In the previous report (Bristol et al. 2003), we observed that tail shock-induced sensitization of tail-elicited siphon withdrawal reflex (TSW) of Aplysia was expressed ipsilaterally, but that dishabituation induced by an identical tail shock was expressed bilaterally. Here we examined the mechanisms of this differential lateralization. We first isolated the modulatory pathway responsible for the induction of contralateral dishabituation by making selective nerve cuts. We found that an intact pleural-abdominal connective, the descending pathway connecting the ring ganglia with the abdominal ganglion, ipsilateral to the shock was required for contralateral dishabituation. We examined whether network inhibition suppresses the contralateral effects of tail shock in non-habituated preparations. We found that blockade of inhibitory transmission in the CNS by the nicotinic Ach inhibitor d-tubocurarine (d-TC) rendered tail shock capable of inducing bilateral sensitization. We next asked whether serotonin (5HT), a neuromodulator released in the CNS in response to tail shock, was affected by d-TC. We found that d-TC does not alter 5HT processes in the ring ganglia: (1) it had no effect on the lateralized pattern of tail nerve shock-induced changes in tail sensory neuron excitability, a 5HT-dependent process, and (2) it did not alter tail nerve shock-evoked release of 5HT. By contrast, d-TC enhanced 5HT release in the abdominal ganglion. Consistent with this observation, restricting d-TC to the abdominal ganglion rendered tail nerve shock capable of producing bilateral sensitization. Together with the results of the preceding paper, our results suggest a model in which TSW sensitization and dishabituation can be dissociated both anatomically and mechanistically.