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Presynaptic Inhibition of GABA_A Receptor-Mediated Unitary IPSPs by Cannabinoid Receptors at Synapses Between CCK-Positive Interneurons in Rat Hippocampus

Department of Pharmacology, University of London, School of Pharmacy, London, United Kingdom

Submitted 12 February 2007; accepted in final form 11 June 2007

There is growing evidence to link cholecystokinin (CCK)-positive interneurons and anxiety disorders. Despite this, little is known about the physiology and pharmacology of synaptic interactions between CCK-positive interneurons. This study aims to investigate the local circuit connections among CCK-positive Schaffer collateral associated (SCA) interneurons in stratum radiatum (SR) and their modulatory interactions using paired whole cell recordings combined with biocytin and double immunofluorescence labeling in slices of rat hippocampus. The cell bodies of SCA interneurons were located in SR, and their sparsely spiny dendrites projected toward s. pyramidale (SP) and along SR. Their axons innervated SR, SP, and s. oriens (SO) with predominant ramification in SR. These cells were immunopositive for CCK and immunonegative for parvalbumin (PV). SCA interneurons often displayed an accommodating firing pattern with or without a "sag" in response to hyperpolarizing current injection. Pairs of these cells exhibited electrical coupling and reciprocal chemical connections in which inhibitory postsynaptic potentials (IPSPs) displayed powerful frequency-dependent facilitation and augmentation. The synaptic connections were modulated by the endogenous cannabinoid receptor (CB) agonist, anandamide and by depolarization-induced suppression of inhibition (DSI), both of which reduced the amplitude of unitary IPSPs to 50% of control and increased the number of apparent failures of transmission. These effects were blocked by the CB1 receptor antagonist, AM-251. I suggest that synaptic facilitation between CCK-positive SCA interneurons may modify the onset of CB1 receptor-mediated regulation of inhibition, thereby affecting spike timing, and that this process could influence the expression of anxiety.

This article has been cited by other articles:

				M. Galarreta, F. Erdelyi, G. Szabo, and S. Hestrin Cannabinoid Sensitivity and Synaptic Properties of 2 GABAergic Networks in the Neocortex Cereb Cortex, January 17, 2008; (2008) bhm253v1. [Abstract] [Full Text] [PDF]

				F. Lemtiri-Chlieh and E. S. Levine Lack of Depolarization-Induced Suppression of Inhibition (DSI) in Layer 2/3 Interneurons That Receive Cannabinoid-Sensitive Inhibitory Inputs J Neurophysiol, November 1, 2007; 98(5): 2517 - 2524. [Abstract] [Full Text] [PDF]