Biophysical and Behavioral Correlates of Memory Storage, Degradation, and Reactivation

Neural correlates of associative memory and "forgetting" were observed 1, 6, and 14 days after acquisition of a conditioned response (CR) in the marine snail Hermissenda. Behavioral expression of a light-rotation association, as indexed by contraction of the animal's foot in response to light, dissipated throughout the 14-day interval such that a CR was observed 1 and 6 days after conditioning but was absent 14 days later. In relation to naive or pseudoconditioned animals, membrane resistance (inversely related to neuronal membrane conductance and directly related to excitability) of the isolated Type B photoreceptor (B cell) was elevated in conditioned animals on Days 1 and 6, whereas no elevation was detectable on Day 14. However, both the behavioral response and the elevated membrane resistance in conditioned animals were hypersensitive to light-rotation pairings (i.e., exhibited "savings") on Day 14, which is indicative of a latent memory trace. In a second experiment, a current-induced depolarization of the B cell after 14 retention days resulted in an increase in input resistance of the B cell membrane in previously conditioned animals but a weaker, transient rise in resistance in B cells from animals exposed to the nonassociative control procedure 14 days earlier. This effect was Ca²⁺-dependent because no rise in resistance was observed if Ca²⁺ was removed from the extracellular bath. These results indicate that modification of membrane conductance (i.e., elevated resistance), although apparently critical for the behavioral expression of the memory, is not essential for the maintenance of the latent memory trace, whereas Ca²⁺ hypersensitivity may be a principal contributor to the storage of a latent memory trace and memory reactivation.