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The Journal of Neuroscience, September 30, 2009, 29(39):12244-12254; doi:10.1523/JNEUROSCI.1970-09.2009

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Behavioral/Systems/Cognitive
Involvement of Actin Rearrangements within the Amygdala and the Dorsal Hippocampus in Aversive Memories of Drug Withdrawal in Acute Morphine-Dependent Rats

Yuan-Yuan Hou, Bin Lu, Mu Li, Yao Liu, Jie Chen, Zhi-Qiang Chi, and Jing-Gen Liu

State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China

Correspondence should be addressed to Jing-Gen Liu, State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China. Email: jgliu{at}mail.shcnc.ac.cn

Aversive memories of drug withdrawal can generate a motivational state leading to compulsive drug taking. Changes in synaptic plasticity may be involved in the formation of aversive memories. Dynamic rearrangement of the cytoskeletal actin, a major structural component of the dendritic spine, regulates synaptic plasticity. Here, the potential involvement of actin rearrangements in the induction of aversive memories of morphine withdrawal was examined. We found that lesions of the amygdala or dorsal hippocampus (DH) but not nucleus accumbens (NAc) impaired conditioned place aversion (CPA) of acute morphine-dependent rats. Accordingly, conditioned morphine withdrawal induced actin rearrangements in the amygdala and the DH but not in the NAc. In addition, we found that conditioned morphine withdrawal also increased activity-regulated cytoskeletal-associated protein (Arc) expression in the amygdala but not in the DH, although actin rearrangements were observed in both areas. We further found that inhibition of actin rearrangements by intra-amygdala or intra-DH injections of latrunculin A, an inhibitor of actin polymerization, significantly attenuated CPA. Furthermore, we found that manipulation of amygdala β-adrenoceptor activity by its antagonist propranolol and agonist clenbuterol differentially altered actin rearrangements in the DH. Therefore, our findings reveal that actin rearrangements in the amygdala and the DH are required for the acquisition and consolidation of the aversive memories of drug withdrawal and that the β-noradrenergic system within the amygdala modulates aversive memory consolidation by regulating actin rearrangements but not Arc protein expression in the DH, which is distinct from its role in modulation of inhibitory avoidance memory.

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Received April 26, 2009; revised June 2, 2009; accepted Aug. 11, 2009.

Correspondence should be addressed to Jing-Gen Liu, State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China. Email: jgliu{at}mail.shcnc.ac.cn

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