Operant conditioning of head-waving in Aplysia. III. Cellular analysis of possible reinforcement pathways.

Operant conditioning of the head-waving response in Aplysia, as well as conditioning of the electrical activity of identified neck muscles, can be induced readily when bright light is used as aversive reinforcement (Cook and Carew, 1986, 1989b). A cellular analysis of this type of operant conditioning requires an understanding of the neural circuitry that underlies the reinforcement pathways involved in the conditioning. In the present paper we describe a cellular analysis of possible reinforcement pathways that mediate the aversive effects of bright light in the CNS of Aplysia. Using a semi-intact "split-body" preparation, we explored the effects of bright light on the operant response pathway by recording intracellularly from identified pedal neck and body wall motor neurons, which contribute to the operant response. In these experiments we identified 2 light-sensitive pathways. One pathway, from the eyes and rhinophores, mediated functional inhibition of light-induced excitation of pedal motor neurons. The other pathway, from the oral veil (cerebral ganglion nerves C1-C3) mediated significant excitation of the same motor cells. Randomly occurring blank trials ruled out the possibility that the light-induced effects were due to sampling bias. Finally, surgical isolation of the CNS from the periphery showed that none of the effects of light were due to direct illumination of central neurons. This identification of candidate reinforcement pathways will facilitate a cellular analysis of operant conditioning of head-waving in Aplysia.