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Decorrelation of neural activity during fixational instability: Possible implications for the refinement of V1 receptive fields

Published online by Cambridge University Press:  01 September 2004

MICHELE RUCCI  and
ANTONINO CASILE
MICHELE RUCCI
Affiliation:
Department of Cognitive and Neural Systems, Boston University, Boston Massachusetts
ANTONINO CASILE
Affiliation:
Laboratory for Action Representation and Learning, Department of Cognitive Neurology, University Clinic, Tübingen, Germany
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Abstract

Early in life, visual experience appears to influence the refinement and maintenance of the orientation-selective responses of neurons in the primary visual cortex. After eye opening, the statistical structure of visually driven neural responses depends not only on the stimulus, but also on how the stimulus is scanned during behavior. Modulations of neural activity due to behavior may thus play a role in the experience-dependent refinement of cell response characteristics. To investigate the possible influences of eye movements on the maturation of thalamocortical connectivity, we have simulated the responses of neuronal populations in the lateral geniculate nucleus (LGN) and V1 of the cat while images of natural scenes were scanned in a way that replicated the cat's oculomotor activity. In the model, fixational eye movements were essential to attenuate neural sensitivity to the broad correlational structure of natural visual input, decorrelate neural responses, and establish a regime of neural activity that was compatible with a Hebbian segregation of geniculate afferents to the cortex. We show that this result is highly robust and does not depend on the precise characteristics of the model.

Keywords

Orientation selectivityStriate cortexMicrosaccadeOcular driftComputational model
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 5 , September 2004 , pp. 725 - 738
Copyright
2004 Cambridge University Press

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References

REFERENCES

Abbott, L.F., Varela, J.A., Sen, K., & Nelson, S.B. (1997). Synaptic depression and cortical gain control. Science 275, 220–224.Google Scholar
Albus, K. & Wolf, K. (1984). Early postnatal development of neuronal function in the kitten's visual cortex: A laminar analysis. Journal of Physiology 348, 153–185.Google Scholar
Atick, J.J. & Redlich, A.N. (1992). What does the retina knows about natural scenes. Neural Computation 4, 196–210.Google Scholar
Barlow, H.B. (1961). Possible principles underlying the transformation of sensory messages. In Sensory Communication, ed. Rosenblith, W.A., pp. 217–234. Cambridge, Massachusetts: MIT Press.
Bendat, J.S. & Piersol, A.G. (1986). Random Data: Analysis and Measurement Procedures. New York: John Wiley & Sons Inc.
Blakemore, C. & Van Sluyters, R.C. (1975). Innate and environmental factors in the development of the kitten's visual cortex. Journal of Physiology 248, 663–716.Google Scholar
Buisseret, P. (1995). Influence of extraocular muscle proprioception on vision. Physiological Reviews 75, 323–338.Google Scholar
Buisseret, P. & Gary-Bobo, E. (1979). Development of visual cortical orientation specificity after dark-rearing: Role of extraocular proprioception. Neuroscience Letters 13, 259–263.Google Scholar
Buisseret, P., Gary-Bobo, E., & Imbert, M. (1978). Ocular motility and recovery of orientational properties of visual cortical neurons in dark-reared kittens. Nature 272, 816–817.Google Scholar
Buisseret, P. & Imbert, M. (1976). Visual cortical cells: Their developmental properties in normal and dark-reared kittens. Journal of Physiology 255, 511–525.Google Scholar
Cai, D., DeAngelis, G.C., & Freeman, R.D. (1997). Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kitten. Journal of Neurophysiology 78, 1045–1061.Google Scholar
Chance, F.S., Nelson, S.B., & Abbott, L.F. (1998). Synaptic depression and the temporal response characteristics of V1 cells. Journal of Neuroscience 18, 4785–4799.Google Scholar
Changeux, J.P. & Danchin, A. (1976). Selective stabilization of developing synapses as a mechanism for the specification of neuronal networks. Nature 264, 705–712.Google Scholar
Chapman, B. & Stryker, M.P. (1993). Development of orientation selectivity in ferret visual cortex and effects of deprivation. Journal of Neuroscience 13, 5251–5262.Google Scholar
Chapman, B., Zahs, K.R., & Stryker, M.P. (1991). Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. Journal of Neuroscience 11, 1347–1358.Google Scholar
Chung, S. & Ferster, D. (1998). Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression. Neuron 20, 1177–1189.Google Scholar
Collewijn, H. & Van Der Mark, F. (1972). Ocular stability in variable feedback conditions in the rabbit. Vision Research 36, 47–57.Google Scholar
Crair, M.C., Gillespie, D.C., & Stryker, M.P. (1998). The role of visual experience in the development of columns in cat visual cortex. Science 279, 566–570.Google Scholar
Cynader, M., Berman, N., & Hein, A. (1973). Cats reared in stroboscopic illumination: Effects on receptive fields in visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 70, 1353–1354.Google Scholar
Cynader, M. & Chernenko, G. (1976). Abolition of direction selectivity in the visual cortex of the cat. Science 193, 504–505.Google Scholar
DeAngelis, G.C., Ohzawa, I., & Freeman, R.D. (1993a). Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. Journal of Neurophysiology 69, 1091–1117.Google Scholar
DeAngelis, G.C., Ohzawa, I., & Freeman, R.D. (1993b). 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
DeValois, R.L. & DeValois, K.K. (1990). Spatial Vision. New York: Oxford University Press.
Ditchburn, R. (1973). Eye Movements in Relation to Retinal Action. Oxford: Clarendon Press.
Ferster, D., Chung, S., & Wheat, H. (1996). Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249–252.Google Scholar
Field, D.J. (1987). Relations between the statistics of natural images and the response properties of cortical cells. Journal of the Optical Society of America A 4, 2379–2394.Google Scholar
Freeman, R.D. & Bonds, A.B. (1979). Cortical plasticity in monocularly deprived immobilized kittens depends on eye movement. Science 206, 1093–1095.Google Scholar
Fregnac, Y. & Imbert, M. (1978). Early development of visual cortical cells in normal and dark-reared kittens: Relationship between orientation selectivity and ocular dominance. Journal of Physiology 278, 27–44.Google Scholar
Fregnac, Y., Shulz, D., Thorpe, S., & Bienenstock, E. (1992). Cellular analogs of visual cortical epigenesis. I. Plasticity of orientation selectivity. Journal of Neuroscience 12, 1280–1300.Google Scholar
Gary-Bobo, E., Milleret, C., & Buisseret, P. (1986). Role of eye movements in developmental process of orientation selectivity in the kitten visual cortex. Vision Research 26, 557–567.Google Scholar
Greschner, M., Bongard, M., Rujan, P., & Ammermüller, J. (2002). Retina ganglion cell synchronization by fixational eye movements improves feature estimation. Nature 5, 341–347.Google Scholar
Gur, M., Beylin, A., & Snodderly, D.M. (1997). Response variability of neurons in primary visual cortex (V1) of alert monkeys. Journal of Neuroscience 17, 2914–2920.Google Scholar
Gur, M. & Snodderly, D.M. (1987). Studying striate cortex neurons in behaving monkeys: Benefits of image stabilization. Vision Research 27, 2081–2087.Google Scholar
Hirsch, H. & Spinelli, D. (1970). Visual experience modifies distribution of horizontally and vertically oriented receptive fields in cats. Science 168, 869–871.Google Scholar
Hirsch, H.V.B. (1985). The role of visual experience in the development of cat striate cortex. Cellular and Molecular Neurobiology 5, 103–121.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106–154.Google Scholar
Ikeda, H. & Wright, M.J. (1975). The relationship between the ‘sustained-transient’ and the ‘simple-complex’ classifications of neurones in area 17 of the cat. Journal of Physiology 244, 58P–59P.Google Scholar
Jones, J.P. & Palmer, L.A. (1987a). An evaluation of the two-dimensional gabor filter model of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1233–1258.Google Scholar
Jones, J.P. & Palmer, L.A. (1987b). The two-dimensional spatial structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1187–1211.Google Scholar
Lee, D. & Malpeli, J.G. (1998). Effect of saccades on the activity of neurons in the cat lateral geniculate nucleus. Journal of Neurophysiology 79, 922–936.Google Scholar
Leopold, D.A. & Logothetis, N.K. (1998). Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Experimental Brain Research 123, 341–345.Google Scholar
Linsenmeier, R.A., Frishman, L.J., Jakiela, H.G., & Enroth-Cugell, C. (1982). Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements. Vision Research 22, 1173–1183.Google Scholar
Linsker, R. (1986). From basic network principles to neural architecture: Emergence of orientation-selective cells. Proceedings of the National Academy of Sciences of the U.S.A. 83, 8390–8394.Google Scholar
Martinez-Conde, S., Macknik, S., & Hubel, D.H. (2000). Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys. Nature Neuroscience 3, 251–258.Google Scholar
Mastronarde, D.N. (1983). Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X and Y cells. Journal of Neurophysiology 49, 303–323.Google Scholar
Miller, K.D. (1994). A model of the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF- center inputs. Journal of Neuroscience 14, 409–441.Google Scholar
Miller, K.D., Erwin, E., & Kayser, A. (1999). Is the development of orientation selectivity instructed by activity? Journal of Neurobiology 41, 44–57.Google Scholar
Miyashita, M. & Tanaka, S. (1992). A mathematical model for the self-organization of orientation columns in visual cortex. Neuroreport 3, 69–72.Google Scholar
Müller, J.R., Metha, A.B., Krauskopf, J., & Lennie, P. (1999). Rapid adaptation in visual cortex to the structure of images. Science 285, 1405–1408.Google Scholar
Okatan, M. & Grossberg, S. (2000). Frequency-dependent synaptic potentiation, depression and spike timing induced by Hebbian pairing in cortical pyramidal neurons. Neural Networks 13, 699–708.Google Scholar
Olivier, E., Grantyn, A., Chat, M., & Berthoz, A. (1993). The control of slow orienting eye movements by tectoreticulospinal neurons in the cat: Behavior, discharge patterns and underlying connections. Experimental Brain Research 93, 435–449.Google Scholar
Pettigrew, J.D. (1974). The effect of visual experience on the development of stimulus specificity by kitten cortical neurons. Journal of Physiology 237, 49–74.Google Scholar
Pritchard, R.M. & Heron, W. (1960). Small eye movements of the cat. Canadian Journal of Psychology 14, 131–137.Google Scholar
Reid, R.C. & Alonso, J.M. (1995). Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284.Google Scholar
Rucci, M., Edelman, G.M., & Wray, J. (2000). Modeling LGN responses during free-viewing: A possible role of microscopic eye movements in the refinement of cortical orientation selectivity. Journal of Neuroscience 20, 4708–4720.Google Scholar
Ruderman, D.L. & Bialek, W. (1994). Statistics of natural images: Scaling in the woods. Physics Review Letters 73, 814–817.Google Scholar
Sengpiel, F., Stawinski, P., & Bonhoeffer, T. (1999). Influence of experience on orientation maps in cat visual cortex. Nature Neuroscience 2, 727–732.Google Scholar
Sherk, H. & Stryker, M. (1976). Quantitative study of cortical orientation selectivity in visually inexperienced kitten. Journal of Neurophysiology 39, 63–70.Google Scholar
Singer, W. & Raushecker, J. (1982). Central-core control of developmental plasticity in the kitten visual cortex II. Electrical activation of mesencephalic and diencephalic projections. Experimental Brain Research 47, 22–233.Google Scholar
Skavenski, A., Robinson, D., Steinman, R., & Timberlake, G. (1975). Miniature eye movements of fixation in rhesus monkey. Vision Research 15, 1269–1273.Google Scholar
Snodderly, D.M., Kagan, I., & Gur, M. (2001). Selective activation of visual cortex neurons by fixational eye movements: Implications for neural coding. Visual Neuroscience 18, 259–277.Google Scholar
Steinbach, M.J. & Money, K.E. (1973). Eye movements of the owl. Vision Research 13, 889–891.Google Scholar
Steinman, R.M., Haddad, G.M., Skavenski, A.A., & Wyman, D. (1973). Miniature eye movement. Science 181, 810–819.Google Scholar
Stent, G.S. (1973). A physiological mechanism for Hebb's postulate of learning. Proceedings of the National Academy of Sciences of the U.S.A. 70, 997–1001.Google Scholar
Stryker, M.P. & Harris, W.A. (1986). Binocular impulse blocakade prevents formation of ocular dominance columns in the cat's visual cortex. Journal of Neuroscience 6, 2117–2133.Google Scholar
Stryker, M.P., Sherk, H., Leventhal, A.G., & Hirsch, H.V.B. (1978). Physiological consequences for the cat's visual cortex of effectively restricting early visual experience with oriented contours. Journal of Neurophysiology 41, 896–909.Google Scholar
Tolhurst, D.J., Walker, N.S., Thompson, I.D., & Dean, A.F. (1980). Non-linearities of temporal summation in neurones in area 17 of the cat. Experimental Brain Research 38, 431–435.Google Scholar
Tsodyks, M.V. & Markram, H. (1997). The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proceedings of the National Academy of Sciences of the U.S.A. 94, 719–723.Google Scholar
Tsodyks, M.V., Pawelzik, K., & Markram, H. (1998). Neural networks with dynamic synapses. Neural Comp 10, 821–835.Google Scholar
van Hateren, J.H. & van der Schaaf, A. (1998). Independent component filters of natural images compared with simple cells in primary visual cortex. Proceedings of the Royal Society B (London) 265, 359–366.Google Scholar
Varela, J., Sen, K., Gibson, J., Fost, J., Abbott, L.F., & Nelson, S.B. (1997). A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. Journal of Neuroscience 17, 7926–7940.Google Scholar
Weliki, M. & Katz, L.C. (1997). Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. Nature 386, 680–685.Google Scholar
White, L.E., Coppola, D.M., & Fitzpatrick, D. (2001). The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex. Nature 411, 1049–1052.Google Scholar
Wilson, J.R. & Sherman, S.M. (1976). Receptive-field characteristics of neurons in the cat striate cortex: Changes with visual field eccentricity. Journal of Neurophysiology 39, 512–531.Google Scholar
Winterson, B.J. & Robinson, D.A. (1975). Fixation by the alert but solitary cat. Vision Research 15, 1349–1352.Google Scholar
Zahs, K.R. & Stryker, M.P. (1988). Segregation of ON and OFF afferents to ferret visual cortex. Journal of Neurophysiology 59, 1410–1429.Google Scholar