Temporal order sensitivity of associative neural and behavioral changes in Hermissenda

Abstract

Hermissenda's neural and behavioral changes produced by light-rotation pairings were assessed as a function of the temporal relations between visual and vestibular stimulation. The results of in vitro simulations of conditioning indicated that simultaneous pairings (synchronous onsets and offsets of light and caudal hair cell stimulation) resulted in significantly greater cumulative depolarization of Type B photoreceptors than did either forward (light preceded hair cell stimulation) or backward (hair cell stimulation preceded light) pairings. Further experiments revealed that the attenuation of cumulative depolarization produced by the forward and backward pairings reflected the asynchrony of stimulus offsets that characterize these conditioning sequences, rather than their onsets. Analogous behavioral experiments revealed that intact animals trained with forward or backward pairings exhibited significantly less conditioning than those trained with simultaneous pairings. Strong parallels between the magnitude of cumulative depolarization from in vitro conditioning studies and the behavioral results for intact animals were also observed in experiments in which stimulus onset synchrony was held constant but offsets were made asynchronous, and vice versa. Thus Hermissenda exhibits a sensitivity to the temporal arrangement of light and rotation, and the results of behavioral conditioning can be predicted accurately from the outcome of in vitro conditioning of the isolated nervous system.