Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-24T13:13:02.919Z Has data issue: false hasContentIssue false

Temporal interactions in direction-selective complex cells of area 18 and the posteromedial lateral suprasylvian cortex (PMLS) of the cat

Published online by Cambridge University Press:  24 April 2006

ILDIKÓ VAJDA
Affiliation:
Department of Functional Neurobiology and Helmholtz Institute, Utrecht University, Utrecht, The Netherlands Current address: KNAW, Netherlands Institute for Brain Research, Amsterdam, The Netherlands
BART G. BORGHUIS
Affiliation:
Department of Functional Neurobiology and Helmholtz Institute, Utrecht University, Utrecht, The Netherlands Current address: Department of Neuroscience, University of Pennsylvania, Philadelphia, USA
WIM A. VAN DE GRIND
Affiliation:
Department of Functional Neurobiology and Helmholtz Institute, Utrecht University, Utrecht, The Netherlands
MARTIN J.M. LANKHEET
Affiliation:
Department of Functional Neurobiology and Helmholtz Institute, Utrecht University, Utrecht, The Netherlands

Abstract

Temporal interactions in direction-sensitive complex cells in area 18 and the posteromedial lateral suprasylvian cortex (PMLS) were studied using a reverse correlation method. Reverse correlograms to combinations of two temporally separated motion directions were examined and compared in the two areas. A comparison to the first-order reverse correlograms allowed us to identify nonlinear suppression or facilitation due to pairwise combinations of motion directions. Results for area 18 and PMLS were very different. Area 18 showed a single type of nonlinear behavior: similar directions facilitated and opposite directions suppressed spike probability. This effect was most pronounced for motion steps that followed each other immediately and decreased with increasing delay between steps. In PMLS, the picture was much more diverse. Some cells exhibited nonlinear interactions, that were opposite to those in area 18 (facilitation for opposite directions and suppression for similar ones), while the majority did not show a systematic interaction profile. We conclude that nonlinear second-order reverse correlation characteristics reveal different functional properties, despite similarities in the first-order reverse correlation profiles. Directional interactions in time revealed optimal integration of similar directions in area 18, but motion opponency—at least in some cells—in PMLS.

Type
Research Article
Copyright
2006 Cambridge University Press

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

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, 284299.CrossRefGoogle Scholar
Akase, E., Inokawa, H., & Toyama, K. (1998). Neuronal responsiveness to three-dimensional motion in cat posteromedial lateral suprasylvian cortex. Experimental Brain Research 122, 214226.CrossRefGoogle Scholar
Bacon, B.A., Mimeault, D., Lepore, F., & Guillemot, J.P. (2001). Spatial disparity sensitivity in area PMLS of the Siamese cat. Brain Research 906, 149156.CrossRefGoogle Scholar
Bair, W., Cavanaugh, J.R., Smith, M.A., & Movshon, J.A. (2002). The timing of response onset and offset in macaque visual neurons. Journal of Neuroscience 22, 31893205.Google Scholar
Baker, C.L., Jr. (2001). Linear filtering and nonlinear interactions in direction-selective visual cortex neurons: A noise correlation analysis. Visual Neuroscience 18, 465485.CrossRefGoogle Scholar
Bando, T., Takagi, M., Toda, H., & Yoshizawa, T. (1992). Functional roles of the lateral suprasylvian cortex in ocular near response in the cat. Neuroscience Research 15, 162178.CrossRefGoogle Scholar
Borghuis, B.G., Perge, J.A., Vajda, I., van Wezel, R.J., van de Grind, W.A., & Lankheet, M.J. (2003). The motion reverse correlation (MRC) method: A linear systems approach in the motion domain. Journal of Neuroscience Methods 123, 153166.CrossRefGoogle Scholar
Brenner, E. & Rauschecker, J.P. (1990). Centrifugal motion bias in the cat's lateral suprasylvian visual cortex is independent of early flow field exposure. Journal of Physiology 423, 641660.CrossRefGoogle Scholar
Brosseau-Lachaine, O., Faubert, J., & Casanova, C. (2001). Functional sub-regions for optic flow processing in the posteromedial lateral suprasylvian cortex of the cat. Cerebral Cortex 11, 9891001.CrossRefGoogle Scholar
Camarda, R. & Rizzolatti, G. (1976). Visual receptive fields in the lateral suprasylvian area (Clare-Bishop area) of the cat. Brain Research 101, 427443.CrossRefGoogle Scholar
Casanova, C., Savard, T., Nordmann, J.P., Molotchnikoff, S., & Minville, K. (1995). Comparison of the responses to moving texture patterns of simple and complex cells in the cat's area 17. Journal of Neurophysiology 74, 12711286.Google Scholar
Citron, M.C. & Emerson, R.C. (1983). White noise analysis of cortical directional selectivity in cat. Brain Research 279, 271277.CrossRefGoogle Scholar
Crook, J.M. (1990). Directional tuning of cells in area 18 of the feline visual cortex for visual noise, bar and spot stimuli: a comparison with area 17. Experimental Brain Research 80, 545561.Google Scholar
Emerson, R.C., Citron, M.C., Vaughn, W.J., & Klein, S.A. (1987). Nonlinear directionally selective subunits in complex cells of cat striate cortex. Journal of Neurophysiology 58, 3365.Google Scholar
Emerson, R.C., Korenberg, J., & Citron, M.C. (1992). Identification of complex-cell intensive nonlinearities in a cascade model of cat visual cortex. Biological Cybernetics 66, 291300.CrossRefGoogle Scholar
Gaska, J.P., Jacobson, L.D., Chen, H.W., & Pollen, D.A. (1994). Space-time spectra of complex cell filters in the macaque monkey: A comparison of results obtained with pseudowhite noise and grating stimuli. Visual Neuroscience 11, 805821.CrossRefGoogle Scholar
Hamada, T. (1987). Neural response to the motion of textures in the lateral suprasylvian area of cats. Behavioral Brain Research 25, 175185.CrossRefGoogle Scholar
Hammond, P. & Ahmed, B. (1985). Length summation of complex cells in cat striate cortex: A reappraisal of the “special/standard” classification. Neuroscience 15, 639649.CrossRefGoogle Scholar
Hammond, P. & MacKay, D.M. (1975). Differential responses of cat visual cortical cells to textured stimuli. Experimental Brain Research 22, 427430.Google Scholar
Hammond, P. & MacKay, D.M. (1977). Differential responsiveness of simple and complex cells in cat striate cortex to visual texture. Experimental Brain Research 30, 275296.Google Scholar
Hammond, P. & Pomfrett, C.J. (1989). Directional and orientational tuning of feline striate cortical neurones: correlation with neuronal class. Vision Research 29, 653662.CrossRefGoogle Scholar
Hammond, P. & Pomfrett, C.J. (1990). Directionality of cat striate cortical neurones: contribution of suppression. Experimental Brain Research 81, 417425.CrossRefGoogle Scholar
Jacobson, L.D., Gaska, J.P., Chen, H.W., & Pollen, D.A. (1993). Structural testing of multi-input linear-nonlinear cascade models for cells in macaque striate cortex. Vision Research 33, 609626.CrossRefGoogle Scholar
Julesz, B. (1971). Foundations of Cyclopean Perception. Chicago, Illinois: University of Chicago Press.
Krüger, K., Kiefer, W., & Groh, A. (1993b). Lesion of the suprasylvian cortex impairs depth perception of cats. Neuroreport 4, 883886.Google Scholar
Li, B., Chen, Y., Li, B.W., Wang, L.H., & Diao, Y.C. (2001). Pattern and component motion selectivity in cortical area PMLS of the cat. European Journal of Neuroscience 14, 690700.CrossRefGoogle Scholar
Li, B., Li, B.W., Chen, Y., Wang, L.H., & Diao, Y.C. (2000). Response properties of PMLS and PLLS neurons to simulated optic flow patterns. European Journal of Neuroscience 12, 15341544.CrossRefGoogle Scholar
Lomber, S.G. (2001). Behavioral cartography of visual functions in cat parietal cortex: areal and laminar dissociations. Progress in Brain Research 134, 265284.CrossRefGoogle Scholar
Lomber, S.G., Payne, B.R., Cornwell, P., & Long, K.D. (1996a). Perceptual and cognitive visual functions of parietal and temporal cortices in the cat. Cerebral Cortex 6, 673695.Google Scholar
Lomber, S.G., Payne, B.R., & Cornwell, P. (1996b). Learning and recall of form discriminations during reversible cooling deactivation of ventral-posterior suprasylvian cortex in the cat. Proceedings of the National Academy of Sciences of the U.S.A. 93, 16541658.Google Scholar
Merabet, L., Minville, K., Ptito, M., & Casanova, C. (2000). Responses of neurons in the cat posteromedial lateral suprasylvian cortex to moving texture patterns. Neuroscience 97, 611623.CrossRefGoogle Scholar
Molenaar, J. & Van de Grind, W.A. (1980). A stereotaxic method of recording from single neurons in the intact in vivo eye of the cat. Journal of Neuroscience Methods 2, 135152.CrossRefGoogle Scholar
Orban, G.A. (1984). Neuronal Operations in the Visual Cortex: Studies of Brain Function. Berlin: Springer.CrossRef
Pasternak, T., Horn, K.M., & Maunsell, J.H. (1989). Deficits in speed discrimination following lesions of the lateral suprasylvian cortex in the cat. Visual Neuroscience 3, 365375.CrossRefGoogle Scholar
Perge, J.A., Borghuis, B.G., Bours, R.J., Lankheet, M.J.M., & Van Wezel., R.J.A. (2005). Temporal dynamics of direction tuning in motion-sensitive macaque area MT. Journal of Neurophysiology 93, 21042116.Google Scholar
Priebe, N.J, Churchland, M.M., & Lisberger, S.G. (2002). Constraints on the source of short-term motion adaptation in macaque area MT. I. the role of input and intrinsic mechanisms. Journal of Neurophysiology 88, 354369.Google Scholar
Rauschecker, J.P., von Grünau, M.W., & Poulin, C. (1987). Centrifugal organization of direction preferences in the cat's lateral suprasylvian visual cortex and its relation to flow field processing. Journal of Neuroscience 7, 943958.Google Scholar
Reinoso-Suarez, F. (1961). Topografischer Hirnatlas der Katze fuer experimentalphysiologische untersuchung. Darmstadt, Germany: E. Marck AG.
Spear, P.D. & Baumann, T.P. (1975). Receptive-field characteristics of single neurons in lateral suprasylvian visual area of the cat. Journal of Neurophysiology 38, 14031420.Google Scholar
Spear, P.D. (1991). Functions of extrastriate visual cortex in non-primate species. In The Neural Basis of Visual Dysfunction, ed. Leventhal, A.G., pp. 339370. London, UK: Macmillan Press.
Takada, R., Hara, N., Yamamoto, K., Toda, H., Ando, T., Hasebe, H., Abe, H., & Bando, T. (2000). Effects of localized lesions in the lateral suprasylvian cortex on convergence eye movement in cats. Neuroscience Research 36, 275283.CrossRefGoogle Scholar
Takagi, M., Toda, H., Yoshizawa, T., Hara, N., Ando, T., Abe, H., & Bando, T. (1992). Ocular convergence-related neuronal responses in the lateral suprasylvian area of alert cats. Neuroscience Research 15, 229234.CrossRefGoogle Scholar
Toda, H., Yoshizawa, T., Takagi, M., & Bando, T. (2001). The properties of convergence eye movements evoked from the rostral and caudal lateral suprasylvian cortex in the cat. Neuroscience Research 39, 359367.CrossRefGoogle Scholar
Touryan, J., Lau, B., & Dan, Y. (2002). Isolation of relevant visual features from random stimuli for cortical complex cells. Journal of Neuroscience 22, 1081110818.Google Scholar
Toyama, K., Kitaoji, H., & Umetani, K. (1991). Binocular neuronal responsiveness in Clare-Bishop cortex of Siamese cats. Experimental Brain Research 86, 471482.Google Scholar
Toyama, K., Komatsu, Y., Kasai, H., Fujii, K., & Umetani, K. (1985). Responsiveness of Clare-Bishop neurons to visual cues associated with motion of a visual stimulus in three-dimensional space. Vision Research 25, 407414.CrossRefGoogle Scholar
Vajda, I., Lankheet, M.J.M., Borghuis, B.G., & Van de Grind, W.A. (2004). Dynamics of directional selectivity in area 18 and PMLS of the cat. Cerebral Cortex 14, 759767.CrossRefGoogle Scholar
Vajda, I., Lankheet, M.J.M., & Van de Grind, W.A. (2005). Spatio-temporal requirements for direction selectivity in area 18 and PMLS complex cells. Vision Research 45, 17691779.CrossRefGoogle Scholar
Von Grünau, M.W. & Frost, B.J. (1983). Double-opponent-process mechanism underlying RF-structure of directionally specific cells of cat lateral suprasylvian visual area. Experimental Brain Research 49, 8492.CrossRefGoogle Scholar
Von Grünau, M.W., Zumbroich, T.J., & Poulin, C. (1987). Visual receptive field properties in the posterior suprasylvian cortex of the cat: A comparison between the areas PMLS and PLLS. Vision Research 27, 343356.CrossRefGoogle Scholar
Yin, T.C. & Greenwood, M. (1992). Visuomotor interactions in responses of neurons in the middle and lateral suprasylvian cortices of the behaving cat. Experimental Brain Research 88, 1532.CrossRefGoogle Scholar
Zernicki, B. & Stasiak, M. (1994). The contralateral impairment of the orienting ocular-following reflex after lesions of the lateral suprasylvian cortex in cats. Acta Neurobiologica Experimenta (Warsz) 54, 405409.Google Scholar