Neurophysiology 70, 2024–2034.Google Scholar
Hamilton, D.B., Albrecht, D.G. & Geisler, W. S. (1989). Visual cortical receptive fields in monkey and cat: Spatial and temporal phase transfer function. Vision Research 29, 1285–1308.Google Scholar
Hammond, P., Mouat, G.S. & Smith, A.T. (1985). Motion aftereffects in cat striate cortex elicited by moving gratings. Experimental Brain Research 60, 411–416.CrossRefGoogle ScholarPubMed
Hammond, R., Mouat, G.S. & Smith, A.T. (1986). Motion aftereffects in cat striate cortex elicited by moving texture. Vision Research 26, 1055–1060.CrossRefGoogle ScholarPubMed
Hammond, P., Mouat, G.S. & Smith, A.T. (1988). Neural correlates of motion aftereffects in cat striate cortical neurones: Monocular adaptation. Experimental Brain Research 72, 1–20.Google Scholar
Hammond, P. & Mouat, G.S. (1988). Neural correlates of motion aftereffects in cat striate cortical neurones: Interocular transfer. Experimental Brain Research 72, 21–28.Google Scholar
Hammond, P., Pomfrett, C.J.D. & Ahmed, B. (1989). Neural motion aftereffects in the cat's striate cortex: Orientation selectivity. Vision Research 29, 1671–1683.Google Scholar
Heeger, D.J. (1992). Normalization of cell responses in cat striate cortex. Visual Neuroscience 9, 181–197.Google Scholar
Heggelund, P. (1986). Quantitative studies of enhancement and suppression zones in the receptive field of simple cells in cat striate cortex. Journal of Physiology 373, 293–310.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1959). Receptive fields of single neurones in cat's visual cortex. Journal of Physiology 160, 106–154.Google Scholar
Humphrey, A.L. & Weller, R.E. (1988). Structural correlates of functionally distinct X-cells in the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 268, 448–468.CrossRefGoogle ScholarPubMed
Kulikowski, J.J., Rao, V.M. & Vidyasagar, T.R. (1981). Effects of directional adaptation on the response profiles of simple cells in the visual cortex of cat and macaque. Journal of Physiology 318, 21.Google Scholar
Lee, B.B., Elepfandt, A. & Virsu, V. (1981). Phase of responses to sinusoidal gratings of simple cells in cat striate cortex. Journal of Neurophysiology 45, 818–828.Google Scholar
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.Google Scholar
Maffei, L., Fiorentini, A. & Bisti, S. (1973). Neural correlate of perceptual adaptation to gratings. Science 182, 1036–1038.CrossRefGoogle ScholarPubMed
Maffei, L., Bernardi, N. & Bisti, S. (1986). Interocular transfer of adaptation after effect in neurons of area 17 and 18 of split chiasm cats. Journal of Neurophysiology 55, 966–976.Google Scholar
Marlin, S.G., Hasan, S.J. & Cynader, M. (1988). Direction-selective adaptation in simple and complex cells in cat striate cortex. Journal of Neurophysiology 59, 1314–1330.CrossRefGoogle ScholarPubMed
Marlin, S.G., Douglas, R.M. & Cynader, M.S. (1991). Position-specific adaptation in simple cell receptive fields of the cat striate cortex. Journal of Neurophysiology 66, 1769–1784.CrossRefGoogle ScholarPubMed
Marlin, S.G., Douglas, R.M. & Cynader, M.S. (1993). Positionspecific adaptation in complex cell receptive fields of the cat striate cortex. Journal of Neurophysiology 69, 2209–2221.CrossRefGoogle ScholarPubMed
McLean, J. & Palmer, L.A. (1992). Contrast adaptation and excitatory amino acid (EAA) receptors in striate cortex. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1021.Google Scholar
McLean, J., Raab, S. & Palmer, L.A. (1994). Contribution of linear mechanisms to the specification of local motion by simple cells in areas 17 and 18 of the cat. Visual Neuroscience 11, 271–294.CrossRefGoogle Scholar
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978). Spatial summation in the receptive fields of simple cells in the cat's striate cortex. Journal of Physiology 283, 53–77.Google Scholar
Movshon, J.A. & Lennie, P. (1979). Pattern-selective adaptation in visual cortical neurones. Nature 278, 850–852.Google Scholar
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat's visual system. Journal of Neurophysiology 54, 651–667.Google Scholar
Palmer, L.A. & Davis, T.L. (1981). Receptive-field structure in cat striate cortex. Journal of Neurophysiology 46, 260–276.Google Scholar
Pettet, M.W. & Gilbert, C.D. (1992). Dynamic changes in receptive-field size in cat primary visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 89, 8366–8370.Google Scholar
Reid, R.C., Victor, J.D. & Shapley, R.M. (1992). Broad-band temporal stimuli decrease the integration time of neurons in cat striate cortex. Visual Neuroscience 9, 39–45.Google Scholar
Saul, A.B. & Daniels, J.D. (1986). Modeling and simulation II: Specificity models for visual cortex development. Journal of Electrophysiological Techniques 13, 211–231.Google Scholar
Saul, A.B. & Cynader, M.S. (1989 a). Adaptation in single units in visual cortex: The tuning of aftereffects in the spatial domain. Visual Neuroscience 2, 593–607.Google Scholar
Saul, A.B. & Cynader, M.S. (1989 b). Adaptation in single units in visual cortex: The tuning of aftereffects in the temporal domain. Visual Neuroscience 2, 609–620.Google Scholar
Saul, A.B. & Humphrey, A.L. (1990). Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. Journal of Neurophysiology 64, 206–224.Google Scholar
Saul, A.B. & Humphrey, A.L. (1992 a). Temporal-frequency tuning of direction selectivity in cat visual cortex. Visual Neuroscience 8, 365–372.Google Scholar
Saul, A.B. & Humphrey, A.L. (1992 b). Evidence of input from lagged cells in the lateral geniculate nucleus to simple cells in cortical area 17 of the cat. Journal of Neurophysiology 68, 1190–1208.CrossRefGoogle ScholarPubMed
Saul, A.B. (1993). Adapting retards response timing in single neurons of cat visual cortex. Society for Neuroscience Abstracts 19, 1575.Google Scholar
Shapley, R.M. & Victor, J.D. (1981). How the contrast gain control modifies the frequency response of cat retinal ganglion cells. Journal of Physiology 318, 161–179.CrossRefGoogle ScholarPubMed
Tolhurst, D.J. & Dean, A.F. (1987). Spatial summation by simple cells in the striate cortex of the cat. Experimental Brain Research 66, 607–620.Google Scholar
Tolhurst, D.J. & Dean, A.F. (1990). The effects of contrast on the linearity of spatial summation of simple cells in the cat's striate cortex. Experimental Brain Research 79, 582–588.CrossRefGoogle ScholarPubMed
Vautin, R.G. & Berkley, M.A. (1977). Responses of single cells in cat visual cortex to prolonged stimulus movement: Neural correlates of visual aftereffects. Journal of Neurophysiology 40, 1051–1065.CrossRefGoogle ScholarPubMed
Victor, J.D. (1987). The dynamics of the cat retinal X-cell centre. Journal of Physiology 386, 219–246.CrossRefGoogle ScholarPubMed
Victor, J.D. (1988). The dynamics of the cat retinal Y-cell subunit. Journal of Physiology 405, 289–320.Google Scholar
Vidyasagar, T.R. (1990). Pattern adaptation in cat visual cortex is a co-operative phenomenon. Neuroscience 36, 175–179.Google Scholar
Von Der Heydt, R., Hanny, P. & Adorjani, C. (1978). Movement aftereffects in the visual cortex. Archives of Italian Biology 116, 248–254.Google Scholar
Wilson, H.R. (1975). A synaptic model for spatial-frequency adaptation. Journal of Theoretical Biology 50, 327–352.Google Scholar
Wilson, H.R. & Humanski, R. (1993). Spatial-frequency adaptation and contrast gain control. Vision Research 33, 1133–1149.Google Scholar