Identification of a reinforcement pathway necessary for operant conditioning of head waving in Aplysia californica

The marine mollusc Aplysia californica exhibits a wide range of nonassociative and associative forms of learning. Recently, we found that the learning repertoire of Aplysia includes operant conditioning (^{Cook & Carew, 1986, 1989b}). The behavior we examined is a naturally occurring, side-to-side head-waving response used by Aplysia in seeking food, obtaining a foothold, and egg laying. Aplysia can be operantly conditioned to reduce head-waving to one side of their body if such a response results in exposure to bright uniform-field illumination, which the animals find aversive. An essential step toward achieving a mechanistic understanding of operant conditioning is to identify and characterize the reinforcement pathway used during the learning. Toward this end, we wished to determine which of the peripheral visual pathways in Aplysia are critical for performance of the operant task. Previous experiments indicated that photic input from the optic and rhinophore nerves functionally inhibited motor neurons that participate in the operant response (head-waving), while photic input from the oral veil nerves excited these same motor neurons (^{Cook & Carew, 1989c}). These findings suggested the hypothesis that one or both of these pathways could play an important role in mediating reinforcement during training. To explore this possibility we operantly trained animals that had received chronic bilateral transections of either the optic and rhinophore nerves or the oral veil nerves C₁-C₃ (in conjunction with transection of the optic and rhinophore nerves). We found that operant conditioning was not disrupted by ablation of input from the eyes and rhinophores. By contrast, ablation of input from the oral veil (together with that from the eyes and rhinophores) abolished operant conditioning. Thus, the oral veil nerves play a critical modulatory role in operant conditioning of head-waving. This observation further suggested that photic input from the oral veil is conveyed to the CNS via the oral veil nerves. In a final experiment we confirmed that stimulation of the oral veil with light evokes increased afferent activity in the oral veil nerves C₁-C₂. These results support the idea that the oral veil nerves contain processes that are critical components of the reinforcement pathway for operant conditioning of head-waving.