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.

The Role of Serotonin in the Influence of Intense Locomotion on the Behavior Under Uncertainty in the Mollusk Lymnaea stagnalis

“…All values are given as median with the lower and upper quartiles * indicates p < 0.05. from the breeding stock (Kruskal-Wallis test: H (2, N = 91) = 7.5, p = 0.0234; Figure 2C, post hoc tests ER/Ch p = 0.020; ER/Cn p = 0.2; Ch/Cn p = 0.9). Recently, we reported that locomotor arousal developed more quickly in the ER snails than in the Cn group (Dyakonova et al, 2019). Similar trend can be seen in Figure 3D.…”

“…No measurable FIGURE 1 | Schematic representation of the experimental procedure. (A) Procedure for the investigation of the effects of enhanced motor activity (exercise, E, EE) and rest after exercise (ER), redrawn after (Korshunova et al, 2016;Dyakonova et al, 2019). In double-blind experiments, snails were divided into control and experimental groups and resided in similar light conditions before being placed in the test arena.…”

“…We measured the levels of 5-HTP, 5-HT, Nac-5-HT, and 5-HIAA in the in the pedal and cerebral ganglia. The pedal ganglia contain neurons related to locomotion, including the serotonergic PeA cluster, whose activity is influenced by intense locomotion (Korshunova et al, 2016;Dyakonova et al, 2019). The cerebral ganglia were included in the analysis for two reasons: first, to verify the hypothesis that serotonin metabolism in the functionally distinct parts of the CNS can be differently affected by the same behavioral context; second, to check whether the exercise produces any changes in the serotonin metabolism within the "cognitive" (cerebral) ganglia of the snail CNS that are believed to participate in learning, memory and decision-making.…”

“…Many of the above-mentioned behavioral effects of exercise are similar to the influences ascribed to the increased level of serotonin in Lymnaea. Therefore, we hypothesized that the increased activity of these neurons is required for intense locomotion (Dyakonova et al, 2019) and that enhanced extrasynaptic release of serotonin may underlie the behavioral changes observed after the motor load.…”

Effects of Thryptophan Hydroxylase Blockade by P-Chlorophenylalanine on Contextual Memory Reconsolidation after Training of Different Intensity

“…Reconsolidation of a contextual memory has been shown in invertebrate animals [49,[56][57][58][59][60][61]. The investigation of the memory formation process and memory reconsolidation in mollusks is also attractive due to the possibility of investigate the correlations between memory mechanisms and changes occurs at the cellular and receptor level [40,[62][63][64][65][66][67][68][69][70][71][72][73][74][75].…”