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Correlated binocular activity guides recovery from monocular deprivation

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Abstract

Monocular deprivation (MD) has much more rapid and severe effects on the ocular dominance of neurons in the primary visual cortex (V1) than does binocular deprivation1. This finding underlies the widely held hypothesis that the developmental plasticity of ocular dominance reflects competitive interactions for synaptic space between inputs from the two eyes2. According to this view, the relative levels of evoked activity in afferents representing the two eyes determine functional changes in response to altered visual experience. However, if the deprived eye of a monocularly deprived kitten is simply reopened, there is substantial physiological and behavioural recovery, leading to the suggestion that absolute activity levels, or some other non-competitive mechanisms, determine the degree of recovery from MD3,4,5,6,7. Here we provide evidence that correlated binocular input is essential for such recovery. Recovery is far less complete if the two eyes are misaligned after a period of MD. This is a powerful demonstration of the importance of cooperative, associative mechanisms in the developing visual cortex.

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Figure 3: Orientation and ocular-dominance maps for deprived (D) and nondeprived (ND) eyes from a kitten imaged immediately after MD (a), a cat (MDB3) with concordant binocular recovery (b) and a cat (MDS3) with strabismus after MD (c).
Figure 1: Ocular-dominance maps from left-hemisphere V1 of cats with 10-day MD of the left eye.
Figure 2: Histograms of cortical surface area dominated by each of the two eyes in MDB cats (a) and in MDS cats (b).
Figure 4: Recovery of visual acuity in the previously deprived eye of three kittens with binocular recovery (MDB, filled symbols) and three kittens with esotropic strabismus (MDS, open symbols) after a period of MD.

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Acknowledgements

We thank M. Bear and H. Shouval for their helpful discussions, and I. Kehrer and M. Jones for technical assistance. This work was supported by the Wellcome Trust (P.C.K.), the Medical Research Council (C.B., F.S., B.A.), Max-Planck-Gesellschaft (T.B., F.S.), the Canadian Institutes of Health Research (D.E.M.) and the Oxford McDonnell Centre for Cognitive Neuroscience (C.B., B.A.).

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Authors and Affiliations

  1. University Laboratory of Physiology, Parks Road, Oxford, OX1 3PT, UK

    Peter C. Kind, Bashir Ahmed & Colin Blakemore

  2. Department of Biomedical Sciences, University of Edinburgh, Hugh Robson Building, George Square, Edinburgh, EH8 9XD, UK

    Peter C. Kind

  3. Department of Psychology, Dalhousie University, Halifax, B3H 4J1, Nova Scotia, Canada

    Donald E. Mitchell

  4. Max-Planck-Institut für Neurobiologie, Am Klopferspitz 18a, München-Martinsried, 82152, Germany

    Tobias Bonhoeffer & Frank Sengpiel

  5. Cardiff School of Biosciences, Museum Avenue, PO Box 911, Cardiff, CF10 3US, UK

    Frank Sengpiel

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  1. Peter C. Kind
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Correspondence to Peter C. Kind.

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Kind, P., Mitchell, D., Ahmed, B. et al. Correlated binocular activity guides recovery from monocular deprivation. Nature 416, 430–433 (2002). https://doi.org/10.1038/416430a

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