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The Journal of Neuroscience, March 5, 2008, 28(10):2563-2575; doi:10.1523/JNEUROSCI.5407-07.2008

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Cellular/Molecular
Action Potential-Independent and Nicotinic Receptor-Mediated Concerted Release of Multiple Quanta at Hippocampal CA3–Mossy Fiber Synapses

Geeta Sharma, Michael Grybko, and Sukumar Vijayaraghavan

Department of Physiology and Biophysics and Neuroscience Program, University of Colorado at Denver and Health Sciences Center, Aurora, Colorado 80045

Correspondence should be addressed to Sukumar Vijayaraghavan, Department of Physiology and Biophysics, University of Colorado at Denver and Health Sciences Center, Mail Stop 8307, P.O. Box 6511, 12800 East 19th Avenue, Aurora, CO 80045. Email: sukumar.v{at}uchsc.edu

Presynaptic action potential-independent transmitter release is a potential means of information transfer across synapses. We show that in the hippocampal mossy fiber boutons, activation of the {alpha}7-subtype of nicotinic acetylcholine receptors ({alpha}7-nAChRs) results in a large increase in the amplitude of spontaneous events, resulting from concerted release of multiple quanta from the mossy fiber boutons. This amplitude increase is abolished at low temperatures. Activation of {alpha}7-nAChRs causes a rise in intraterminal calcium at mossy fiber boutons, involving ryanodine receptors. Regulation of concerted release requires the subsequent activation of presynaptic calcium/calmodulin-dependent protein kinase II (CaMKII). Activation of CaMKII is required to drive presynaptic action potential-independent transmission at the mossy fiber–CA3 pyramidal cell synapse. The effects of {alpha}7-nAChR activation are mediated by biologically relevant doses of nicotine. Our results demonstrate a novel form of synaptic plasticity mediated by presynaptic {alpha}7-nAChRs and store calcium that is temporally different and might respond to a different history of synaptic activity than that mediated by incoming action potentials.

Key words: nicotine; addiction; synaptic plasticity; synaptic vesicle release; acetylcholine receptor; synaptic communication; multivesicular; mEPSCs

Received Aug. 29, 2007; revised Jan. 14, 2008; accepted Jan. 16, 2008.

Correspondence should be addressed to Sukumar Vijayaraghavan, Department of Physiology and Biophysics, University of Colorado at Denver and Health Sciences Center, Mail Stop 8307, P.O. Box 6511, 12800 East 19th Avenue, Aurora, CO 80045. Email: sukumar.v{at}uchsc.edu






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