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Effects of different forms of monocular deprivation on primary visual cortex maps

Published online by Cambridge University Press:  13 August 2012

SAJJIDA JAFFER
Affiliation:
School of Biosciences, Cardiff University, Cardiff, United Kingdom Present address: School of Biological Sciences, University of Reading, Hopkins Building, Reading, RG6 6UB, UK
VASILY VOROBYOV
Affiliation:
School of Biosciences, Cardiff University, Cardiff, United Kingdom Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Russia
FRANK SENGPIEL*
Affiliation:
School of Biosciences, Cardiff University, Cardiff, United Kingdom

Abstract

Monocular deprivation (MD) by lid suture is one of the classic paradigms for the study of developmental plasticity in the cerebral cortex, and we have detailed knowledge of its anatomical and physiological consequences as well as underlying molecular and cellular mechanisms. However, the effects of other forms of manipulating visual input through one eye on the functional architecture of the primary visual cortex (V1) have not yet been examined directly. We compared MD by lid suture with the effects of daily monocular lens wear using either a frosted lens or a neutral density (ND) filter. We used optical imaging of intrinsic signals and visually evoked potentials (VEPs) to assess responses in V1 to monocular stimulation. We found that loss of stimulus contrast through monocular frosted lens wear resulted in marked takeover of cortical territory by the nondeprived eye (NDE) similar to that caused by classic MD, and in virtual absence of orientation-selective responses following stimulation of the deprived eye (DE). Furthermore, amplitudes of VEPs in response to gratings of a range of spatial frequencies were significantly reduced in the DE compared to the NDE. In contrast, differences in luminance between two eyes caused by an ND filter in front of one eye did not affect ocular dominance and orientation maps, and there was no significant difference in the amplitude of VEPs elicited through the two eyes. Our results are consistent with previous electrophysiological studies in demonstrating that binocular pattern information is necessary to maintain normal functional maps in both eyes, while reduced luminance in one eye has little effect on the overall functional architecture and visual responses in V1.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2012

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References

Antonini, A. & Stryker, M.P. (1996). Plasticity of geniculocortical afferents following brief or prolonged monocular occlusion in the cat. The Journal of Comparative Neurology 369, 6482.3.0.CO;2-I>CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1969). Changes in the maintained discharge with adaptation level in the cat retina. The Journal of Physiology, 202, 699718.CrossRefGoogle ScholarPubMed
Bienenstock, E.L., Cooper, L. & Munro, P.W. (1982). Theory for the development of neuron selectivity: Orientation specificity and binocular interaction in visual cortex. The Journal of Neuroscience 2, 3248.CrossRefGoogle ScholarPubMed
Blakemore, C. (1976). The conditions required for the maintenance of binocularity in the kitten’s visual cortex. The Journal of Physiology 261, 423444.CrossRefGoogle ScholarPubMed
Bonhoeffer, T. & Grinvald, A. (1996). Optical imaging based on intrinsic signals. The methodology. In: Brain Mapping: The Methods, ed. Toga, A.W. & Mazziotta, J.C., pp. 5597. London: Academic Press.Google Scholar
Blais, B.S., Shouval, H.Z. & Cooper, L.N. (1999). The role of presynaptic activity in monocular deprivation: Comparison of homosynaptic and heterosynaptic mechanisms. Proceedings of the National Academy of Sciences of the United States of America 96, 10831087.CrossRefGoogle ScholarPubMed
Christen, W.G. & Mower, G.D. (1987). Effects of monocular occlusion and diffusion on visual system development in the cat. Brain Research 415, 233241.CrossRefGoogle ScholarPubMed
Crawford, M.L. & Marc, R.E. (1976). Light transmission of cat and monkey eyelids. Vision Research 16, 323324.CrossRefGoogle Scholar
Dews, P.B. & Wiesel, T.N. (1970). Consequences of monocular deprivation on visual behaviour in kittens. The Journal of Physiology 206, 437455.CrossRefGoogle ScholarPubMed
Eggers, H.M. & Blakemore, C. (1978). Physiological basis of anisometropic amblyopia. Science 201, 264267.CrossRefGoogle ScholarPubMed
Frenkel, M.Y. & Bear, M.F. (2004). How monocular deprivation shifts ocular dominance in visual cortex of young mice. Neuron 44, 917923.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1970). The period of susceptibility to the physiological effects of unilateral eye closure in kittens. The Journal of Physiology 206, 419436.CrossRefGoogle Scholar
Hunt, J.J., Giacomantonio, C.E., Tang, H., Mortimer, D., Jaffer, S., Vorobyov, V., Ericksson, G., Sengpiel, F. & Goodhill, G.J. (2009). Natural scene statistics and the structure of orientation maps in the visual cortex. NeuroImage 47, 157172.CrossRefGoogle ScholarPubMed
Jaffer, S., Vorobyov, V., Kind, P.C. & Sengpiel, F. (2012). Experience-dependent regulation of functional maps and synaptic protein expression in the cat visual cortex. The European Journal of Neuroscience 8, 12811294.CrossRefGoogle Scholar
Loop, M.S. & Sherman, S.M. (1977). Visual discriminations during eyelid closure in the cat. Brain Research 128, 329339.CrossRefGoogle ScholarPubMed
Mrsic-Flogel, T.D., Hofer, S.B., Ohki, K., Reid, R.C., Bonhoeffer, T. & Hubener, M. (2007). Homeostatic regulation of eye-specific responses in visual cortex during ocular dominance plasticity. Neuron 54, 961972.CrossRefGoogle ScholarPubMed
Rittenhouse, C.D., Sieglar, B.A., Voelker, C.C., Shouval, H.Z., Paradiso, M.A. & Bear, M.F. (2006). Stimulus for rapid ocular dominance plasticity in visual cortex. Journal of Neurophysiology 95, 29472950.CrossRefGoogle ScholarPubMed
Schwarzkopf, D.S., Vorobyov, V., Mitchell, D.E. & Sengpiel, F. (2007). Brief daily binocular vision prevents monocular deprivation effects in visual cortex. The European Journal of Neuroscience. 25, 270280.CrossRefGoogle ScholarPubMed
Shatz, C.J. & Stryker, M.P. (1978). Ocular dominance in layer IV of the cat’s visual cortex and the effects of monocular deprivation. The Journal of Physiology 281, 267283.CrossRefGoogle ScholarPubMed
Spear, P.D., Tong, L. & Langsetmo, A. (1978). Striate cortex neurons of binocularly deprived kittens respond to visual stimuli through the closed eyelids. Brain Research 155, 141146.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1963). Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology 26, 10031017.CrossRefGoogle Scholar