Storage and erasure of behavioural experiences at the single neuron level

Abstract

Although predictions from the past about the future have been of major interest to current neuroscience, how past and present behavioral experience interacts at the level of a single neuron remains largely unknown. Using the pond snail Lymnaea stagnalis we found that recent experience of terrestrial locomotion (exercise) results in a long-term increase in the firing rate of serotonergic pedal (PeA) neurons. Isolation from the CNS preserved the “memory” about previous motor activity in the neurons even after the animals rested for two hours in deep water after the exercise. In contrast, in the CNS, no difference in the firing rate between the control and “exercise-rested” (ER) neurons was seen. ER snails, when placed again on a surface to exercise, nevertheless showed faster locomotor arousal. The difference in the firing rate between the control and ER isolated neurons disappeared when the neurons were placed in the microenvironment of their home ganglia. It is likely that an increased content of dopamine in the CNS masks an increased excitation of PeA neurons after rest: the dopamine receptor antagonist sulpiride produced sustained excitation in PeA neurons from ER snails but not in the control. Therefore, our data suggest the involvement of two mechanisms in the interplay of past and present experiences at the cellular level: intrinsic neuronal changes in the biophysical properties of the cell membrane and extrinsic modulatory environment of the ganglia.