In Aplysia, serotonergic neurons are widely activated during sensitization training, but the effects of exogenous serotonin (5-HT) on reflex circuits vary, inducing short- or long-term synaptic facilitation or synaptic inhibition, depending on the site of application. During learning, it is possible that specific spatial patterns of 5-HT release evoked by training may produce different phases of sensitization or behavioral inhibition. To test this hypothesis, we examined the modulation of the tail-induced siphon withdrawal reflex by repeated noxious stimuli applied to one of three sites: the (1) ipsilateral or (2) contralateral sides of the tail or (3) the head. Ipsilateral tail shock produced long-term sensitization, whereas contralateral tail shock induced only short-term sensitization, and head shock produced inhibition. In parallel cellular experiments, tail-nerve shock evoked large 5-HT release localized around the ipsilateral tail sensory neurons (SNs) and motor neurons (MNs) but only modest 5-HT release in the contralateral pleural-pedal ganglia and in the abdominal ganglion, in which the siphon MNs are located. Head-nerve shock, in contrast, produced only modest 5-HT release in the pleural, pedal, and abdominal ganglia. Thus, each training protocol evoked a specific pattern of 5-HT release within the CNS. In addition, we found that 5-HT released in the pleural ganglia was correlated with facilitation of SN-MN synapses; however, in the abdominal ganglion, it was associated with inhibition of the synapses between identified interneurons (L29s) and siphon MNs (LFSs). Because 5-HT differentially modulates synaptic efficacy at different synaptic sites, our data can explain how specific spatial patterns of 5-HT release in local modulatory fields can contribute to the induction of short- or long-term sensitization or to behavioral inhibition.
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