Contingency learning and causal detection in Hermissenda: II. Cellular mechanisms

Neural correlates of contingency-sensitive behavioral changes in the nudibranch Hermissenda were studied by in vitro conditioning of the isolated nervous system. The additions of unpaired light-alone or hair cell-alone stimulation presentations to sequences of light-hair cell stimulation pairings were found to attenuate the cumulative depolarization of Type B photoreceptors that normally result from pairings. Unpaired light presentations produced a transitory depression of the light-induced depolarizing generator potential of the B cell. Unpaired hair cell stimulation synaptically hyperpolarized the B photoreceptor and thus acted in a retroactive manner to partially reverse the cumulative depolarization owing to prior pairings. Behavioral experiments revealed a striking temporal specificity for the decremental effects of added light and rotational stimulation. The present experiments indicate that contiguity and contingency relations are both encoded and stored in the Type B photoreceptors, and to a first approximation reflect similar biophysical mechanisms.