Effects of Intracortical Infusion of Anticholinergic Drugs on Neuronal Plasticity in Kitten Striate Cortex

During a critical period of postnatal development the mammalian visual cortex is highly susceptible to experience‐dependent alterations of neuronal response properties. These modifications are facilitated by the neuromodulators noradrenalin and acetylcholine. To identify the cholinergic mechanisms responsible for this facilitation, muscarinic and nicotinic antagonists were infused into the visual cortex of kittens while the animals were subject to monocular deprivation. Subsequently the ocular dominance of cortical cells was assessed by single‐unit recording. Ocular dominance changes were suppressed by scopolamine and pirenzepine but not by gallamine, hexamethonium and mecamylamine. This blocking effect was concentration‐dependent, and control experiments revealed that it was not due to suppression of neuronal responses to light. It is concluded from these results that acetylcholine facilitates neuronal plasticity in the visual cortex through mechanisms activated by muscarinic M1 receptors.

[1]  D. Hubel,et al.  RECEPTIVE FIELDS OF CELLS IN STRIATE CORTEX OF VERY YOUNG, VISUALLY INEXPERIENCED KITTENS. , 1963, Journal of neurophysiology.

[2]  D. Hubel,et al.  SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. , 1963, Journal of neurophysiology.

[3]  D. Hubel,et al.  Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. , 1965, Journal of neurophysiology.

[4]  D. Hubel,et al.  The period of susceptibility to the physiological effects of unilateral eye closure in kittens , 1970, The Journal of physiology.

[5]  J. Pettigrew,et al.  Depletion of brain catecholamines: failure of ocular dominance shift after monocular occlusion in kittens. , 1976, Science.

[6]  P. Molinoff,et al.  beta-Adrenergic receptor involvement in 6-hydroxydopamine-induced supersensitivity in rat cerebral cortex. , 1976, Science.

[7]  J. Pettigrew,et al.  Local perfusion of noradrenaline maintains visual cortical plasticity , 1978, Nature.

[8]  W. Singer,et al.  Changes in the circuitry of the kitten visual cortex are gated by postsynaptic activity , 1979, Nature.

[9]  J. Pettigrew,et al.  Restoration of visual cortical plasticity by local microperfusion of norepinephrine , 1979, The Journal of comparative neurology.

[10]  J. Pettigrew,et al.  Preservation of binocularity after monocular deprivation in the striate cortex of kittens treated with 6‐Hydroxydopamine , 1979, The Journal of comparative neurology.

[11]  N. Birdsall,et al.  Pirenzepine distinguishes between different subclasses of muscarinic receptors , 1980, Nature.

[12]  S. T. Mason,et al.  Modulation of rat brain α- and β-adrenergic receptor populations by lesions of the dorsal noradrenergic bundle , 1980, Brain Research.

[13]  S. T. Mason,et al.  Modulation of rat brain alpha- and beta-adrenergic receptor populations by lesion of the dorsal noradrenergic bundle. , 1980, Brain research.

[14]  R. Duckrow,et al.  Cerebral compensation for chronic noradrenergic denervation induced by locus ceruleus lesion: recovery of receptor binding, isoproterenol- induced adenylate cyclase activity, and oxidative metabolism , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  K. Fuxe,et al.  Muscarinic supersensitivity induced by septal lesion or chronic atropine treatment , 1981, Brain Research.

[16]  J. Pettigrew,et al.  Cortical recovery from effects of monocular deprivation: acceleration with norepinephrine and suppression with 6-hydroxydopamine. , 1981, Journal of neurophysiology.

[17]  J. Movshon,et al.  Visual neural development. , 1981, Annual review of psychology.

[18]  S. Sherman,et al.  Organization of visual pathways in normal and visually deprived cats. , 1982, Physiological reviews.

[19]  N. Birdsall,et al.  Muscarinic receptor subclasses , 1983 .

[20]  S. Nelson,et al.  Two methods of catecholamine depletion in kitten visual cortex yield different effects on plasticity , 1983, Nature.

[21]  M. Ariel,et al.  Effects of 6-hydroxydopamine on visual deprivation in the kitten striate cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  M. Bear,et al.  The plastic response to monocular deprivation persists in kitten visual cortex after chronic depletion of norepinephrine , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  Y. Frégnac,et al.  Development of neuronal selectivity in primary visual cortex of cat. , 1984, Physiological reviews.

[24]  N. Daw,et al.  Substantial reduction of cortical noradrenaline by lesions of adrenergic pathway does not prevent effects of monocular deprivation , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  M. Cynader,et al.  Disruption of cortical activity prevents ocular dominance changes in monocularly deprived kittens , 1984, Nature.

[26]  M. Cynader,et al.  Ontogenesis of muscarinic acetylcholine binding sites in cat visual cortex: reversal of specific laminar distribution during the critical period. , 1984, Brain research.

[27]  D. Mash,et al.  Loss of M2 muscarine receptors in the cerebral cortex in Alzheimer's disease and experimental cholinergic denervation. , 1985, Science.

[28]  Y. Frégnac,et al.  Noradrenaline and functional plasticity in kitten visual cortex: a re‐examination. , 1985, The Journal of physiology.

[29]  D. McCormick,et al.  Two types of muscarinic response to acetylcholine in mammalian cortical neurons. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[30]  W. Singer,et al.  Modulation of visual cortical plasticity by acetylcholine and noradrenaline , 1986, Nature.

[31]  M. Cynader,et al.  The laminar distributions and postnatal development of neurotransmitter and neuromodulator receptors in cat visual cortex , 1986, Brain Research Bulletin.

[32]  C. Blaha,et al.  Doses of 6-hydroxydopamine sufficient to deplete norepinephrine are not sufficient to decrease plasticity in the visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  T. Kasamatsu,et al.  Concentration-dependent suppression by β-adrenergic antagonists of the shift in ocular dominance following monocular deprivation in kitten visual cortex , 1986, Neuroscience.

[34]  W. Singer,et al.  A Possible Role of Calcium Currents in Developmental Plasticity , 1986 .

[35]  W. Singer,et al.  Evidence for a threshold in experience-dependent long-term changes of kitten visual cortex. , 1987, Brain research.

[36]  T. Tsumoto,et al.  Effects of cholinergic depletion on neuron activities in the cat visual cortex. , 1987, Journal of neurophysiology.

[37]  M. Cynader,et al.  Nicotine receptors are located on lateral geniculate nucleus terminals in cat visual cortex , 1987, Brain Research.

[38]  W. Singer,et al.  Blockade of "NMDA" receptors disrupts experience-dependent plasticity of kitten striate cortex. , 1987, Science.

[39]  Y. Frégnac,et al.  A cellular analogue of visual cortical plasticity , 1988, Nature.

[40]  Y. Frégnac,et al.  A cellular analogue of visual cortical plasticity , 1988, Nature.

[41]  M. Stryker,et al.  Neural plasticity without postsynaptic action potentials: less-active inputs become dominant when kitten visual cortical cells are pharmacologically inhibited. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[42]  M. Cynader,et al.  The distribution and ontogenesis of [3H]nicotine binding sites in cat visual cortex. , 1988, Brain research.

[43]  W. Singer,et al.  Pharmacological induction of use-dependent receptive field modifications in the visual cortex. , 1988, Science.

[44]  M. Cynader,et al.  Cellular and subcellular localisation of muscarinic acetylcholine receptors during postnatal development of cat visual cortex using immunocytochemical procedures. , 1988, Brain research. Developmental brain research.

[45]  N. Saito,et al.  The acetylcholine and catecholamine contents in song control nuclei of zebra finch during song ontogeny. , 1989, Brain research. Developmental brain research.

[46]  T. Kasamatsu,et al.  Interaction of noradrenergic and cholinergic systems in regulation of ocular dominance plasticity , 1989, Neuroscience Research.

[47]  W Singer,et al.  Chronic recordings from single sites of kitten striate cortex during experience-dependent modifications of receptive-field properties. , 1989, Journal of neurophysiology.

[48]  W Singer,et al.  Blockade of NMDA-receptors prevents ocularity changes in kitten visual cortex after reversed monocular deprivation. , 1989, Brain research. Developmental brain research.

[49]  T. Kasamatsu,et al.  Noradrenergic control of ocular dominance plasticity in the visual cortex of dark-reared cats. , 1989, Brain research. Developmental brain research.

[50]  P. Schwindt,et al.  Norepinephrine selectively reduces slow Ca2+- and Na+-mediated K+ currents in cat neocortical neurons. , 1989, Journal of neurophysiology.

[51]  A. C. Collins,et al.  Nicotine effects in mouse hippocampus are blocked by mecamylamine, but not other nicotinic antagonists , 1990, Brain Research.

[52]  H. Markram,et al.  Long‐lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. , 1990, The Journal of physiology.

[53]  W Singer,et al.  Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  G. Prusky,et al.  The distribution of M1 and M2 muscarinic acetylcholine receptor subtypes in the developing cat visual cortex. , 1990, Brain research. Developmental brain research.

[55]  W. Singer,et al.  Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex , 1990, Nature.

[56]  J. Rauschecker,et al.  Mechanisms of visual plasticity: Hebb synapses, NMDA receptors, and beyond. , 1991, Physiological reviews.

[57]  W. Singer,et al.  Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex , 1992, Brain Research.

[58]  W Singer,et al.  Intracellular injection of Ca2+ chelators blocks induction of long-term depression in rat visual cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.