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The Journal of Neuroscience, October 25, 2006, 26(43):11001-11013; doi:10.1523/JNEUROSCI.1749-06.2006

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Cellular/Molecular
Spine Ca²⁺ Signaling in Spike-Timing-Dependent Plasticity

Thomas Nevian and Bert Sakmann

Department of Cell Physiology, Max-Planck Institute for Medical Research, D-69120 Heidelberg, Germany

Correspondence should be addressed to Thomas Nevian at his present address: Institute for Physiology, Bern University, Bühlplatz 5, CH-3012 Bern, Switzerland. Email: nevian{at}pyl.unibe.ch

Calcium is a second messenger, which can trigger the modification of synaptic efficacy. We investigated the question of whether a differential rise in postsynaptic Ca²⁺ ([Ca²⁺]_i) alone is sufficient to account for the induction of long-term potentiation (LTP) and long-term depression (LTD) of EPSPs in the basal dendrites of layer 2/3 pyramidal neurons of the somatosensory cortex. Volume-averaged [Ca²⁺]_i transients were measured in spines of the basal dendritic arbor for spike-timing-dependent plasticity induction protocols. The rise in [Ca²⁺]_i was uncorrelated to the direction of the change in synaptic efficacy, because several pairing protocols evoked similar spine [Ca²⁺]_i transients but resulted in either LTP or LTD. The sequence dependence of near-coincident presynaptic and postsynaptic activity on the direction of changes in synaptic strength suggested that LTP and LTD were induced by two processes, which were controlled separately by postsynaptic [Ca²⁺]_i levels. Activation of voltage-dependent Ca²⁺ channels before metabotropic glutamate receptors (mGluRs) resulted in the phospholipase C-dependent (PLC-dependent) synthesis of endocannabinoids, which acted as a retrograde messenger to induce LTD. LTP required a large [Ca²⁺]_i transient evoked by NMDA receptor activation. Blocking mGluRs abolished the induction of LTD and uncovered the Ca²⁺-dependent induction of LTP.

We conclude that the volume-averaged peak elevation of [Ca²⁺]_i in spines of layer 2/3 pyramids determines the magnitude of long-term changes in synaptic efficacy. The direction of the change is controlled, however, via a mGluR-coupled signaling cascade. mGluRs act in conjunction with PLC as sequence-sensitive coincidence detectors when postsynaptic precede presynaptic action potentials to induce LTD. Thus presumably two different Ca²⁺ sensors in spines control the induction of spike-timing-dependent synaptic plasticity.

Key words: LTP; LTD; synaptic plasticity; calcium; two-photon microscopy; spine; spike-timing-dependent plasticity; mGluR; NMDAR

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Received April 25, 2006; revised Sept. 13, 2006; accepted Sept. 14, 2006.

Correspondence should be addressed to Thomas Nevian at his present address: Institute for Physiology, Bern University, Bühlplatz 5, CH-3012 Bern, Switzerland. Email: nevian{at}pyl.unibe.ch

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