Neurophysiological substrates of context conditioning in Hermissenda suggest a temporally invariant form of activity-dependent neuronal facilitation

The neurophysiological basis for context conditioning is conceptually probl ematic because neurophysiological descriptions of activity-dependent (assoc iative) forms of neuronal plasticity uniformly assume that a specific tempo ral relationship between signals is necessary for memory induction. In the present experiments, this problem is addressed empirically by presenting, a s a temporally diffuse contextual signal, a stimulus that results in known neural modifications following punctate (temporally contiguous) pairings wi th an aversive unconditioned stimulus. Hermissenda were trained to discrimi nate between adjoining contexts that were distinguished only in that one wa s lit and one was dark. Thirty unsignaled rotations were presented during e ach of three 15-min sessions in one of the two (lit or dark) contexts. Prio r to training, animals displayed a slight preference for the lit context. A fter exposure to unsignaled rotation, animal's preferences shifted strongly to the dark context if unsignaled rotations were presented in the light, a nd tended (nonsignificantly) to the lit context if unsignaled rotations wer e presented in the dark. The B photoreceptors of the Hermissenda eye underg o several forms of activity-dependent facilitation (e.g., an increase in ne uronal input resistance and evoked spike frequency) following pairings of p unctate light (CS) and presynaptic vestibular stimulation (US). Similar fac ilitation in the B photoreceptor was observed following in vitro training t hat mimicked context conditioning in which presynaptic vestibular stimulati on was presented repetitively during a continuous 7.5-min light. Subsequent ly, Ca2+-imaging experiments were conducted with Fura-2AM. It was determine d that intracellular Ca2+ the CS-induced second messenger critical for the induction of activity-dependent facilitation, was elevated in the B photore ceptor throughout the 7.5-min light presentation. These results indicate th at activity-dependent facilitation within similar neural structures can und erlie learning about both temporally diffuse contextual stimuli and tempora lly punctate CS-US pairings. These results suggest that a common mechanism may underlie learning about diffuse contextual stimuli as well as punctate- conditioned stimuli, provided that the stimuli are processed similarly in e ach type of conditioning arrangement. Consequently, the expression of diffe rent responses to contextual and discrete stimuli are likely to reflect a h igher property of the neural network, and do not necessarily arise from uni que underlying mechanisms. (C) 1999 Academic Press.