Abstract
Brief monocular deprivation during early postnatal development can lead to a depression of synaptic transmission that renders visual cortical neurons unresponsive to subsequent visual stimulation through the deprived eye. The Bienenstock–Cooper–Munro (BCM) theory1 proposes that homosynaptic mechanisms of long-term depression (LTD) account for the deprivation effects2,3. Homosynaptic depression, by definition, occurs only at active synapses. Thus, in contrast to the commonly held view that the synaptic depression caused by monocular deprivation is simply a result of retinal inactivity, this theoretical framework indicates that the synaptic depression may actually be driven by the residual activity in the visually deprived retina4. Here we examine the validity of this idea by comparing the consequences of brief monocular deprivation by lid suture with those of monocular inactivation by intra-ocular treatment with tetrodotoxin. Lid suture leaves the retina spontaneously active, whereas tetrodotoxin eliminates all activity. In agreement with the BCM theory, our results show that monocular lid suture causes a significantly greater depression of deprived-eye responses in kitten visual cortex than does treatment with tetrodotoxin. These findings have important implications for mechanisms of experience-dependent plasticity in the neocortex.
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References
Bienenstock, E. L., Cooper, L. N. & Munro, P. W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci. 2, 32–48 (1982).
Bear, M. F., Cooper, L. N. & Ebner, F. F. Aphysiological basis for a theory of synaptic modification. Science 237, 42–48 (1987).
Bear, M. F. in Mechanistic Relationships between Development and Learning (eds Carew, T. J., Menzel, R. & Shatz, C. J.) 205–225 (Wiley, New York, (1998)).
Blais, B. S., Shouval, H. Z. & Cooper, L. N. The role of presynaptic activity on the ocular dominance shift in monocular deprivation: comparison of homosynaptic and heterosynaptic mechanisms. Proc. Natl Acad. Sci. USA 96, 1083–1087 (1999).
Greuel, J. M., Luhman, H. J. & Singer, W. Evidence for a threshold in experience-dependent long-term changes of kitten visual cortex. Dev. Brain Res. 34, 141–149 (1987).
Chapman, B., Jacobson, M. D., Reiter, H. O. & Stryker, M. P. Ocular dominance shift in kitten visual cortex caused by imbalance in retinal electrical activity. Nature 324, 154–156 (1986).
Mower, G. D. The effect of dark rearing on the time course of the critical period in cat visual cortex. Dev. Brain Res. 58, 151–158 (1991).
Hubel, D. H. & Wiesel, T. N. The period of susceptibility ot the physiological effects of unilateral eye closure in kittens. J. Physiol. 206, 419–436 (1970).
Kaplan, E., Purpura, K. & Shapley, R. M. Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus. J. Physiol. (Lond.) 391, 267–288 (1987).
Stryker, M. P. & Harris, W. A. Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J. Neurosci. 6, 2117–2133 (1986).
Reiter, H. O. & Stryker, M. P. Neural plasticity without postsynaptic action potentials: less active inputs become dominant when kitten visual cortical cells are pharmacologically inhibited. Proc. Natl Acad. Sci. USA 85, 3623–3627 (1988).
Bear, M. F., Kleinschmidt, A., Gu, Q. & Singer, W. Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist. J. Neurosci. 10, 909–925 (1990).
Ramoa, A. S., Paradiso, M. A. & Freeman, R. D. Blockade of intracortical inhibition in the kitten striate cortex: effect on receptive field proper;ties and associated loss of ocular dominance plasticity. Exp. Brain Res. 73, 285–296 (1988).
Artola, A. & Singer, W. Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci. 16, 480–487 (1993).
Bear, M. F. & Kirkwood, A. in Cortical Plasticity: LTP and LTD (eds Fazeli, M. S. & Collingridge, G. L.) 191–205 (Bios Scientific, Oxford, (1996)).
Bear, M. F. & Singer, W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320, 172–176 (1986).
Dudek, S. M. & Friedlander, M. J. Developmental down-regulation of LTD in cortical layer IV and its independence of modulation by inhibition. Neuron 16, 1–20 (1996).
Kirkwood, A., Silva, A. & Bear, M. F. Age-dependent decrease of synaptic plasticity in the neocortex of αCaMKII mutant mice. Proc. Natl Acad. Sci. USA 94, 3380–3383 (1997).
Kirkwood, A. & Bear, M. F. Homosynaptic long-term depression in the visual cortex. J. Neurosci. 14, 3404–3412 (1994).
Kojic, L., Gu, Q., Douglas, R. M. & Cynader, M. S. Serotonin facilitates synaptic plasticity in kitten visual cortex: an in vitro study. Dev. Brain Res. 101, 299–304 (1997).
Kirkwood, A., Rozas, C., Kirkwood, J., Perez, F. & Bear, M. F. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J. Neurosci.(in the press).
Sah, P., Hestrin, S. & Nicoll, R. A. Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons. Science 246, 815–818 (1989).
Wiesel, T. N. & Hubel, D. H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol. 28, 1060–1072 (1965).
Stent, G. S. Aphysiological mechanism for Hebb's postulate of learning. Proc. Natl Acad. Sci. USA 70, 997–1001 (1973).
von der Malsburg, C. Self-organization of orientation-sensitive columns in the striate cortex. Kybernetik 14, 85–100 (1973).
Kirkwood, A., Rioult, M. G. & Bear, M. F. Experience-dependent modification of synaptic plasticity in visual cortex. Nature 381, 526–528 (1996).
Rossi, A. F., Rittenhouse, C. D. & Paradiso, M. A. The representation of brightness in primary visual cortex. Science 273, 1104–1107 (1996).
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This work was supported by the Howard Hughes Medical Institute, the NIH and the Dana Foundation.
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Rittenhouse, C., Shouval, H., Paradiso, M. et al. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature 397, 347–350 (1999). https://doi.org/10.1038/16922
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DOI: https://doi.org/10.1038/16922
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