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The Journal of Neuroscience, April 29, 2009, 29(17):5605-5615; doi:10.1523/JNEUROSCI.5355-08.2009

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Behavioral/Systems/Cognitive
Persistent Transcription- and Translation-Dependent Long-Term Potentiation Induced by mGluR1 in Hippocampal Interneurons

Israeli Ran,¹ Isabel Laplante,¹ Catherine Bourgeois,¹ Julie Pépin,¹ Philippe Lacaille,¹ Mauro Costa-Mattioli,² Jerry Pelletier,² Nahum Sonenberg,² and Jean-Claude Lacaille¹

¹Groupe de Recherche sur le Système Nerveux Central and Département de Physiologie, Université de Montréal, Montreal, Quebec H3C 3J7, Canada, and ²Department of Biochemistry, McGill University, Montreal, Quebec H3G 1Y6, Canada

Correspondence should be addressed to Dr. Jean-Claude Lacaille, Département de Physiologie, Faculté de Médecine, Université de Montréal, Case Postale 6128, Succursale Centre-Ville, Montréal, QC H3C 3J7, Canada. Email: jean-claude.lacaille{at}umontreal.ca

Hippocampal interneurons synchronize the activity of large neuronal ensembles during memory consolidation. Although the latter process is manifested as increases in synaptic efficacy which require new protein synthesis in pyramidal neurons, it is unknown whether such enduring plasticity occurs in interneurons. Here, we uncover a long-term potentiation (LTP) of transmission at individual interneuron excitatory synapses which persists for at least 24 h, after repetitive activation of type-1 metabotropic glutamate receptors [mGluR1-mediated chemical late LTP (cL-LTP_mGluR1)]. cL-LTP_mGluR1 involves presynaptic and postsynaptic expression mechanisms and requires both transcription and translation via phosphoinositide 3-kinase/mammalian target of rapamycin and MAP kinase kinase-extracellular signal-regulated protein kinase signaling pathways. Moreover, cL-LTP_mGluR1 involves translational control at the level of initiation as it is prevented by hippuristanol, an inhibitor of eIF4A, and facilitated in mice lacking the cap-dependent translational repressor, 4E-BP. Our results reveal novel mechanisms of long-term synaptic plasticity that are transcription and translation-dependent in inhibitory interneurons, indicating that persistent synaptic modifications in interneuron circuits may contribute to hippocampal-dependent cognitive processes.

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Received Nov. 6, 2008; revised Jan. 8, 2009; accepted April 2, 2009.

Correspondence should be addressed to Dr. Jean-Claude Lacaille, Département de Physiologie, Faculté de Médecine, Université de Montréal, Case Postale 6128, Succursale Centre-Ville, Montréal, QC H3C 3J7, Canada. Email: jean-claude.lacaille{at}umontreal.ca

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