Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-17T01:18:47.124Z Has data issue: false hasContentIssue false
  • English
  • Français

Adaptation in single units in visual cortex: The tuning of aftereffects in the temporal domain

Published online by Cambridge University Press:  02 June 2009

A. B. Saul  and
M. S. Cynader
A. B. Saul
Affiliation:
Department of Neurobiology, Anatomy, and Cell Science, University of Pittsburgh, Pittsburgh
M. S. Cynader
Affiliation:
Department of Ophthalmology, University of British Columbia, British Columbia
Get access Rights & Permissions [Opens in a new window]

Abstract

Adaptation-induced changes in the temporal-frequency tuning and direction selectivity of cat visual cortical cells were studied. Aftereffects were induced largely independent of direction. Adapting in either direction reduced responses in both directions. Aftereffects in the direction opposite that adapted were only slightly weaker than were aftereffects in the adapted direction. No cell showed any enhancement of responses to drifting test stimuli after adapting with moving gratings. Adapting in a cell's null direction usually had no effect. Dramatic differences between the adaptation characteristics of moving and stationary stimuli were observed, however.

Furthermore, aftereffects were temporal frequency specific. Temporal frequency-specific aftereffects were found in both directions: adapting in one direction induced frequency-specific effects in both directions. This bidirectionality of frequency-specific aftereffects applied to the spatial domain as well. Often, aftereffects in the direction opposite that adapted were more narrowly tuned.

In general, adaptation could shift a cell's preferred temporal frequency. Aftereffects were most prominent at high temporal frequencies when testing in the adapted direction. Aftereffects seemed to be more closely linked to temporal frequency than to velocity matching.

These results constrain models of cortical connectivity. In particular, we argue against schemes by which direction selectivity is generated by inhibiting a cell specifically when stimulated in the nonpreferred direction. Instead, we argue that cells receive bidirectional spatially and temporally tuned inputs, which could combine in spatiotemporal quadrature to produce direction selectivity.

Keywords

Adaptation aftereffectsTemporal frequencyDirection selectivityIntracortical inhibitionCortical organization
Type
Research Article
Information
Visual Neuroscience , Volume 2 , Issue 6 , June 1989 , pp. 609 - 620
Copyright
Copyright © Cambridge University Press 1989

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 A 2, 284–299.CrossRefGoogle ScholarPubMed
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. & Campbell, F.W. (1969). On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. Journal of Physiology 203, 237–260.CrossRefGoogle Scholar
Blakemore, C, Nachmas, J. & Sutton, P. (1970). The perceived spatial frequency shift: evidence for frequency-selective neurones in the human brain. Journal of Physiology 219, 727–750.CrossRefGoogle Scholar
Carpenter, R.H.S. & Blakemore, C. (1973). Interaction between orientations in human vision. Experimental Brain Research 18, 287–303.CrossRefGoogle ScholarPubMed
Creutzfeldt, O.D., Kuhnt, U. & Benevento, L.A. (1974). An intra-cellular analysis of visual cortical neurons to moving stimuli: responses in a cooperative neuronal network. Experimental Brain Research 21, 251–274.CrossRefGoogle Scholar
Dealy, R.S. & Tolhurst, D.J. (1974). Is spatial adaptation an aftereffect of prolonged inhibition? Journal of Physiology 241, 261–270.CrossRefGoogle ScholarPubMed
Dean, A.F. (1983). Adaptation-induced alteration of the relation between response amplitude and contrast in cat striate cortical neurones. Vision Research 23, 249–256.CrossRefGoogle ScholarPubMed
Hammond, P., Mouat, G.S.V. & Smith, A.T. (1985). Motion aftereffects in cat striate cortex elicited by moving gratings. Experimental Brain Research 60, 411–416.CrossRefGoogle ScholarPubMed
Hammond, P., Mouat, G.S.V. & 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.V. & Smith, A.T. (1988). Neural correlates of motion aftereffects in cat striate cortical neurones: monocular adaptation. Experimental Brain Research 72, 1–20.CrossRefGoogle ScholarPubMed
Hebb, D.O. (1949). The Organization of Behavior. New York: Wiley.Google Scholar
Heggelund, P. & Hohmann, A. (1976). Long-term retention of the “Gilinsky-effect”. Vision Research 16, 1015–1017.CrossRefGoogle ScholarPubMed
Humphrey, A.L. & Weller, R.E. (1988). Functionally distinct groups of X cells in the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 268, 429–447.CrossRefGoogle ScholarPubMed
Julesz, B. (1971). Foundations of Cyclopean Perception. Chicago: University of Chicago Press.Google Scholar
Levinson, E. & Sekuler, R. (1975). Inhibition and disinhibition of direction-specific mechanisms in human vision. Nature 254, 692–694.CrossRefGoogle ScholarPubMed
Lovegrove, W. (1976). Inhibition in simultaneous and successive contour interaction in human vision. Vision Research 16, 1519–1521.CrossRefGoogle ScholarPubMed
Maffei, L., Berardi, N. & Bisti, S. (1986). Interocular transfer of adaptation aftereffect in neurons of area 17 and 18 of split chiasm cats. Journal of Neurophysiology 55, 966–976.CrossRefGoogle ScholarPubMed
Magnussen, S. & Johnsen, T. (1986). Temporal aspects of spatial adaptation. A study of the tilt aftereffect. Vision Research 26, 661–672.CrossRefGoogle ScholarPubMed
Mandler, M.B. (1984). Temporal-frequency discrimination above threshold. Vision Research 24, 1873–1880.CrossRefGoogle ScholarPubMed
Marlin, S.G., Hasan, S.J. & Cynader, M.S. (1988). Direction selective adaptation in simple and complex cells in cat striate cortex. Journal of Neurophysiology 59, 1314–1330.CrossRefGoogle ScholarPubMed
Mastronarde, D.N. (1987). Two classes of single-input X cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. Journal of Neurophysiology 57, 381–413.CrossRefGoogle ScholarPubMed
McCollough, C. (1965). Color adaptation of edge-detectors in the human visual system. Science 149, 1115–1116.CrossRefGoogle ScholarPubMed
Movshon, J.A. & Lennie, P. (1979). Pattern-selective adaptation in visual cortical neurones. Nature 278, 850–852.CrossRefGoogle ScholarPubMed
Movshon, J.A., Bonds, A.B. & Lennie, P. (1980). Pattern adaptation in striate cortical neurons. Investigative Ophthalmology and Visual Science (Suppl.) 21, 193.Google Scholar
Nakayama, K. (1985). Biological image motion processing: a review. Vision Research 25, 625–660.CrossRefGoogle ScholarPubMed
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat's visual system. Journal of Neurophysiology 54, 651–667.CrossRefGoogle ScholarPubMed
Orban, G.A., Hoffmann, K.-P. & Duysens, J. (1985). Velocity selectivity in the cat visual system. I. Responses of LGN cells to moving bar stimuli: a comparison with cortical areas 17 and 18. Journal of Neurophysiology 54, 1026–1049.CrossRefGoogle Scholar
Pantle, A. & Sekuler, R. (1969). Contrast response of human visual mechanisms sensitive to orientation and direction of motion. Vision Research 9, 397–406.CrossRefGoogle Scholar
Pantle, A. (1974). Motion aftereffect magnitude as a measure of the spatio-temporal response properties of direction-sensitive analyzers. Vision Research 14, 1229–1236.CrossRefGoogle ScholarPubMed
Reichardt, W. (1961). Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. In Sensory Communication, ed. Rosenblith, W.A., New York: Wiley, pp. 303–317.Google Scholar
SAUL, A.B. (1982). Development and mechanisms of visual cortical specificity. Society for Neuroscience Abstracts 8, 296.Google Scholar
Saul, A.B. & Daniels, J.D. (1985). Adaptation effects from conditioning area 17 cortical units in kittens during physiological recording. Society for Neuroscience Abstracts 11, 461.Google Scholar
Saul, A.B. & Daniels, J.D. (1986). Modeling and simulation. II: Specificity models for visual cortex development. Journal of Electrophys-iological Techniques 13, 211–231.Google Scholar
Saul, A.B. & Cynader, M.S. (1989). Adaptation in single units in visual cortex: the tuning of aftereffects in the spatial domain. Visual Neuroscience 2, 593–607.CrossRefGoogle ScholarPubMed
Sekuler, R.W. & Ganz, L. (1963). Aftereffect of seen motion with a stabilized image. Science 139, 419–420.CrossRefGoogle Scholar
Shadlen, M. & Carney, T. (1986). Mechanisms of human motion perception revealed by a new cyclopean illusion. Science 232, 95–97.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Victor, J.D. (1981). How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. Journal of Physiology 318, 161–179.CrossRefGoogle ScholarPubMed
Sillito, A.M. (1977). Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex. Journal of Physiology 271, 699–720.CrossRefGoogle ScholarPubMed
Stecher, S., Sigel, C. & Lange, R.V. (1973). Spatial-frequency channels in human vision and the threshold for adaptation. Vision Research 13, 1691–1700.CrossRefGoogle ScholarPubMed
Thompson, P. (1981). Velocity aftereffects: the effects of adaptation to moving stimuli on the perception of subsequently seen moving stimuli. Vision Research 21, 337–345.CrossRefGoogle ScholarPubMed
Thompson, P. (1983). Discrimination of moving gratings at and above detection threshold. Vision Research 23, 1533–1538.CrossRefGoogle ScholarPubMed
Tolhurst, D.J. (1972). Adaptation to square-wave gratings: inhibition between spatial-frequency channels in the human visual system. Journal of Physiology 226, 231–248.CrossRefGoogle ScholarPubMed
Ullman, S. & Schechtman, G. (1982). Adaptation and gain normalization. Proceedings of the Royal Society B (London) 216, 299–313.Google ScholarPubMed
van Santen, J.P.H. & Sperling, G. (1984). Temporal covariance model of human motion perception. Journal of the Optical Society of America A 1, 451–473.CrossRefGoogle ScholarPubMed
van Santen, J.P.H. & Sperling, G. (1985). Elaborated Reichardt detectors. Journal of the Optical Society of America A 2, 300–321.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
von der Heydt, R., Hänny, P. & Adorjani, C. (1978). Movement aftereffects in the visual cortex. Archives of Italian Biology 116, 248–254.Google ScholarPubMed
Watson, A.B. & Ahumada, A.J. (1985). Model of human visual-motion sensing. Journal of the Optical Society of America A 2, 322–342.CrossRefGoogle ScholarPubMed
Wilson, H.R. (1975). A synaptic model for spatial-frequency adaptation. Journal of Theoretical Biology 50, 327–352.CrossRefGoogle ScholarPubMed