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

Kathryn J. Reissner, Lu Pu, Joanna H. Schaffhausen, Heather D. Boyle, Ian F. Smith, Ian Parker, Thomas Carew

Research output: Contribution to journalArticle

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

Original languageEnglish (US)
Pages (from-to)8797-8806
Number of pages10
JournalJournal of Neuroscience
Volume30
Issue number26
DOIs
StatePublished - Jun 30 2010

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Sensory Receptor Cells
Synapses
Aplysia
Metabotropic Glutamate Receptors
Neuronal Plasticity
Photolysis
Tetanus
Motor Neurons
Injections

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Reissner, K. J., Pu, L., Schaffhausen, J. H., Boyle, H. D., Smith, I. F., Parker, I., & Carew, T. (2010). A novel postsynaptic mechanism for heterosynaptic sharing of short-term plasticity. Journal of Neuroscience, 30(26), 8797-8806. https://doi.org/10.1523/JNEUROSCI.4767-09.2010

A novel postsynaptic mechanism for heterosynaptic sharing of short-term plasticity. / Reissner, Kathryn J.; Pu, Lu; Schaffhausen, Joanna H.; Boyle, Heather D.; Smith, Ian F.; Parker, Ian; Carew, Thomas.

In: Journal of Neuroscience, Vol. 30, No. 26, 30.06.2010, p. 8797-8806.

Research output: Contribution to journalArticle

Reissner, KJ, Pu, L, Schaffhausen, JH, Boyle, HD, Smith, IF, Parker, I & Carew, T 2010, 'A novel postsynaptic mechanism for heterosynaptic sharing of short-term plasticity', Journal of Neuroscience, vol. 30, no. 26, pp. 8797-8806. https://doi.org/10.1523/JNEUROSCI.4767-09.2010
Reissner KJ, Pu L, Schaffhausen JH, Boyle HD, Smith IF, Parker I et al. A novel postsynaptic mechanism for heterosynaptic sharing of short-term plasticity. Journal of Neuroscience. 2010 Jun 30;30(26):8797-8806. https://doi.org/10.1523/JNEUROSCI.4767-09.2010
Reissner, Kathryn J. ; Pu, Lu ; Schaffhausen, Joanna H. ; Boyle, Heather D. ; Smith, Ian F. ; Parker, Ian ; Carew, Thomas. / A novel postsynaptic mechanism for heterosynaptic sharing of short-term plasticity. In: Journal of Neuroscience. 2010 ; Vol. 30, No. 26. pp. 8797-8806.
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