Motility of dendritic spines in visual cortex in vivo: Changes during the critical period and effects of visual deprivation

Cortical dendritic spines are highly motile postsynaptic structures onto which most excitatory synapses are formed. It has been postulated that spine dynamics might reflect synaptic plasticity of cortical neurons. To test this hypothesis, we have investigated spine dynamics during the critical period in mouse visual cortex in vivo with and without sensory deprivation. The motility of spines on apical dendrites of layer 5 neurons was assayed by time-lapse two-photon microscopy. Spines were motile at the ages examined, postnatal days (P)21–P42, although motility decreased between P21 and P28 and then remained stable through P42. Binocular deprivation from before the time of eye-opening up-regulated spine motility during the peak of the critical period (P28), without affecting average spine length, class distribution, or density. Deprivation at the start of the critical period had no effect on spine motility, whereas continued deprivation through the end of the critical period appeared to reduce spine motility slightly. We conclude that spine motility might be involved in critical-period plasticity and that reduction of activity during the critical period enhances spine dynamics.

[1]  R. Yuste,et al.  Developmental regulation of spine motility in the mammalian central nervous system. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[2]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

[3]  M P Stryker,et al.  Experience-Dependent Plasticity of Binocular Responses in the Primary Visual Cortex of the Mouse , 1996, The Journal of Neuroscience.

[4]  B. Sakmann,et al.  Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[5]  K. Svoboda,et al.  Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex , 2002, Nature.

[6]  T. Hensch,et al.  Permissive proteolytic activity for visual cortical plasticity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Bear,et al.  Experience-dependent modification of synaptic plasticity in visual cortex , 1996, Nature.

[8]  D. Fitzpatrick,et al.  The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex , 2001, Nature.

[9]  G. Feng,et al.  Imaging Neuronal Subsets in Transgenic Mice Expressing Multiple Spectral Variants of GFP , 2000, Neuron.

[10]  R. Yuste,et al.  Mechanisms of Calcium Decay Kinetics in Hippocampal Spines: Role of Spine Calcium Pumps and Calcium Diffusion through the Spine Neck in Biochemical Compartmentalization , 2000, The Journal of Neuroscience.

[11]  K. Harris,et al.  Slices Have More Synapses than Perfusion-Fixed Hippocampus from both Young and Mature Rats , 1999, The Journal of Neuroscience.

[12]  M Sur,et al.  Rapid acquisition of dendritic spines by visual thalamic neurons after blockade of N-methyl-D-aspartate receptors. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[13]  E. Fifková,et al.  Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area , 1977, Journal of neurocytology.

[14]  K. Harris,et al.  Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated , 1999, Nature Neuroscience.

[15]  M. Stryker,et al.  The role of visual experience in the development of columns in cat visual cortex. , 1998, Science.

[16]  M. Didier-Bazès,et al.  Spatiotemporal Expression Patterns of Metalloproteinases and Their Inhibitors in the Postnatal Developing Rat Cerebellum , 1999, The Journal of Neuroscience.

[17]  M P Stryker,et al.  Rapid Anatomical Plasticity of Horizontal Connections in the Developing Visual Cortex , 2001, The Journal of Neuroscience.

[18]  M P Stryker,et al.  Rapid remodeling of axonal arbors in the visual cortex. , 1993, Science.

[19]  R. Freeman,et al.  Responsivity of normal kitten striate cortex deteriorates after brief binocular deprivation. , 1981, Journal of neurophysiology.

[20]  L. Maffei,et al.  Patterned Vision Causes CRE-Mediated Gene Expression in the Visual Cortex through PKA and ERK , 2003, The Journal of Neuroscience.

[21]  N. Toni,et al.  LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite , 1999, Nature.

[22]  A. S. Ramoa,et al.  cAMP/Ca2+ Response Element-Binding Protein Function Is Essential for Ocular Dominance Plasticity , 2002, The Journal of Neuroscience.

[23]  M. Fischer,et al.  Rapid Actin-Based Plasticity in Dendritic Spines , 1998, Neuron.

[24]  C. Rittenhouse,et al.  Molecular basis for induction of ocular dominance plasticity. , 1999, Journal of neurobiology.

[25]  R. Yuste,et al.  Regulation of Spine Calcium Dynamics by Rapid Spine Motility Materials and Methods , 2022 .

[26]  M. Fagiolini,et al.  Inhibitory threshold for critical-period activation in primary visual cortex , 2000, Nature.

[27]  L. Maffei,et al.  Functional postnatal development of the rat primary visual cortex and the role of visual experience: Dark rearing and monocular deprivation , 1994, Vision Research.

[28]  E. De robertis,et al.  SOME FEATURES OF THE SUBMICROSCOPIC MORPHOLOGY OF SYNAPSES IN FROG AND EARTHWORM , 1955, The Journal of biophysical and biochemical cytology.

[29]  Alcino J. Silva,et al.  Autophosphorylation of αCaMKII Is Required for Ocular Dominance Plasticity , 2002, Neuron.

[30]  W. Denk,et al.  Dendritic spines as basic functional units of neuronal integration , 1995, Nature.

[31]  KM Harris,et al.  Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation [published erratum appears in J Neurosci 1992 Aug;12(8):following table of contents] , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Stephen J. Smith,et al.  Evidence for a Role of Dendritic Filopodia in Synaptogenesis and Spine Formation , 1996, Neuron.

[33]  M. Fischer,et al.  Glutamate receptors regulate actin-based plasticity in dendritic spines , 2000, Nature Neuroscience.

[34]  M. Stryker,et al.  CRE-Mediated Gene Transcription in Neocortical Neuronal Plasticity during the Developmental Critical Period , 1999, Neuron.

[35]  Rafael Yuste,et al.  A custom-made two-photon microscope and deconvolution system , 2000, Pflügers Archiv.

[36]  Rafael Yuste,et al.  Imaging neurons : a laboratory manual , 1999 .

[37]  J. Trachtenberg,et al.  Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. , 2000, Science.

[38]  L. Kaczmarek,et al.  Matrix Metalloproteinase-9 Undergoes Expression and Activation during Dendritic Remodeling in Adult Hippocampus , 2002, The Journal of Neuroscience.

[39]  L. Maffei,et al.  Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex , 2002, Science.

[40]  K. Svoboda,et al.  Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo , 2000, Nature.

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

[42]  M. Segal,et al.  Regulation of Dendritic Spine Motility in Cultured Hippocampal Neurons , 2001, The Journal of Neuroscience.

[43]  M P Stryker,et al.  Plasticity of geniculocortical afferents following brief or prolonged monocular occlusion in the cat , 1996, The Journal of comparative neurology.

[44]  C. Rittenhouse,et al.  Monocular deprivation induces homosynaptic long-term depression in visual cortex , 1999, Nature.

[45]  Rafael Yuste,et al.  Spine motility with synaptic contact , 2001, Nature Neuroscience.

[46]  M. Bear,et al.  Visual Experience and Deprivation Bidirectionally Modify the Composition and Function of NMDA Receptors in Visual Cortex , 2001, Neuron.

[47]  S. Young,et al.  Effect of anisomycin on stimulation-induced changes in dendritic spines of the dentate granule cells , 1982, Journal of neurocytology.

[48]  M. Segal,et al.  Spike-Associated Fast Contraction of Dendritic Spines in Cultured Hippocampal Neurons , 2001, Neuron.

[49]  T. Bliss,et al.  Single Synaptic Events Evoke NMDA Receptor–Mediated Release of Calcium from Internal Stores in Hippocampal Dendritic Spines , 1999, Neuron.

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

[51]  F. Engert,et al.  Dendritic spine changes associated with hippocampal long-term synaptic plasticity , 1999, Nature.

[52]  K. Svoboda,et al.  Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. , 1999, Science.

[53]  N. Kasthuri,et al.  Long-term dendritic spine stability in the adult cortex , 2002, Nature.

[54]  D. Feldman,et al.  Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. , 1999, Journal of neurobiology.