Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-28T12:46:26.176Z Has data issue: false hasContentIssue false
  • English
  • Français

The direction-selective contrast response of area 18 neurons is different for first- and second-order motion

Published online by Cambridge University Press:  05 April 2005

TIMOTHY LEDGEWAY ,
CHANG'AN ZHAN ,
AARON P. JOHNSON ,
YUNING SONG  and
CURTIS L. BAKER
TIMOTHY LEDGEWAY
Affiliation:
McGill Vision Research, Department of Ophthalmology, McGill University, Montreal, Quebec, Canada
CHANG'AN ZHAN
Affiliation:
McGill Vision Research, Department of Ophthalmology, McGill University, Montreal, Quebec, Canada
AARON P. JOHNSON
Affiliation:
McGill Vision Research, Department of Ophthalmology, McGill University, Montreal, Quebec, Canada
YUNING SONG
Affiliation:
McGill Vision Research, Department of Ophthalmology, McGill University, Montreal, Quebec, Canada
CURTIS L. BAKER
Affiliation:
McGill Vision Research, Department of Ophthalmology, McGill University, Montreal, Quebec, Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

Cortical neurons selective for the direction of motion often exhibit some limited response to motion in their nonpreferred directions. Here we examine the dependence of neuronal direction selectivity on stimulus contrast, both for first-order (luminance-modulated, sine-wave grating) and second-order (contrast-modulated envelope) stimuli. We measured responses from single neurons in area 18 of cat visual cortex to both kinds of moving stimuli over a wide range of contrasts (1.25–80%). Direction-selective contrast response functions (CRFs) were calculated as the preferred-minus-null difference in average firing frequency as a function of contrast. We also applied receiver operating characteristic analysis to our CRF data to obtain neurometric functions characterizing the potential ability of each neuron to discriminate motion direction at each contrast level tested. CRFs for sine-wave gratings were usually monotonic; however, a substantial minority of neurons (35%) exhibited nonmonotonic CRFs (such that the degree of direction selectivity decreased with increasing contrast). The underlying preferred and nonpreferred direction CRFs were diverse, often having different shapes in a given neuron. Neurometric functions for direction discrimination showed a similar degree of heterogeneity, including instances of nonmonotonicity. For contrast-modulated stimuli, however, CRFs for either carrier or envelope contrast were always monotonic. In a given neuron, neurometric thresholds were typically much higher for second- than for first-order stimuli. These results demonstrate that the degree of a cell's direction selectivity depends on the contrast at which it is measured, and therefore is not a characteristic parameter of a neuron. In general, contrast response functions for first-order stimuli were very heterogeneous in shape and sensitivity, while those for second-order stimuli showed less sensitivity and were quite stereotyped in shape.

Keywords

Visual cortexDirection selectivityContrast response functionFirst-order motionSecond-order motion
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 1 , January 2005 , pp. 87 - 99
Copyright
© 2005 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

Albrecht, D.H. (1995). Visual cortex neurons in monkey and cat: Effect of contrast on the spatial and temporal phase transfer functions. Visual Neuroscience 12, 1191–1210.CrossRefGoogle Scholar
Albrecht, D.H. & Geisler, W.S. (1991). Motion selectivity and the contrast response function of simple cells in the visual cortex. Visual Neuroscience 7, 531–546.CrossRefGoogle Scholar
Albrecht, D.H. & Hamilton, D.B. (1982). Striate cortex of monkey and cat: Contrast response function. Journal of Neurophysiology 48, 217–237.Google Scholar
Baddeley, R., Abbot, L.F., Booth, M.C., Sengpiel, F., Freeman, T., Wakeman, E.A., & Rolls, E.T. (1998). Responses of neurons in primary and inferior temporal visual cortices to natural scenes. Proceedings of the Royal Society B (London) 264, 1775–1783.Google Scholar
Baker, C.L., Jr. (1999). Central neural mechanisms for detecting second-order motion. Current Opinion in Neurobiology 9, 461–466.CrossRefGoogle Scholar
Barlow, H.B., (2001). Redundancy reduction revisited. Network 12, 241–253.CrossRefGoogle Scholar
Barlow, H.B., Levick, W.R., & Yoon, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Research 11, 87–101.CrossRefGoogle Scholar
Bonds, A.B. (1991). Temporal dynamics of contrast gain in single cells of the cat striate cortex. Visual Neuroscience 6, 239–255.CrossRefGoogle Scholar
Bonds, A.B. (1993). The encoding of cortical contrast gain control. In Contrast Sensitivity, ed. Shapley, S. & Lam, D.M.-K., pp. 215–230. Cambridge, Massachusetts: MIT Press.
Brainard, D.H. (1997). The psychophysics toolbox. Spatial Vision 10, 433–436.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, 4745–4865.Google Scholar
Brugge, J.F. & Merzenich, M.M. (1973). Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. Journal of Neurophysiology 36, 1138–1158.Google Scholar
Carandini, M. & Heeger, D. (1994). Summation and division by neurons in primate visual cortex. Science 264, 1333–1336.CrossRefGoogle Scholar
Cavanagh, P. & Mather, G. (1989). Motion: The long and short of it. Spatial Vision 4, 103–129.CrossRefGoogle Scholar
Chaudhuri, A. & Albright, T.D. (1997). A comparison of neuronal responses to edges defined by luminance or temporal texture in macaque area V1. Visual Neuroscience 14, 949–962.CrossRefGoogle Scholar
Chubb, C. & Sperling, G. (1988). Drift-balanced random stimuli: A general basis for studying non-Fourier motion perception. Journal of the Optical Society of America A 5, 1986–2007.CrossRefGoogle Scholar
Cleary, R. (1990). Contrast dependence of short-range apparent motion. Vision Research 30, 463–478.CrossRefGoogle Scholar
Cooper, G.F. & Robson, J.G. (1968). Successive transformations of visual information in the visual system. In Pattern Recognition, IEEE N.P.L Conference publication, No. 42. London: IEEE.
Dean, A.F. (1980). The contrast-dependence of direction selectivity. Journal of Physiology (London) 303, 38–39.Google Scholar
Dean, A.F. (1981). The relationship between response amplitude and contrast for cat striate cortical neurons. Journal of Physiology 318, 413–427.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. II. Linearity of temporal and spatial summation. Journal of Neurophysiology 69, 1118–1135.Google Scholar
Derrington, A.M. & Goddard, P.A. (1989). Failure of motion discrimination at high contrasts: Evidence for saturation. Vision Research 29, 1767–1776.CrossRefGoogle Scholar
Durgin, F.H. & Hammer, J.T. (2001). Visual aftereffects of sequential perception: Dynamic adaptation to changes in texture density and contrast. Vision Research 41, 2607–2617.CrossRefGoogle Scholar
Foster, K.H., Gaska, J.P., Nagler, M., & Pollen, D.A. (1985). Spatial and temporal frequency selectivity of neurones in visual cortical areas V1 and V2 of the macaque monkey. Journal of Physiology (London) 365, 331–363.CrossRefGoogle Scholar
Geisler, W.S. & Albrecht, D.G. (1992). Cortical neurons: Isolation of contrast gain control. Vision Research 32, 1409–1410.CrossRefGoogle Scholar
Geisler, W.S. & Albrecht, D.G. (1995). Bayesian analysis of identification performance in monkey visual cortex: Nonlinear mechanisms and stimulus certainty. Vision Research 35, 2723–2730.CrossRefGoogle Scholar
Graham, N. & Sutter, A. (1998). Spatial summation in simple (Fourier) and complex (non-Fourier) channels in texture segregation. Vision Research 38, 231–257.CrossRefGoogle Scholar
Heeger, D.J. (1992a). Half-squaring in responses of cat striate cells. Visual Neuroscience 9, 427–443.Google Scholar
Heeger, D.J. (1992b). Normalization of cell responses in cat striate cortex. Visual Neuroscience 9, 181–197.Google Scholar
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.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology (London) 195, 215–243.CrossRefGoogle Scholar
Humphrey, A.L. & Saul, A.B. (2002). The emergence of direction selectivity in cat primary visual cortex. In The Cat Primary Visual Cortex, ed. Payne, B.R. & Peters, A., pp. 343–386. San Diego, California: Academic Press.CrossRef
Landy, M.S. & Graham, N. (2004). Visual perception of texture. In The Visual Neurosciences, ed. Chalupa, L.M. & Werner, J.S., pp. 1106–1118. Cambridge, Massachusetts: MIT Press.
Laughlin, S.B. (1981). A simple coding procedure enhances a neuron's information capacity. Zeitschrift fur Naturforschung C 36, 910–912.Google Scholar
Ledgeway, T. & Baker, C.L., Jr. (2001). A neurometric function analysis of the direction selectivity of visual cortex neurons as a function of stimulus contrast. Society for Neuroscience Abstracts 27, 164.3.Google Scholar
Ledgeway, T., Zhan, C., Johnson, A., Song, Y., & Baker, C.L., Jr. (2004). Direction selectivity and the contrast response function of cortical neurones to first-order and second-order motion. Perception (Supplement) 33, 159–160.Google Scholar
Leventhal, A.G., Wang, Y., Schmolesky, M.T., & Zhou, Y. (1998). Neural correlates of boundary perception. Visual Neuroscience 15, 1107–1118.CrossRefGoogle Scholar
Li, C.-Y. & Creutzfeldt, O. (1984). The representation of contrast and other stimulus parameters by single neurons in area 17 of the cat. Pflugers Archives 401, 304–314.Google Scholar
Mareschal, I. & Baker, C.L., Jr. (1998). Temporal and spatial response to second-order stimuli in cat area 18. Journal of Neurophysiology 80, 2811–2823.Google Scholar
Mareschal, I. & Baker, C.L. (1999). Cortical processing of second-order motion. Visual Neuroscience 16, 527–540.CrossRefGoogle Scholar
Movshon, J.A. & Tolhurst, D. (1975). On the response linearity of cells in the cat visual cortex. Journal of Physiology 249, 56–57.Google Scholar
O'Keefe, L.P. & Movshon, J.A. (1998). Processing of first- and second-order motion signals by neurons in area MT of the macaque monkey. Visual Neuroscience 15, 305–317.Google Scholar
Olshausen, B.A. & Field, D.J. (2004). Sparse coding of sensory inputs. Current Opinion in Neurobiology 14, 1–7.CrossRefGoogle Scholar
Parker, A.J. & Newsome, W.T. (1998). Sense and the single neuron: Probing the physiology of perception. Annual Review of Neuroscience 21, 227–277.CrossRefGoogle Scholar
Pelli, D.G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision 10, 437–442.CrossRefGoogle Scholar
Peterson, M.R. & Freeman, R.D. (2003). Direction selectivity of neurons in striate cortex changes with stimulus contrast. Abstract Viewer/Itinerary Planner, Program No. 484.17. Washington, DC: Society for Neuroscience. Online.
Phillips, D.P., Semple, M.N., Calford, M.B., & Kitzes, L.M. (1994). Level-dependent representation of stimulus frequency in cat primary auditory cortex. Experimental Brain Research 102, 210–226.Google Scholar
Robson, J.G. (1975). Receptive fields: Spatial and intensive representation of the visual image. In Handbook of Perception, Vol. 5: Vision, ed. Carterette, E.C. & Friedman, M.P., pp. 81–112. New York: Springer-Verlag.
Sachs, A.J. & Baker, C.L., Jr. (2003). Irregular firing patterns of visual cortex neurons behave like a Markov-modulated Poisson process. Journal of Computational Neuroscience (submitted).Google Scholar
Sclar, G., Maunsell, J.H.R., & Lennie, P. (1990). Coding of image contrast in central visual pathways of macaque monkey. Vision Research 30, 1–10.Google Scholar
Simoncelli, E.P. (2003). Vision and the statistics of the natural environment. Current Opinion in Neurobiology 13, 144–149.CrossRefGoogle Scholar
Skottun, B.C., Bradley, A., Sclar, G., Ohzawa, I., & Freeman, R.D. (1987). The effects of contrast on visual orientation and spatial frequency discrimination: A comparison of single cells and behaviour. Journal of Neurophysiology 57, 773–786.Google Scholar
Skottun, B.C., DeValois, R.L., Grosof, D.H., Movshon, J.A., Albrecht, D.G., & Bonds, A.B. (1991). Classifying simple and complex cells on the basis of response modulation. Vision Research 31, 1079–1086.Google Scholar
Somers, D., Dragoi, V., & Sur, M. (2002). Orientation selectivity and its modulation by local and long-range connections in visual cortex. In The cat primary visual cortex, ed. Payne, B.R. & Peters, A., pp. 471–520. San Diego, California: Academic Press.CrossRef
Song, Y. & Baker, C.L., Jr. (2003). Distinct linear and nonlinear mechanisms for illusory contour responses in visual cortex neurones. Abstract Viewer/Itinerary Planner, Program No. 910.10. Washington, DC: Society for Neuroscience. Online.
Tolhurst, D.J., Movshon, J.A., & Dean, A.F. (1983). The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Research 23, 775–785.CrossRefGoogle Scholar
Weibull, W.A. (1951). A statistical distribution function of wide applicability. Journal of Applied Mechanics, 21, 292–277.Google Scholar
Zhan, C., Ledgeway, T., & Baker, C.L., Jr. (2002). Optical imaging of contrast-dependent direction selectivity in visual cortex. Abstract Viewer/Itinerary Planner, Program No. 657.4. Washington, DC: Society for Neuroscience. Online.
Zhan, C. & Baker, C.L., Jr. (2003). Optical imaging of form-cue invariant orientation domains for illusory contours and contrast envelopes in visual cortex. Abstract Viewer/Itinerary Planner, program No. 910.8. Washington, DC: Society for Neuroscience. Online.
Zhou, Y.-X. & Baker, C.L., Jr. (1993). A processing stream in mammalian visual cortex neurons for non-Fourier responses. Science 261, 98–101.CrossRefGoogle Scholar
Zhou, Y.-X. & Baker, C.L., Jr. (1994). Envelope-responsive neurones in areas 17 and 18 of cat. Journal of Neurophysiology 72, 2134–2150.Google Scholar