Neural circuit of tail-elicited siphon withdrawal in Aplysia. I. Differential lateralization of sensitization and dishabituation.

The tail-elicited siphon withdrawal reflex (TSW) has been a useful preparation in which to study learning and memory in Aplysia. However, comparatively little is known about the neural circuitry that translates tail sensory input (via the P9 nerves to the pleural ganglion) to final reflex output by siphon motor neurons (MNs) in the abdominal ganglion. To address this question, we examined the functional architecture of the TSW circuit by selectively severing nerves of semi-intact preparations and recording either tail-evoked responses in the siphon MNs or measuring siphon withdrawal responses directly. We found that the neural circuit underlying TSW is functionally lateralized. We next tested whether the expression of learning in the TSW reflects the underlying circuit architecture and shows side-specificity. We tested behavioral and physiological correlates of three forms of learning: sensitization, habituation, and dishabituation. Consistent with the circuit architecture, we found that sensitization and habituation of TSW are expressed in a side-specific manner. Unexpectedly, we found that dishabituation was expressed bilaterally, suggesting that a modulatory pathway bridges the two (ipsilateral) input pathways of the circuit, but this path is only revealed for a specific form of learning, dishabituation. These results suggest that the effects of a descending modulatory signal are differentially "gated" during sensitization and dishabituation.