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1 School of Biomedical Sciences, Worsley Building, University of Leeds, Leeds LS2 9JT, UK
2
Johannes-Müller-Institute of Physiology at the charité, Humboldt University Berlin, Tucholskystr. 2, 10117 Berlin, Germany
3
University Hospital Neurology, Department of Clinical Neurobiology Im Neuenheimerfeld 364, Heidelberg D-69120, Germany
4
Department of Physiology and Pharmacology, SUNY Health Science Center, Brooklyn, NY 11203, USA
Abstract
Using whole-cell patch-clamp recordings in conjunction with post hoc anatomy we investigated the physiological properties of hippocampal stratum oriens and stratum pyramidale inhibitory interneurones, before and following the induction of pharmacologically evoked gamma frequency network oscillations. Prior to kainate-induced transient epochs of gamma activity, two distinct classes of oriens interneurones, oriens lacunosum-moleculare (O-LM) and trilaminar cells, showed prominent differences in their membrane and firing properties, as well as in the amplitude and kinetics of their excitatory postsynaptic events. In the active network both types of neurone received a phasic barrage of gamma frequency excitatory inputs but, due to their differential functional integration, showed clear differences in their output patterns. While O-LM cells fired intermittently at theta frequency, trilaminar interneurones discharged on every gamma cycle and showed a propensity to fire spike doublets. Two other classes of fast spiking interneurones, perisomatic targeting basket and bistratified cells, in the active network discharged predominantly single action potentials on every gamma cycle. Thus, within a locally excited network, O-LM cells are likely to provide a theta-frequency patterned output to distal dendritic segments, whereas basket and bistratified cells are involved in the generation of locally synchronous gamma band oscillations. The anatomy and output profile of trilaminar cells suggest they are involved in the projection of locally generated gamma rhythms to distal sites. Therefore a division of labour appears to exist whereby different frequencies and spatiotemporal properties of hippocampal rhythms are mediated by different interneurone subtypes.
(Received 31 July 2004;
accepted after revision 11 October 2004;
first published online 14 October 2004)
Corresponding author T. Gloveli: Johannes-Müller-Institut für Physiologie, Charité Universitätsmedizin Berlin, Tucholskystr. 2, 10117 Berlin, Germany. Email: tengis.gloveli{at}charite.de
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