Intermediate and long-term memory are different at the neuronal level in Lymnaea stagnalis (L.)

Abstract

Both intermediate-term memory (ITM) and long-term memory (LTM) require novel protein synthesis; however, LTM also requires gene transcription. This suggests that the behavioural output of the two processes may be produced differently at the neuronal level. The fresh-water snail, Lymnaea stagnalis, can be operantly conditioned to decrease its rate of aerial respiration and, depending on the training procedure, the memory can last 3h (ITM) or >24h (LTM). RPeD1, one of the 3 interneurons that form the respiratory central pattern generator (CPG) that drives aerial respiration, is necessary for memory formation. By comparing RPeD1’s electrophysiological properties in naïve, ‘ITM-trained’, ‘LTM-trained’ and yoked control snails we discovered that while the behavioural phenotype of memory at 3 and 24h is identical, the situation at the neuronal level is different. When examined 3h after either the ‘ITM’ or ‘LTM’ training procedure RPeD1 activity is significantly depressed. That is, the firing rate, input resistance, excitability and the number of action potential bursts are all significantly decreased. In snails receiving the ITM-training, these changes return to normal 24h post-training. However, in snails receiving the ‘LTM-training’, measured RPeD1 properties (firing rate, excitability, membrane resistance, and the number of action potential bursts fired) are significantly different at 24h than they were at 3h. Additionally, 24h following LTM training RPeD1 appears to be functionally “uncoupled” from its control of the pneumostome as the link between RPeD1 excitation and pneumostome opening is weakened. These data suggest that the behavioural changes occurring during LTM are due to more widespread neuronal reorganization than similar behavioural changes occurring during ITM. Thus ITM and LTM are not just distinct in a chronological and transcriptional manner but are also distinct at the level of neuronal properties.