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The Journal of Neuroscience, February 1, 2006, 26(5):1465-1469; doi:10.1523/JNEUROSCI.4587-05.2006

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Brief Communications
Presynaptic, Activity-Dependent Modulation of Cannabinoid Type 1 Receptor-Mediated Inhibition of GABA Release

Csaba Földy,¹ Axel Neu,¹ Mathew V. Jones,² and Ivan Soltesz¹

¹Department of Anatomy and Neurobiology, University of California, Irvine, Irvine, California 92697-1280, and ²Department of Physiology, University of Wisconsin–Madison, Madison, Wisconsin 53706-1510

Correspondence should be addressed to Csaba Földy, Department of Anatomy and Neurobiology, University of California, Irvine, Irvine, CA 92697-1280. Email: cfoldy{at}uci.edu

Endocannabinoid signaling couples activity-dependent rises in postsynaptic Ca²⁺ levels to decreased presynaptic GABA release. Here, we present evidence from paired recording experiments that cannabinoid-mediated inhibition of GABA release depends on the firing rates of the presynaptic interneurons. Low-frequency action potentials in post hoc identified cholecystokinin-positive CA1 basket cells elicited IPSCs in the postsynaptic pyramidal cells that, as expected, were fully abolished by the exogenous application of the cannabinoid receptor agonist WIN55,212-2 [R-(+)-(2,3-dihydro-5-methyl-3-[(4-morpholinyl)methyl]pyrol[1,2,3-de]-1,4-benzoxazin-6-yl)(1-naphthalenyl) methanone monomethanesulfonate] at 5 µM. However, the presynaptic basket cells recovered from the cannabinoid agonist-induced inhibition of GABA release when the presynaptic firing rate was increased to 20 Hz. Pharmacological experiments showed that the recovered transmission was exclusively dependent on presynaptic N-type Ca²⁺ channels. Furthermore, the increased presynaptic firing could also overcome even complete depolarization-induced suppression of inhibition, indicating that the magnitude of DSI markedly depends on the activity levels of basket cells. These results reveal a new locus of activity-dependent modulation for endocannabinoid signaling and suggest that endocannabinoid-mediated inhibition of GABA release may differ in distinct behavioral states.

Key words: cannabinoid; IPSC; paired recording; plasticity; hippocampus; GABA

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Received Oct. 26, 2005; revised Dec. 20, 2005; accepted Dec. 21, 2005.

Correspondence should be addressed to Csaba Földy, Department of Anatomy and Neurobiology, University of California, Irvine, Irvine, CA 92697-1280. Email: cfoldy{at}uci.edu

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