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The Journal of Neuroscience, February 28, 2007, 27(9):2403-2409; doi:10.1523/JNEUROSCI.2916-06.2007

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Development/Plasticity/Repair
Anandamide Regulates Postnatal Development of Long-Term Synaptic Plasticity in the Rat Dorsolateral Striatum

Kristen K. Ade¹ and David M. Lovinger²

¹Department of Physiology and Biophysics, Georgetown University School of Medicine, Washington, DC 20007, and ²Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, Maryland 20892

Correspondence should be addressed to David M. Lovinger, Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism–National Institutes of Health, 5625 Fishers Lane, TS-13, Bethesda, MD 20892.

Long-term changes in synaptic efficacy produced by high-frequency stimulation (HFS) of glutamatergic afferents to the rat dorsolateral striatum exhibit heterogeneity during early stages of postnatal development. Whereas HFS most often induces striatal long-term potentiation (LTP) in rats postnatal day 12 (P12)–P14, the same stimulation tends to induce long-term depression (LTD) at ages P16–P34. Previous studies have shown that striatal LTD induction depends on retrograde endocannabinoid signaling and activation of the CB1 cannabinoid receptor. It is also known that levels of one of the primary endogenous CB1 receptor agonists, anandamide (AEA), increases during development in whole-brain samples. In the present study, we sought to determine whether this developmental increase in AEA also takes place in striatal tissue and whether increased AEA levels contribute to the postnatal switch in the response to HFS. We observed a pronounced increase in striatal levels of AEA, but not the other major endogenous cannabinoid 2-arachidonoylglycerol (2-AG), during the postnatal period characterized by the switch from LTP to LTD. Furthermore, application of synthetic AEA during HFS in field recordings of slices from P12–P14 rats allowed for induction of LTD whereas blocking the CB1 receptor during HFS in animals P16–P34 resulted in expression of LTP. However, blocking 2-AG synthesis with the DAG-lipase inhibitor tetrahydrolipstatin did not alter HFS-induced striatal LTD. In addition, synaptic depression produced by a synthetic CB1 agonist was similar across development. Together, these findings suggest that the robust developmental increase in striatal AEA may be the key factor in the emergence of HFS-induced striatal LTD.

Key words: endocannabinoid; basal ganglia; long-term depression; LTD; long-term potentiation; LTP; glutamate; development

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Received July 10, 2006; revised Jan. 28, 2007; accepted Jan. 29, 2007.

Correspondence should be addressed to David M. Lovinger, Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism–National Institutes of Health, 5625 Fishers Lane, TS-13, Bethesda, MD 20892.

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