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The Journal of Neuroscience, March 21, 2007, 27(12):3111-3119; doi:10.1523/JNEUROSCI.3908-06.2007

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Cellular/Molecular
5-Hydroxytryptamine Induces a Protein Kinase A/Mitogen-Activated Protein Kinase-Mediated and Macromolecular Synthesis-Dependent Late Phase of Long-Term Potentiation in the Amygdala

Yan-You Huang² and Eric R. Kandel^1,2,3,4

¹Kavli Institute for Brain Science, ²Center for Neurobiology and Behavior of the College of Physicians and Surgeons of Columbia University, ³New York State Psychiatric Institute, and ⁴Howard Hughes Medical Institute, Columbia University, New York, New York 10032

Correspondence should be addressed to Eric R. Kandel, Columbia University, 722 West 168th Street, New York, NY 10032. Email: ERK5{at}columbia.edu

The amygdala is a critical site for the acquisition of learned fear memory in mammals, and the formation and long-term maintenance of fear memories are thought to be associated with changes of synaptic strength in the amygdala. Here we report that serotonin (5-hydroxytryptamine; 5-HT), a modulatory neurotransmitter known to be linked to learned fearful and emotional behavior, has dual effects on excitatory synaptic transmission in the basolateral amygdala. There is an early depression of synaptic transmission lasting 30–50 min, mediated by 5-HT_1A, and a late, long-lasting facilitation lasting >5 h in slice recordings, mediated by the 5-HT₄ receptor. 5-HT late phase long-term potentiation (L-LTP) is blocked by inhibitors of either protein kinase A (PKA) and/or mitogen-activated kinase (MAPK) and requires new protein synthesis and gene transcription. Moreover, the 5-HT-induced L-LTP in neurons of amygdala is blocked by the actin inhibitor cytochalasin D, suggesting that 5-HT stimulates a cytoskeletal rearrangement. These results show, for the first time, that 5-HT can produce long-lasting facilitation of synaptic transmission in the amygdala and provides evidence for the possible synaptic role of 5-HT in long-term memory for learned fear.

Key words: serotonin; amygdala; protein; protein kinase; cytoskeleton; L-LTP

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Received Sept. 8, 2006; revised Jan. 30, 2007; accepted Jan. 30, 2007.

Correspondence should be addressed to Eric R. Kandel, Columbia University, 722 West 168th Street, New York, NY 10032. Email: ERK5{at}columbia.edu

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