Spatiotemporal dynamics of dendritic spines in the living brain

Dendritic spines are ubiquitous postsynaptic sites of most excitatory synapses in the mammalian brain, and thus may serve as structural indicators of functional synapses. Recent works have suggested that neuronal coding of memories may be associated with rapid alterations in spine formation and elimination. Technological advances have enabled researchers to study spine dynamics in vivo during development as well as under various physiological and pathological conditions. We believe that better understanding of the spatiotemporal patterns of spine dynamics will help elucidate the principles of experience-dependent circuit modification and information processing in the living brain.

[1]  T. Murphy,et al.  In Vivo Voltage-Sensitive Dye Imaging in Adult Mice Reveals That Somatosensory Maps Lost to Stroke Are Replaced over Weeks by New Structural and Functional Circuits with Prolonged Modes of Activation within Both the Peri-Infarct Zone and Distant Sites , 2009, The Journal of Neuroscience.

[2]  J. Lund,et al.  Development of neurons in the visual cortex (area 17) of the monkey (Macaca nemestrina): A Golgi study from fetal day 127 to postnatal maturity , 1977, The Journal of comparative neurology.

[3]  W. Gan,et al.  Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance , 2013, Nature Neuroscience.

[4]  Mochtar Pribadi,et al.  Laminar and compartmental regulation of dendritic growth in mature cortex , 2009, Nature Neuroscience.

[5]  A. Dunaevsky,et al.  Altered Structural and Functional Synaptic Plasticity with Motor Skill Learning in a Mouse Model of Fragile X Syndrome , 2013, The Journal of Neuroscience.

[6]  E Gould,et al.  Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  M. Sheng,et al.  Molecular mechanisms of dendritic spine morphogenesis , 2006, Current Opinion in Neurobiology.

[8]  Yi Zuo,et al.  Spine plasticity in the motor cortex , 2011, Current Opinion in Neurobiology.

[9]  M. Segal Dendritic spines and long-term plasticity , 2005, Nature Reviews Neuroscience.

[10]  Karel Svoboda,et al.  A protocol for preparing GFP-labeled neurons previously imaged in vivo and in slice preparations for light and electron microscopic analysis , 2009, Nature Protocols.

[11]  Stephen J. Smith,et al.  Array Tomography: A New Tool for Imaging the Molecular Architecture and Ultrastructure of Neural Circuits , 2007, Neuron.

[12]  Mriganka Sur,et al.  Structural Dynamics of Synapses in Vivo Correlate with Functional Changes during Experience-Dependent Plasticity in Visual Cortex , 2010, The Journal of Neuroscience.

[13]  A. Dunaevsky,et al.  Dendritic spine plasticity: Looking beyond development , 2007, Brain Research.

[14]  Anthony Holtmaat,et al.  The Relationship between PSD-95 Clustering and Spine Stability In Vivo , 2014, The Journal of Neuroscience.

[15]  Yi Zuo,et al.  Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex , 2005, Nature.

[16]  T. Murphy,et al.  Extensive Turnover of Dendritic Spines and Vascular Remodeling in Cortical Tissues Recovering from Stroke , 2007, The Journal of Neuroscience.

[17]  Denise M. Piscopo,et al.  Cocaine-induced structural plasticity in frontal cortex correlates with conditioned place preference , 2013, Nature Neuroscience.

[18]  W. Gan,et al.  Opposite effects of fear conditioning and extinction on dendritic spine remodelling , 2012, Nature.

[19]  W. Greenough,et al.  Dendritic spine structural anomalies in fragile-X mental retardation syndrome. , 2000, Cerebral cortex.

[20]  P. T. Nguyen,et al.  Dendritic Spine Abnormalities in Amyloid Precursor Protein Transgenic Mice Demonstrated by Gene Transfer and Intravital Multiphoton Microscopy , 2005, The Journal of Neuroscience.

[21]  Elly Nedivi,et al.  Clustered Dynamics of Inhibitory Synapses and Dendritic Spines in the Adult Neocortex , 2012, Neuron.

[22]  Timothy H Murphy,et al.  Rapid Reversible Changes in Dendritic Spine Structure In Vivo Gated by the Degree of Ischemia , 2005, The Journal of Neuroscience.

[23]  K. Svoboda,et al.  Spine growth precedes synapse formation in the adult neocortex in vivo , 2006, Nature Neuroscience.

[24]  P. Penzes,et al.  Dendritic spine pathology in neuropsychiatric disorders , 2011, Nature Neuroscience.

[25]  Ania K. Majewska,et al.  Microglial Interactions with Synapses Are Modulated by Visual Experience , 2010, PLoS biology.

[26]  S. B. Kater,et al.  Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. , 1994, Annual review of neuroscience.

[27]  Brice Bathellier,et al.  Dynamics of dendritic spines in the mouse auditory cortex during memory formation and memory recall , 2013, Proceedings of the National Academy of Sciences.

[28]  J. DeFelipe,et al.  Density and morphology of dendritic spines in mouse neocortex , 2006, Neuroscience.

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

[30]  K. Svoboda,et al.  Experience-dependent structural synaptic plasticity in the mammalian brain , 2009, Nature Reviews Neuroscience.

[31]  T. Bonhoeffer,et al.  Experience leaves a lasting structural trace in cortical circuits , 2008, Nature.

[32]  Willie F. Tobin,et al.  Rapid formation and selective stabilization of synapses for enduring motor memories , 2009, Nature.

[33]  H. Zoghbi,et al.  Dendritic Arborization and Spine Dynamics Are Abnormal in the Mouse Model of MECP2 Duplication Syndrome , 2013, The Journal of Neuroscience.

[34]  Lu Chen,et al.  Accelerated Experience-Dependent Pruning of Cortical Synapses in Ephrin-A2 Knockout Mice , 2013, Neuron.

[35]  Karel Svoboda,et al.  Structural Plasticity Underlies Experience-Dependent Functional Plasticity of Cortical Circuits , 2010, The Journal of Neuroscience.

[36]  Y. Zuo,et al.  Experience-dependent structural plasticity in the cortex , 2011, Trends in Neurosciences.

[37]  J. Bourne,et al.  Do thin spines learn to be mushroom spines that remember? , 2007, Current Opinion in Neurobiology.

[38]  K. Svoboda,et al.  Structure and function of dendritic spines. , 2002, Annual review of physiology.

[39]  Stephen J. Smith,et al.  Single-Synapse Analysis of a Diverse Synapse Population: Proteomic Imaging Methods and Markers , 2010, Neuron.

[40]  W. Gan,et al.  Stably maintained dendritic spines are associated with lifelong memories , 2009, Nature.

[41]  J. Yates,et al.  Microglia Promote Learning-Dependent Synapse Formation through Brain-Derived Neurotrophic Factor , 2013, Cell.

[42]  J. Trachtenberg,et al.  Pattern, and not magnitude, of neural activity determines dendritic spine stability in awake mice , 2012, Nature Neuroscience.

[43]  Karel Svoboda,et al.  Experience-dependent and cell-type-specific spine growth in the neocortex , 2006, Nature.

[44]  A. Holtmaat,et al.  Peripheral Deafferentation-Driven Functional Somatosensory Map Shifts Are Associated with Local, Not Large-Scale Dendritic Structural Plasticity , 2013, The Journal of Neuroscience.

[45]  W. Gan,et al.  Development of Long-Term Dendritic Spine Stability in Diverse Regions of Cerebral Cortex , 2005, Neuron.

[46]  C. Portera-Cailliau,et al.  Delayed Stabilization of Dendritic Spines in Fragile X Mice , 2010, The Journal of Neuroscience.

[47]  N. Spruston Pyramidal neurons: dendritic structure and synaptic integration , 2008, Nature Reviews Neuroscience.

[48]  Lawrence C Katz,et al.  Dendritic stability in the adult olfactory bulb , 2003, Nature Neuroscience.

[49]  S. Tonegawa,et al.  A clustered plasticity model of long-term memory engrams , 2006, Nature Reviews Neuroscience.

[50]  Ju Lu,et al.  REPETITIVE MOTOR LEARNING INDUCES COORDINATED FORMATION OF CLUSTERED DENDRITIC SPINES IN VIVO , 2012, Nature.

[51]  J. Nabekura,et al.  Rapid Synaptic Remodeling in the Adult Somatosensory Cortex following Peripheral Nerve Injury and Its Association with Neuropathic Pain , 2011, The Journal of Neuroscience.

[52]  G. Shepherd,et al.  Transient and Persistent Dendritic Spines in the Neocortex In Vivo , 2005, Neuron.

[53]  W. Gan,et al.  Dendritic spine instability and insensitivity to modulation by sensory experience in a mouse model of fragile X syndrome , 2010, Proceedings of the National Academy of Sciences.

[54]  A. Polsky,et al.  Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study , 2007, Nature Neuroscience.

[55]  Mriganka Sur,et al.  Motility of dendritic spines in visual cortex in vivo: Changes during the critical period and effects of visual deprivation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[56]  A. Holtmaat,et al.  Dendritic Spine Instability Leads to Progressive Neocortical Spine Loss in a Mouse Model of Huntington's Disease , 2013, The Journal of Neuroscience.

[57]  S. R. Cajal,et al.  Estructura de los centros nerviosos de las Aves , 1888 .

[58]  Jaime Grutzendler,et al.  Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches , 2004, Nature Neuroscience.

[59]  Nathalie L Rochefort,et al.  Functional mapping of single spines in cortical neurons in vivo , 2011, Nature.

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

[61]  Carlos Portera-Cailliau,et al.  Absence of Large-Scale Dendritic Plasticity of Layer 5 Pyramidal Neurons in Peri-Infarct Cortex , 2011, The Journal of Neuroscience.

[62]  Kristen M Harris,et al.  Dendritic Spine Pathology: Cause or Consequence of Neurological Disorders? , 2002, Brain Research Reviews.

[63]  Mark Hübener,et al.  PirB regulates a structural substrate for cortical plasticity , 2013, Proceedings of the National Academy of Sciences.

[64]  A. Dunaevsky,et al.  Dendritic spine morphogenesis and plasticity. , 2005, Journal of neurobiology.

[65]  Richard Mooney,et al.  Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning , 2010, Nature.

[66]  M. Sheng,et al.  Dentritic spines : structure, dynamics and regulation , 2001, Nature Reviews Neuroscience.

[67]  Carlos Portera-Cailliau,et al.  Altered Synaptic Dynamics during Normal Brain Aging , 2013, The Journal of Neuroscience.

[68]  I. Weiler,et al.  Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[70]  C. Portera-Cailliau,et al.  Chronic in vivo imaging shows no evidence of dendritic plasticity or functional remapping in the contralesional cortex after stroke. , 2013, Cerebral cortex.

[71]  S. Hyman Addiction: a disease of learning and memory. , 2005, The American journal of psychiatry.

[72]  Kristina D. Micheva,et al.  Array Tomography: A New Tool for Imaging the Molecular Architecture and Ultrastructure of Neural Circuits , 2007, Neuron.