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The Journal of Neuroscience, November 3, 2004, 24(44):9953-9961; doi:10.1523/JNEUROSCI.2134-04.2004
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Cellular/Molecular
Circuitry for Associative Plasticity in the Amygdala Involves Endocannabinoid Signaling
Shahnaz C. Azad,1,3 Krisztina Monory,2 Giovanni Marsicano,2 Benjamin F. Cravatt,4 Beat Lutz,2 Walter Zieglgänsberger,1 andGerhard Rammes1,5 1Clinical Neuropharmacology and 2Molecular Genetics of Behaviour, Max-Planck-Institute of Psychiatry, 80804 Munich, Germany, 3Department of Anaesthesiology, Ludwig-Maximilians-University, 81377 Munich, Germany, 4The Skaggs Institute for Chemical Biology and Department of Chemistry, The Scripps Research Institute, La Jolla, California 92037, and 5Department of Anaesthesiology, Technische Universität, 81675 Munich, Germany
Endocannabinoids are crucial for the extinction of aversive memories, a process that considerably involves the amygdala. Here, we show that low-frequency stimulation of afferents in the lateral amygdala with 100 pulses at 1 Hz releases endocannabinoids postsynaptically from neurons of the basolateral amygdala of mice in vitro and thereby induces a long-term depression of inhibitory GABAergic synaptic transmission (LTDi) via a presynaptic mechanism. Lowering inhibitory synaptic transmission significantly increases the amplitude of excitatory synaptic currents in principal neurons of the central nucleus, which is the main output site of the amygdala. LTDi involves a selective mGluR1 (metabotropic glutamate receptor 1)-mediated calcium-independent mechanism and the activation of the adenylyl cyclase-protein kinase A pathway. LTDi is abolished by the cannabinoid type 1 (CB1) receptor antagonist SR141716A and cannot be evoked in CB1 receptor-deficient animals. LTDi is significantly enhanced in mice lacking the anandamide-degrading enzyme fatty acid amide hydrolase. The present findings show for the first time that mGluR activation induces a retrograde endocannabinoid signaling via activation of the adenylyl cyclase-protein kinase A pathway and the release of anandamide. Furthermore, the results indicate that anandamide decreases the activity of inhibitory interneurons in the amygdala. This disinhibition increases the activity of common output neurons and could provide a prerequisite for extinction by formation of new memory.
Key words: endocannabinoids; amygdala; long-term depression; mGluR; anandamide; synaptic plasticity
Received March 2, 2004; revised August 22, 2004; accepted August 25, 2004.
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