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The Journal of Neuroscience, November 24, 2004, 24(47):10707-10715; doi:10.1523/JNEUROSCI.3502-04.2004
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Cellular/Molecular
Prefrontal Cortex Stimulation Induces 2-Arachidonoyl-Glycerol-Mediated Suppression of Excitation in Dopamine Neurons
Miriam Melis,1,2 * Simona Perra,1,2 * Anna Lisa Muntoni,1,3 Giuliano Pillolla,1,2 Beat Lutz,4 Giovanni Marsicano,4 Vincenzo Di Marzo,5 Gian Luigi Gessa,1,2 andMarco Pistis1,2 1Center of Excellence "Neurobiology of Addiction," 2"B. B. Brodie" Department of Neuroscience, and 3Consiglio Nazionale delle Ricerche (CNR) Institute of Neuroscience, University of Cagliari, 09042 Monserrato (CA), Italy, 4Group Molecular Genetics of Behavior, Max Planck Institute of Psychiatry, 80804 Munich, Germany, and 5CNR Endocannabinoid Research Group, Institute of Biomolecular Chemistry, 80078 Pozzuoli, Italy
Endocannabinoids form a novel class of retrograde messengers that modulate short- and long-term synaptic plasticity. Depolarization-induced suppression of excitation (DSE) and inhibition (DSI) are the best characterized transient forms of endocannabinoid-mediated synaptic modulation. Stimulation protocols consisting of long-lasting voltage steps to the postsynaptic cell are routinely used to evoke DSE-DSI. Little is known, however, about more physiological conditions under which these molecules are released in vitro. Moreover, the occurrence in vivo of such forms of endocannabinoid-mediated modulation is still controversial. Here we show that physiologically relevant patterns of synaptic activity induce a transient suppression of excitatory transmission onto dopamine neurons in vitro. Accordingly, in vivo endocannabinoids depress the increase in firing and bursting activity evoked in dopamine neurons by prefrontal cortex stimulation. This phenomenon is selectively mediated by the endocannabinoid 2-arachidonoyl-glycerol (2-AG), which activates presynaptic cannabinoid type 1 receptors. 2-AG synthesis involves activation of metabotropic glutamate receptors and Ca2+ mobilization from intracellular stores. These findings indicate that dopamine neurons release 2-AG to shape afferent activity and ultimately their own firing pattern. This novel endocannabinoid-mediated self-regulatory role of dopamine neurons may bear relevance in the pathogenesis of neuropsychiatric disorders such as schizophrenia and addiction.
Key words: CB1; dopamine; endocannabinoid; excitatory transmission; midbrain; retrograde signal
Received Aug 25, 2004; revised October 7, 2004; accepted October 12, 2004.
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