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The Journal of Neuroscience, September 5, 2007, 27(36):9560-9572; doi:10.1523/JNEUROSCI.1237-07.2007

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Cellular/Molecular
Synaptic Kainate Receptors Tune Oriens-Lacunosum Moleculare Interneurons to Operate at Theta Frequency

Miri Goldin, Jérôme Epsztein, Isabel Jorquera, Alfonso Represa, Yehezkel Ben-Ari, Valérie Crépel, and Rosa Cossart

Institut de Neurobiologie de la Méditeranée, Inserm, Unité 29, Université de la Méditerranée, Parc Scientifique de Luminy, 13273 Marseille cedex 9, France

Correspondence should be addressed to Dr. Rosa Cossart, Institut de Neurobiologie de la Méditerranée, Inserm, Unité 29, Parc Scientifique de Luminy, Boîte Postale 13, 13273 Marseille cedex 9, France. Email: cossart{at}inmed.univ-mrs.fr

GABAergic interneurons of the hippocampus play an important role in the generation of behaviorally relevant network oscillations. Among this heterogeneous neuronal population, somatostatin (SOM)-positive oriens-lacunosum moleculare (O-LM) interneurons are remarkable because they are tuned to operate at theta frequencies (6–10 Hz) in vitro and in vivo. Recent studies show that a high proportion of glutamatergic synapses that impinge on O-LM interneurons are mediated by kainate receptors (KA-Rs). In the present study, we thus tested the hypothesis that KA-Rs transmit afferent inputs in O-LM neurons during synaptic stimulation at theta frequency. We combined multibeam two-photon calcium imaging in hippocampal slices from SOM–enhanced green fluorescent protein (EGFP) mice, to record the activity of SOM cells as well as hundreds of neurons simultaneously, and targeted electrophysiological recordings and morphological analysis to describe the morphofunctional features of particular cells. We report that EGFP-positive O-LM neurons are the only subtype of interneuron that reliably follows synaptic stimulation of the alveus in the theta frequency range. Electrophysiological recordings revealed the crucial contribution of KA-Rs to the firing activity and to the glutamatergic response to theta stimuli in O-LM cells compared with other cell types. The reliable activation of O-LM cells in the theta frequency range did not simply result from the longer kinetics of KA-R-mediated postsynaptic events (EPSP_KA) but presumably from a specific interaction between EPSP_KA and their intrinsic active membrane properties. Such preferential processing of excitatory inputs via KA-Rs by distally projecting GABAergic microcircuits could provide a key role in theta band frequency oscillations.

Key words: kainate; O-LM; theta; imaging; interneuron; network

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Received Oct. 11, 2006; revised June 25, 2007; accepted June 26, 2007.

Correspondence should be addressed to Dr. Rosa Cossart, Institut de Neurobiologie de la Méditerranée, Inserm, Unité 29, Parc Scientifique de Luminy, Boîte Postale 13, 13273 Marseille cedex 9, France. Email: cossart{at}inmed.univ-mrs.fr

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