Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-28T12:49:49.066Z Has data issue: false hasContentIssue false

Two expressions of “surround suppression” in V1 that arise independent of cortical mechanisms of suppression

Published online by Cambridge University Press:  12 April 2007

CHRIS TAILBY
Affiliation:
Center for Neural Science, New York University, New York, New York
SAMUEL G. SOLOMON
Affiliation:
Department of Physiology, The University of Sydney, New South Wales, Australia
JONATHAN W. PEIRCE
Affiliation:
School of Psychology, University of Nottingham, University Park, Nottingham UK
ANDREW B. METHA
Affiliation:
Department of Optometry and Vision Sciences, The University of Melbourne, Carlton, Australia

Abstract

The preferred stimulus size of a V1 neuron decreases with increases in stimulus contrast. It has been supposed that stimulus contrast is the primary determinant of such spatial summation in V1 cells, though the extent to which it depends on other stimulus attributes such as orientation and spatial frequency remains untested. We investigated this by recording from single cells in V1 of anaesthetized cats and monkeys, measuring size-tuning curves for high-contrast drifting gratings of optimal spatial configuration, and comparing these curves with those obtained at lower contrast or at sub-optimal orientations or spatial frequencies. For drifting gratings of optimal spatial configuration, lower contrasts produced less surround suppression resulting in increases in preferred size. High contrast gratings of sub-optimal spatial configuration produced more surround suppression than optimal low-contrast gratings, and as much or more surround suppression than optimal high-contrast gratings. For sub-optimal spatial frequencies, preferred size was similar to that for the optimal high-contrast stimulus, whereas for sub-optimal orientations, preferred size was smaller than that for the optimal high-contrast stimulus. These results indicate that, while contrast is an important determinant of spatial summation in V1, it is not the only determinant. Simulation of these experiments on a cortical receptive field modeled as a Gabor revealed that the small preferred sizes observed for non-preferred stimuli could result simply from linear filtering by the classical receptive field. Further simulations show that surround suppression in retinal ganglion cells and LGN cells can be propagated to neurons in V1, though certain properties of the surround seen in cortex indicate that it is not solely inherited from earlier stages of processing.

Type
Research Article
Copyright
© 2007 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

Blakemore, C. & Tobin, E.A. (1972). Lateral inhibition between orientation detectors in the cat's visual cortex. Experimental Brain Research 15, 439440.Google Scholar
Bonin, V., Mante, V. & Carandini, M. (2005). The suppressive field of neurons in lateral geniculate nucleus. Journal of Neuroscience 25, 1084410856.Google Scholar
Carandini, M., Heeger, D.J. & Movshon, J.A. (1997). Linearity and normalization in simple cells of the macaque primary visual cortex. Journal of Neuroscience 17, 86218644.Google Scholar
Cavanaugh, J.R., Bair, W. & Movshon, J.A. (2002a). Nature and interaction of signals from the receptive field center and surround in macaque v1 neurons. Journal of Neurophysiology 88, 25302546.Google Scholar
Cavanaugh, J.R., Bair, W. & Movshon, J.A. (2002b). Selectivity and spatial distribution of signals from the receptive field surround in macaque v1 neurons. Journal of Neurophysiology 88, 25472556.Google Scholar
Daugman, J.G. (1980). Two-dimensional spectral analysis of cortical receptive field profiles. Vision Research 20, 847856.Google Scholar
DeAngelis, G.C., Freeman, R.D. & Ohzawa, I. (1994). Length and width tuning of neurons in the cat's primary visual cortex. Journal of Neurophysiology 71, 347374.Google Scholar
DeAngelis, G.C., Robson, J.G., Ohzawa, I. & Freeman, R.D. (1992). Organization of suppression in receptive fields of neurons in cat visual cortex. Journal of Neurophysiology 68, 144163.Google Scholar
Einevoll, G.T. & Plesser, H.E. (2005). Response of the difference-of-Gaussians model to circular drifting-grating patches. Visual Neuroscience 22, 437446.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction, and functional architecture of the cat's visual cortex. Journal of Physiology (Lond) 160, 106154.Google Scholar
Ikeda, H. & Wright, M.J. (1974). Sensitivity of neurones in visual cortex (area 17) under different levels of anaesthesia. Experimental Brain Research 20, 471484.Google Scholar
Jones, J.P. & Palmer, L.A. (1987). An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 12331258.Google Scholar
Levitt, J.B. & Lund, J.S. (1997). Contrast dependence of contextual effects in primate visual cortex. Nature 387, 7376.Google Scholar
Maffei, L. & Fiorentini, A. (1976). The unresponsive regions of visual cortical receptive fields. Vision Research 16, 11311139.Google Scholar
Marcelja, S. (1980). Mathematical description of the responses of simple cortical cells. Journal of the Ophthalmic Society of America 70, 12971300.Google Scholar
Metha, A.B., Crane, A.M., Rylander, H.G., 3rd, Thomsen, S.L. & Albrecht, D.G. (2001). Maintaining the cornea and the general physiological environment in visual neurophysiology experiments. Journal of Neuroscience Methods 109, 153166.Google Scholar
Nolt, M.J., Kumbhani, R.D. & Palmer, L.A. (2004). Contrast-dependent spatial summation in the lateral geniculate nucleus and retina of the cat. Journal of Neurophysiology 92, 17081717.Google Scholar
Ozeki, H., Sadakane, O., Akasaki, T., Naito, T., Shimegi, S. & Sato, H. (2004). Relationship between excitation and inhibition underlying size tuning and contextual response modulation in the cat primary visual cortex. Journal of Neuroscience 24, 1428.Google Scholar
Rodieck, R.W. & Dreher, B. (1979). Visual suppression from nondominant eye in the lateral geniculate nucleus: a comparison of cat and monkey. Experimental Brain Research 35, 465477.Google Scholar
Sceniak, M.P., Hawken, M.J. & Shapley, R. (2001). Visual spatial characterization of macaque v1 neurons. Journal of Neurophysiology 85, 18731887.Google Scholar
Sceniak, M.P., Ringach, D.L., Hawken, M.J. & Shapley, R. (1999). Contrast's effect on spatial summation by macaque V1 neurons. Nature Neuroscience 2, 733739.Google Scholar
Sengpiel, F., Sen, A. & Blakemore, C. (1997). Characteristics of surround inhibition in cat area 17. Experimental Brain Research 116, 216228.Google Scholar
Sillito, A.M., Cudeiro, J. & Murphy, P.C. (1993). Orientation sensitive elements in the corticofugal influence on centre-surround interactions in the dorsal lateral geniculate nucleus. Experimental Brain Research 93, 616.Google 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 behavior. Journal of Neurophysiology 57, 773786.Google Scholar
Solomon, S.G., Lee, B.B. & Sun, H. (2006). Suppressive surrounds and contrast gain in magnocellular-pathway retinal ganglion cells of macaque. Journal of Neuroscience 26, 87158726.Google Scholar
Solomon, S.G., Peirce, J.W. & Lennie, P. (2004). The impact of suppressive surrounds on chromatic properties of cortical neurons. Journal of Neuroscience 24, 148160.Google Scholar
Solomon, S.G., White, A.J. & Martin, P.R. (2002). Extraclassical receptive field properties of parvocellular, magnocellular, and koniocellular cells in the primate lateral geniculate nucleus. Journal of Neuroscience 22, 338349.Google Scholar
Walker, G.A., Ohzawa, I. & Freeman, R.D. (2000). Suppression outside the classical cortical receptive field. Visual Neuroscience 17, 369379.Google Scholar
Webb, B.S., Dhruv, N.T., Solomon, S.G., Tailby, C. & Lennie, P. (2005). Early and late mechanisms of surround suppression in striate cortex of macaque. Journal of Neuroscience 25, 1166611675.Google Scholar
Webb, B.S., Tinsley, C.J., Barraclough, N.E., Easton, A., Parker, A. & Derrington, A.M. (2002). Feedback from V1 and inhibition from beyond the classical receptive field modulates the responses of neurons in the primate lateral geniculate nucleus. Visual Neuroscience 19, 583592.Google Scholar
Wielaard, J. & Sajda, P. (2006). Extraclassical receptive field phenomena and short-range connectivity in V1. Cerebral Cortex 16, 15311545.Google Scholar