Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-18T19:17:37.415Z Has data issue: false hasContentIssue false

Temporal properties of surround suppression in cat primary visual cortex

Published online by Cambridge University Press:  09 August 2007

SÉVERINE DURAND
Affiliation:
Institute of Neuroinformatics, University of Zurich and Swiss Federal Institute of Technology, Zurich, Switzerland
TOBE C.B. FREEMAN
Affiliation:
Institute of Neuroinformatics, University of Zurich and Swiss Federal Institute of Technology, Zurich, Switzerland Current address: Genedata AG, Maulbeerstrasse 46, CH-4016 Basel, Switzerland
MATTEO CARANDINI
Affiliation:
Institute of Neuroinformatics, University of Zurich and Swiss Federal Institute of Technology, Zurich, Switzerland Current address: Smith-Kettlewell Eye Research Institute, 2318 Fillmore Street, San Francisco, CA 94115.

Abstract

The responses of neurons in primary visual cortex (V1) are suppressed by stimuli presented in the region surrounding the receptive field. There is debate as to whether this surround suppression is due to intracortical inhibition, is inherited from lateral geniculate nucleus (LGN), or is due to a combination of these factors. The mechanisms involved in surround suppression may differ from those involved in suppression within the receptive field, which is called cross-orientation suppression. To compare surround suppression to cross-orientation suppression, and to help elucidate its underlying mechanisms, we studied its temporal properties in anesthetized and paralyzed cats. We first measured the temporal resolution of suppression. While cat LGN neurons respond vigorously to drift rates up to 30 Hz, most cat V1 neurons stop responding above 10–15 Hz. If suppression originated in cortical responses, therefore, it should disappear above such drift rates. In a majority of cells, surround suppression decreased substantially when surround drift rate was above ∼15 Hz, but some neurons demonstrated suppression with surround drift rates as high as 21 Hz. We then measured the susceptibility of suppression to contrast adaptation. Contrast adaptation reduces responses of cortical neurons much more than those of LGN neurons. If suppression originated in cortical responses, therefore, it should be reduced by adaptation. Consistent with this hypothesis, we found that prolonged exposure to the surround stimulus decreased the strength of surround suppression. The results of both experiments differ markedly from those previously obtained in a study of cross-orientation suppression, whose temporal properties were found to resemble those of LGN neurons. Our results provide further evidence that these two forms of suppression are due to different mechanisms. Surround suppression can be explained by a mixture of thalamic and cortical influences. It could also arise entirely from intracortical inhibition, but only if inhibitory neurons respond to somewhat higher drift rates than most cortical cells.

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

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 (London) 347, 713739.Google Scholar
Albrecht, D.G. & Hamilton, D.B. (1982). Striate cortex of monkey and cat: Contrast response function. Journal of Neurophysiology 48, 217237.Google Scholar
Allison, J.D., Smith, K.R. & Bonds, A.B. (2001). Temporal-frequency tuning of cross-orientation suppression in the cat striate cortex. Visual Neuroscience 18, 941948.Google Scholar
Angelucci, A. & Bressloff, P.C. (2006). Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons. Progress in Brain Research 154, 93120.Google Scholar
Angelucci, A. & Bullier, J. (2003). Reaching beyond the classical receptive field of V1 neurons: Horizontal or feedback axons? Journal of Physiology (Paris) 97, 141154.Google Scholar
Angelucci, A., Levitt, J.B., Walton, E.J., Hupe, J.M., Bullier, J. & Lund, J.S. (2002). Circuits for local and global signal integration in primary visual cortex. Journal of Neuroscience 22, 86338646.Google Scholar
Azouz, R., Gray, C.M., Nowak, L.G. & McCormick, D.A. (1997). Physiological properties of inhibitory interneurons in cat striate cortex. Cerebral Cortex 7, 534545.Google Scholar
Bair, W., Cavanaugh, J.R. & Movshon, J.A. (2003). Time course and time-distance relationships for surround suppression in macaque V1 neurons. Journal of Neuroscience 23, 76907701.Google Scholar
Blakemore, C. & Tobin, E.A. (1972). Lateral inhibition between orientation detectors in the cat's visual cortex. Experimental Brain Research 15, 439440.Google Scholar
Bonds, A.B. (1989). Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Visual Neuroscience 2, 4155.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
Brainard, D.H. (1997). The Psychophysics Toolbox. Spatial Vision 10, 433436.Google Scholar
Carandini, M. (2004). Receptive fields and suppressive fields in the early visual system. In The Cognitive Neurosciences III, ed. Gazzaniga, M.S., pp. 313326. Cambridge, MA: MIT Press.
Carandini, M. & Ferster, D. (1997). A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276, 949952.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
Carandini, M., Heeger, D.J. & Senn, W. (2002). A synaptic explanation of suppression in visual cortex. Journal of Neuroscience 22, 1005310065.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
Chen, C.C., Kasamatsu, T., Polat, U. & Norcia, A.M. (2001). Contrast response characteristics of long-range lateral interactions in cat striate cortex. Neuroreport 12, 655661.Google Scholar
DeAngelis, G.C., Anzai, A., Ohzawa, I. & Freeman, R.D. (1995). Receptive field structure in the visual cortex: Does selective stimulation induce plasticity? Proceedings of the National Academy of Sciences 92, 96829686.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). The organization of suppression in receptive fields of neurons in cat visual cortex. Journal of Neurophysiology 68, 144163.Google Scholar
Durand, S., Freeman, T.C.B., Mante, V., Kiper, D. & Carandini, M. (2001). Cross-orientation suppression in cat V1 with very fast stimuli. Society for Neuroscience Abstracts Vol. 27, Program No. 12.10.Google Scholar
Durand, S., Mante, V., Freeman, T.C.B. & Carandini, M. (2002). Temporal properties of surround suppression in primary visual cortex. European Journal of Neuroscience, Abstract # 051.6.Google Scholar
Efron, B. & Tibshirani, R.J. (1993). An introduction to the Bootstrap, vol. 57. New York: Chapman & Hall.
Fitzpatrick, D. (2000). Seeing beyond the receptive field in primary visual cortex. Current Opinion in Neurobiology 10, 438443.Google Scholar
Freeman, T.C., Durand, S., Kiper, D.C. & Carandini, M. (2002). Suppression without inhibition in visual cortex. Neuron 35, 759771.Google Scholar
Gegenfurtner, K.R., Kiper, D.C. & Levitt, J.B. (1997). Functional properties of neurons in macaque area V3. Journal of Neurophysiology 77, 19061923.Google Scholar
Heeger, D.J. (1992). Normalization of cell responses in cat striate cortex. Visual Neuroscience 9, 181197.Google Scholar
Hubel, D. & Wiesel, T. (1965). Receptive field and functional architecture in two nonstriate visual areas (18–19) of the cat. Journal of Neurophysiology 28, 229289.Google Scholar
Ikeda, H. & Wright, M.J. (1975). Spatial and temporal properties of ‘sustained’ and ‘transient’ neurones in area 17 of the cat's visual cortex. Experimental Brain Research 22, 363383.Google Scholar
Jagadeesh, B. & Ferster, D. (1990). Receptive field lengths in cat striate cortex can increase with decreasing stimulus contrast. Society for Neuroscience Abstracts 16, 293.Google Scholar
Jones, H.E., Andolina, I.M., Oakely, N.M., Murphy, P.C. & Sillito, A.M. (2000). Spatial summation in lateral geniculate nucleus and visual cortex. Experimental Brain Research 135, 279284.Google Scholar
Kapadia, M.K., Westheimer, G. & Gilbert, C.D. (1999). Dynamics of spatial summation in primary visual cortex of alert monkeys. Proceedings of the National Academy of Sciences 96, 1207312078.Google Scholar
Lehmkuhle, S., Kratz, K.E., Mangel, S.C. & Sherman, S.M. (1980). Spatial and temporal sensitivity of X- and Y-cells in dorsal lateral geniculate nucleus of the cat. Journal of Neurophysiology 43, 520541.Google Scholar
Levitt, J.B. & Lund, J.S. (2002). The spatial extent over which neurons in macaque striate cortex pool visual signals. Visual Neuroscience 19, 439452.Google Scholar
Li, B., Peterson, M.R., Thompson, J.K., Duong, T. & Freeman, R.D. (2005). Cross-orientation suppression: Monoptic and dichoptic mechanisms are different. Journal of Neurophysiology 94, 16451650.Google Scholar
Li, B., Thompson, J.K., Duong, T., Peterson, M.R. & Freeman, R.D. (2006). Origins of cross-orientation suppression in the visual cortex. Journal of Neurophysiology 96, 17551764.Google Scholar
Li, C. & Li, W. (1994). Extensive integration beyond the classical receptive field of cat's striate cortical neurons—classification and tuning properties. Vision Research 34, 23372356.Google Scholar
Maffei, L. & Fiorentini, A. (1976). The unresponsive regions of visual cortical receptive fields. Vision Research 13, 12551267.Google Scholar
Maffei, L., Fiorentini, A. & Bisti, S. (1973). Neural correlate of perceptual adaptation to gratings. Science 182, 10361038.Google Scholar
Morrone, M.C., Burr, D.C. & Maffei, L. (1982). Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence. Proceedings of the Royal Society of London, Series B 216, 335354.Google Scholar
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978). Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. Journal of Physiology (London) 283, 101120.Google Scholar
Newsome, W.T., Gizzi, M.S. & & Movshon, J.A. (1983). Spatial and temporal properties of neurons in macaque MT. Investigative Ophthalmology & Visual Science Supplement 24, 106.Google Scholar
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat visual system. Journal of Neurophysiology 54, 651665.Google Scholar
Orban, G.A., Hoffman, 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, 10261049.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, 14281438.Google Scholar
Palmer, L.A. & Contreras, D. (2001). Differential contrast sensitivity of excitatory and inhibitory neurons in cat area 17. Society for Neuroscience Abstracts 27, Program No.821.61.Google Scholar
Pelli, D.G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision 10, 437442.Google Scholar
Petrov, Y., Carandini, M. & McKee, S. (2005). Two distinct mechanisms of suppression in human vision. Journal of Neuroscience 25, 87048707.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 89, 83668370.Google Scholar
Priebe, N.J. & Ferster, D. (2006). Mechanisms underlying cross-orientation suppression in cat visual cortex. Nature Neuroscience 9, 552561.Google Scholar
Sanchez-Vives, M.V., Nowak, L.G. & McCormick, D.A. (2000). Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. Journal of Neuroscience 20, 42674285.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, 206224.Google Scholar
Saul, A.B. & Humphrey, A.L. (1992). Temporal-frequency tuning of direction selectivity in cat visual cortex. Visual Neuroscience 8, 365372.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., Baddeley, R.J., Freeman, T.C., Harrad, R. & Blakemore, C. (1998). Different mechanisms underlie three inhibitory phenomena in cat area 17. Vision Research 38, 20672080.Google Scholar
Sengpiel, F., Sen, A. & Blakemore, C. (1997). Characteristics of surround inhibition in cat area 17. Experimental Brain Research 116, 216228.Google Scholar
Sengpiel, F. & Vorobyov, V. (2005). Intracortical origins of interocular suppression in the visual cortex. Journal of Neuroscience 25, 63946400.Google Scholar
Shou, T., Li, X., Zhou, Y. & Hu, B. (1996). Adaptation of visually evoked responses of relay cells in the dorsal lateral geniculate nucleus of the cat following prolonged exposure to drifting gratings. Visual Neuroscience 13, 605613.Google Scholar
Simons, D. (1978). Response properties of vibrissa units in rat SI somatosensory neocortex. Journal of Neurophysiology 41, 798820.Google Scholar
Sincich, L.C., Park, K.F., Wohlgemuth, M.J. & Horton, J.C. (2004). Bypassing V1: A direct geniculate input to area MT. Nature Neuroscience 7, 11231128.Google Scholar
Skottun, B.C., De Valois, 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, 10791086.Google Scholar
Smith, M.A., Bair, W. & Movshon, J.A. (2006). Dynamics of suppression in macaque primary visual cortex. Journal of Neuroscience 26, 48264834.Google Scholar
Solomon, S.G., Peirce, J.W., Dhruv, N.T. & Lennie, P. (2004). Profound contrast adaptation early in the visual pathway. Neuron 42, 155162.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
Swadlow, H. (1988). Efferent neurons and suspected interneurons in binocular visual cortex of the awake rabbit: Receptive fields and binocular properties. Journal of Neurophysiology 59, 11621187.Google Scholar
Swadlow, H. (1989). Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: Receptive fields and axonal properties. Journal of Neurophysiology 62(1), 288308.Google Scholar
Walker, G.A., Ohzawa, I. & Freeman, R.D. (1999). Asymmetric suppression outside the classical receptive field of the visual cortex. Journal of Neuroscience 19, 1053610553.Google Scholar
Webb, B.S., Dhruv, N.T., Solomon, S.G., Tailby, C. & Lennie, P. (2005a). 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., Vincent, C.J. & Derrington, A.M. (2005b). Spatial distribution of suppressive signals outside the classical receptive field in lateral geniculate nucleus. Journal of Neurophysiology 94, 17891797.Google Scholar