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A novel postsynaptic mechanism for heterosynaptic sharing of short-term plasticity

  • Author(s): Reissner, KJ
  • Pu, L
  • Schaffhausen, JH
  • Boyle, HD
  • Smith, IF
  • Parker, I
  • Carew, TJ
  • et al.
Abstract

Postsynaptic release of Ca2+ from intracellular stores is an important means of cellular signaling that mediates numerous forms of synaptic plasticity. Previous studies have identified a postsynaptic intracellular Ca2+ requirement for a form of short-term plasticity, post-tetanic potentiation (PTP) at sensory neuron (SN) - motor neuron synapses in Aplysia. Here, we show that postsynaptic IP3-mediated Ca2+ release in response to a presynaptic tetanus in an SN that induces PTP can confer transient plasticity onto a neighboring SN synapse receiving subthreshold activation. This heterosynaptic sharing of plasticity represents a dynamic, short-term synaptic enhancement of synaptic inputs onto a common postsynaptic target. Heterosynaptic sharing is blocked by postsynaptic disruption of Ca 2+- and IP3-mediated signaling, and, conversely, it is mimicked by postsynaptic injection of nonhydrolyzable IP3 , and by photolysis of caged IP3 in the MN. The molecular mechanism for heterosynaptic sharing involves metabotropic glutamate receptors and Homerdependent interactions, indicating that Homer can facilitate the integration of Ca2+-dependent plasticity at neighboring postsynaptic sites and provides a postsynaptic mechanism for the spread of plasticity induced by presynaptic activation. Our results support a model in which postsynaptic summation of IP3 signals from suprathreshold and subthreshold inputs results in molecular coincidence detection that gives rise to a novel form of heterosynaptic plasticity. Copyright©2010 the authors.

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