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The Journal of Neuroscience, March 29, 2006, 26(13):3474-3481; doi:10.1523/JNEUROSCI.4338-05.2006

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Cellular/Molecular
B-Ephrin Reverse Signaling Is Required for NMDA-Independent Long-Term Potentiation of Mossy Fibers in the Hippocampus

John N. Armstrong,¹ Michael J. Saganich,¹ Nan-Jie Xu,² Mark Henkemeyer,² Stephen F. Heinemann,¹ and Anis Contractor³

¹Molecular Neurobiology Laboratory, The Salk Institute, La Jolla, California 93037, ²Center for Developmental Biology and Kent Waldrep Foundation Center for Basic Neuroscience Research on Nerve Growth and Regeneration, University of Texas Southwestern Medical Center, Dallas, Texas 75235, and ³Department of Physiology and Northwestern University Institute for Neuroscience, Northwestern University Feinberg School of Medicine, Chicago, Illinois 60611

Correspondence should be addressed to Anis Contractor, Department of Physiology, Northwestern University Feinberg School of Medicine, 303 East Chicago Avenue, Chicago, IL 60611. Email: a-contractor{at}northwestern.edu

The mossy fiber to CA3 pyramidal neuron synapse in the hippocampus displays an atypical form of NMDA receptor-independent long-term potentiation (LTP). Plasticity at this synapse is expressed in the presynaptic terminal as an elevated probability of neurotransmitter release. However, evidence indicates that postsynaptic mechanisms and trans-synaptic signaling through an association between postsynaptic EphB receptors and presynaptic B-ephrins are necessary for the induction of LTP. Here we show that ephrin-B3 protein is highly expressed in mossy fiber axons and terminals. There are specific deficits in mossy fiber LTP in mice in which the cytoplasmic C-terminal signaling domain of the ephrin-B3 protein is replaced with -galactosidase. These deficits are not observed in ephrin-B3 null mutant mice because of functional redundancy by virtue of other B-ephrins. These results indicate that B-ephrin reverse signaling into the presynaptic mossy fiber bouton is required for the induction of NMDA receptor-independent LTP at this synapse.

Key words: long-term potentiation; mossy fiber; hippocampus; ephrin; pyramidal neuron; presynaptic signaling

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Received Oct. 11, 2005; revised Feb. 9, 2006; accepted Feb. 14, 2006.

Correspondence should be addressed to Anis Contractor, Department of Physiology, Northwestern University Feinberg School of Medicine, 303 East Chicago Avenue, Chicago, IL 60611. Email: a-contractor{at}northwestern.edu

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