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The Journal of Neuroscience, October 27, 2004, 24(43):9612-9622; doi:10.1523/JNEUROSCI.5583-03.2004

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Cellular/Molecular
Calcium Release from Presynaptic Ryanodine-Sensitive Stores Is Required for Long-Term Depression at Hippocampal CA3-CA3 Pyramidal Neuron Synapses

Vivek K. Unni,¹ Stanislav S. Zakharenko,¹ Leonard Zablow,^1,3 Anthony J. DeCostanzo,² and Steven A. Siegelbaum^1,2,3

¹Center for Neurobiology and Behavior, ²Department of Pharmacology, and ³Howard Hughes Medical Institute, Columbia University, New York, New York 10032

Although Ca²⁺ release from internal stores has been proposed to be important for the induction of long-term synaptic plasticity, the importance of Ca²⁺ stores localized in presynaptic terminals remains unclear. Here, we have selectively applied pharmacological antagonists to either the presynaptic or postsynaptic cell in paired whole-cell recordings from hippocampal CA3 pyramidal neurons in slice culture. We demonstrate directly the necessary role of presynaptic, but not postsynaptic, ryanodine-sensitive Ca²⁺ stores in the induction of NMDA receptor (NMDAR)-dependent long-term depression (LTD). Using two-photon laser scanning microscopy, we further find that release from the ryanodine-sensitive stores during prolonged synaptic stimulation generates a slowly rising Ca²⁺ signal in the presynaptic terminal that is required for the induction of LTD. Moreover, this form of LTD has a significant presynaptic component of expression because it causes a marked decrease in the rate of release from CA3 neuron presynaptic terminals of FM 1-43, a fluorescent probe of synaptic vesicle cycling. Thus, Ca²⁺ release from presynaptic ryanodine-sensitive stores is critical in the induction of a presynaptic component of NMDAR-dependent LTD.

Key words: long-term depression; CA3; internal calcium stores; ryanodine-sensitive stores; hippocampus; synaptic plasticity

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Received Dec 18, 2003; revised September 7, 2004; accepted September 9, 2004.

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