Differential plasticity in neocortical networks

Understanding the synaptic and molecular basis for learning and memory in the neocortex depends upon a clear understanding of the anatomical and connectional diversity within this structure. To the extent that different types of synapses within the neocortex have distinct electrophysiological and, thus, molecular properties, the types of plasticity that these synapses manifest may also be distinct. If thresholds for plasticity are different for excitatory synapses onto inhibitory neurons than for excitatory synapses onto excitatory neurons, the same pattern of excitatory presynaptic activity will have difference consequences on excitatory and inhibitory networks. Differential plasticity will thus affect the way in which experience can modify sensory maps in the neocortex. Experimental support for this hypothesis is presented, as well as some predictions about the function of different types of neocortical pathways and plasticity.

[1]  H. Markram,et al.  Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. , 2002, Cerebral cortex.

[2]  Mark F. Bear,et al.  Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo , 1999, Nature Neuroscience.

[3]  B. Connors,et al.  Thalamocortical responses of mouse somatosensory (barrel) cortexin vitro , 1991, Neuroscience.

[4]  Yasuo Kawaguchi,et al.  Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons , 1997, Brain Research.

[5]  J. Lübke,et al.  Columnar Organization of Dendrites and Axons of Single and Synaptically Coupled Excitatory Spiny Neurons in Layer 4 of the Rat Barrel Cortex , 2000, The Journal of Neuroscience.

[6]  G. Elston,et al.  Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey , 1999, The Journal of comparative neurology.

[7]  Michael B. Calford,et al.  Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation , 1988, Nature.

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

[9]  A. Schleicher,et al.  Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of a novel environment , 2002, Neuroscience.

[10]  T. Woolsey,et al.  Computer‐assisted analyses of barrel neuron axons and their putative synaptic contacts , 1983, The Journal of comparative neurology.

[11]  Michael C. Crair,et al.  A critical period for long-term potentiation at thalamocortical synapses , 1995, Nature.

[12]  Alison L. Barth,et al.  Upregulation of cAMP Response Element-Mediated Gene Expression during Experience-Dependent Plasticity in Adult Neocortex , 2000, The Journal of Neuroscience.

[13]  C. Gilbert,et al.  Axonal sprouting accompanies functional reorganization in adult cat striate cortex , 1994, Nature.

[14]  Alcino J. Silva,et al.  Requirement for α-CaMKII in Experience-Dependent Plasticity of the Barrel Cortex , 1996, Science.

[15]  L. Kaczmarek,et al.  Tactile experience induces c-fos expression in rat barrel cortex. , 2000, Learning & memory.

[16]  Daniel E Feldman,et al.  Long-Term Depression at Thalamocortical Synapses in Developing Rat Somatosensory Cortex , 1998, Neuron.

[17]  M. Bear,et al.  Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity , 2000, Nature.

[18]  J. Donoghue,et al.  Learning-induced LTP in neocortex. , 2000, Science.

[19]  K. Fox,et al.  Time course of experience-dependent synaptic potentiation and depression in barrel cortex of adolescent rats. , 1996, Journal of neurophysiology.

[20]  Alison L. Barth,et al.  NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses , 2001, Nature Neuroscience.

[21]  J. Kaas,et al.  The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. , 1983, Annual review of neuroscience.

[22]  Y. Kubota,et al.  Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex , 1998, Neuroscience.

[23]  C. Gall,et al.  Contrasting patterns in the localization of glutamic acid decarboxylase and Ca2+ /calmodulin protein kinase gene expression in the rat centrat nervous system , 1992, Neuroscience.

[24]  J. Allman,et al.  A neuronal morphologic type unique to humans and great apes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[26]  M. Crair,et al.  Barrel Cortex Critical Period Plasticity Is Independent of Changes in NMDA Receptor Subunit Composition , 2001, Neuron.

[27]  K. Tóth,et al.  Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons , 1998, Nature Neuroscience.

[28]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

[29]  Y. Kubota,et al.  Dependence of GABAergic Synaptic Areas on the Interneuron Type and Target Size , 2000, The Journal of Neuroscience.

[30]  J F Fulton,et al.  Physiology of the Nervous System , 1939, Science.

[31]  I. Soltesz,et al.  Long-term plasticity in interneurons of the dentate gyrus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  K. Tóth,et al.  Differential Mechanisms of Transmission at Three Types of Mossy Fiber Synapse , 2000, The Journal of Neuroscience.

[33]  Pankaj Sah,et al.  Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala , 1998, Nature.

[34]  M. Gulisano,et al.  Emx1 is a marker for pyramidal neurons of the cerebral cortex. , 2001, Cerebral cortex.

[35]  M. Mishkin,et al.  Massive cortical reorganization after sensory deafferentation in adult macaques. , 1991, Science.