Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex

Paired whole-cell voltage recordings were made from synaptically connected spiny stellate neurons in layer 4 of the barrel field in young (P14) rat somatosensory cortex. When postsynaptic action potentials (APs) followed each of 5 presynaptic APs in a 10- or 20-Hz train by less than 25 ms, subsequent unitary EPSP amplitudes were persistently reduced. Induction of long-term depression (LTD) depended on activation of group II metabotropic glutamate receptors, but not on NMDA or AMPA receptors. Reducing postsynaptic increases in intracellular calcium ([Ca2+]i) by intracellular loading with a fast- (BAPTA) or a slow- (EGTA) acting Ca2+ buffer blocked synaptic depression. Analysis of EPSP failures suggested mediation of LTD by a reduction in release probability. We propose a mechanism by which coincident activity results in long-lasting reduction of synaptic efficacy between synaptically connected neurons.

[1]  G. W. Snedecor Statistical Methods , 1964 .

[2]  Statistical methods , 1980 .

[3]  G. Lynch,et al.  Intracellular injections of EGTA block induction of hippocampal long-term potentiation , 1983, Nature.

[4]  T. H. Brown,et al.  Associative long-term potentiation in hippocampal slices. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Alan Peters,et al.  Cellular components of the cerebral cortex , 1984 .

[6]  R. R. Sturrock,et al.  Problems of the Keimbahn: New Work on Mammalian Germ Cell Lineage , 1985 .

[7]  S. Kelso,et al.  Hebbian synapses in hippocampus. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[8]  T. Sejnowski,et al.  Associative long-term depression in the hippocampus induced by hebbian covariance , 1989, Nature.

[9]  J. Lisman,et al.  A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Gary Lynch,et al.  Stable depression of potentiated synaptic responses in the hippocampus with 1–5 Hz stimulation , 1990, Brain Research.

[11]  D. Madison,et al.  A requirement for the intercellular messenger nitric oxide in long-term potentiation. , 1991, Science.

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

[13]  M. Bear,et al.  Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[14]  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.

[15]  R. Malenka,et al.  Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus , 1992, Neuron.

[16]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[17]  S. Siegelbaum,et al.  Postsynaptic induction and presynaptic expression of hippocampal long-term depression. , 1994, Science.

[18]  H. Tse,et al.  Actions of two new antagonists showing selectivity for different sub‐types of metabotropic glutamate receptor in the neonatal rat spinal cord , 1994, British journal of pharmacology.

[19]  B. Sakmann,et al.  Active propagation of somatic action potentials into neocortical pyramidal cell dendrites , 1994, Nature.

[20]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

[21]  H. Markram,et al.  Dendritic calcium transients evoked by single back‐propagating action potentials in rat neocortical pyramidal neurons. , 1995, The Journal of physiology.

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

[23]  Robert S. Zucker,et al.  Postsynaptic Levels of [Ca2+]i Needed to Trigger LTD and LTP , 1996, Neuron.

[24]  K. Martin,et al.  Excitatory synaptic inputs to spiny stellate cells in cat visual cortex , 1996, Nature.

[25]  S. Dudek,et al.  Developmental Down-Regulation of LTD in Cortical Layer IV and Its Independence of Modulation by Inhibition , 1996, Neuron.

[26]  R. Petralia,et al.  The metabotropic glutamate receptors, MGLUR2 and MGLUR3, show unique postsynaptic, presynaptic and glial localizations , 1996, Neuroscience.

[27]  H. Tse,et al.  Potent antagonists at the L-AP4- and (1S,3S)-ACPD-sensitive presynaptic metabotropic glutamate receptors in the neonatal rat spinal cord , 1996, Neuropharmacology.

[28]  MF Bear Progress in understanding NMDA-receptor-dependent synaptic plasticity in the visual cortex , 1996, Journal of Physiology-Paris.

[29]  Denise Manahan-Vaughan,et al.  Group 1 and 2 Metabotropic Glutamate Receptors Play Differential Roles in Hippocampal Long-Term Depression and Long-Term Potentiation in Freely Moving Rats , 1997, The Journal of Neuroscience.

[30]  T. Tsumoto,et al.  Quantal analysis suggests presynaptic involvement in expression of neocortical short- and long-term depression. , 1997, Neuroscience.

[31]  D. Lovinger,et al.  Decreased Frequency But Not Amplitude of Quantal Synaptic Responses Associated with Expression of Corticostriatal Long-Term Depression , 1997, The Journal of Neuroscience.

[32]  V. Han,et al.  Synaptic plasticity in a cerebellum-like structure depends on temporal order , 1997, Nature.

[33]  P. Somogyi,et al.  Differential plasma membrane distribution of metabotropic glutamate receptors mGluR1α, mGluR2 and mGluR5, relative to neurotransmitter release sites , 1997, Journal of Chemical Neuroanatomy.

[34]  D. Johnston,et al.  Contribution of voltage-gated Ca2+ channels to homosynaptic long-term depression in the CA1 region in vitro. , 1997, Journal of neurophysiology.

[35]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[36]  Yue Wang,et al.  Induction of LTD in the dentate gyrus in vitro is NMDA receptor independent, but dependent on Ca2+ influx via low-voltage-activated Ca2+ channels and release of Ca2+ from intracellular stores. , 1997, Journal of neurophysiology.

[37]  D. Johnston,et al.  A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons , 1997, Science.

[38]  D. Clapham,et al.  NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation , 1998, Nature Neuroscience.

[39]  E. Cherubini,et al.  Two distinct forms of long-term depression coexist at the mossy fiber-CA3 synapse in the hippocampus during development. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[41]  J. Connor,et al.  Requirement of rapid Ca2+ entry and synaptic activation of metabotropic glutamate receptors for the induction of long‐term depression in adult rat hippocampus , 1998, The Journal of physiology.

[42]  F. Crépel,et al.  Cellular mechanisms of cerebellar LTD , 1998, Trends in Neurosciences.

[43]  Thanos Tzounopoulos,et al.  A Role for cAMP in Long-Term Depression at Hippocampal Mossy Fiber Synapses , 1998, Neuron.

[44]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[45]  D. Debanne,et al.  Long‐term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures , 1998, The Journal of physiology.

[46]  J. Lübke,et al.  Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single ‘barrel’ of developing rat somatosensory cortex , 1999, The Journal of physiology.

[47]  R. Anwyl,et al.  Activation of mGluRII induces LTD via activation of protein kinase A and protein kinase C in the dentate gyrus of the hippocampus in vitro , 1999, Neuropharmacology.

[48]  A. Craig,et al.  Axon/Dendrite Targeting of Metabotropic Glutamate Receptors by Their Cytoplasmic Carboxy-Terminal Domains , 1999, Neuron.