Abstract
The effects of stress on memory are typically assessed individually; however, in reality different stressors are often experienced simultaneously. Here we determined the effect that two environmentally relevant stressors, crowding and low calcium availability, have on memory and neural activity following operant conditioning of aerial respiration in the pond snail, Lymnaea stagnalis. We measured aerial breathing behaviour and activity of a neuron necessary for memory formation, right pedal dorsal 1 (RPeD1), in the central pattern generator (CPG) that drives aerial respiration in untrained animals, and assessed how these traits changed following training. In naïve animals both crowding and combined stressors significantly depressed burst activity in RPeD1 which correlated with a depression in aerial breathing behaviour, whereas low calcium availability had no effect on RPeD1 activity. Following training, changes in burst activity in RPeD1 correlated with behavioural changes, decreasing relative to their naïve state at 3 h and 24 h in control conditions when both intermediate-term memory (ITM: 3 h) and long-term memory (LTM: 24 h) are formed, at 3 h but not 24 h when exposed to individual stressors when only ITM is formed, and did not change in combined stressors (i.e. when no memory is formed). Additionally, we also found that Lymnaea formed short-term memory (STM: 10 min) in the presence of individual stressors or under control conditions, but failed to do so in the presence of combined stressors. Our data demonstrate that by combining stressors that individually block LTM only we can block all memory processes. Therefore the effects of two stressors with similar individual affects on memory phenotype may be additive when experienced in combination.
Highlights
Memories shape the way in which an individual interacts with its environment
Electrophysiological activity of right pedal dorsal 1 (RPeD1) in naıve Lymnaea In naıve Lymnaea, RPeD1 activity did not differ between snails in control conditions and those exposed to low calcium stress alone (Figure 1) in agreement with previous findings [11]
We demonstrate that different forms of stress which produce a similar behavioural phenotype, i.e. blocking long-term memory (LTM) but not intermediate-term memory (ITM) or short-term memory (STM), differ in the way they affect activity of a neuron (RPeD1), known to be necessary for LTM formation [9,25]
Summary
Memories shape the way in which an individual interacts with its environment. Stress experienced before, during or following a period of learning can enhance or block memory formation depending on the nature of the stress [1,2]. Different stressors can have similar effects on memory phenotype; the way in which each of the stressors affects the central nervous system (CNS) may differ [3,4], and we cannot always make a priori predictions about how combining stressors will alter memory phenotype based on their individual effects [5]. We addressed whether the effect on memory following exposure to multiple forms of stress with identical individual effects on memory phenotype are additive when combined. We use operant conditioning of aerial respiration in Lymnaea to assess the effects of various stressors on memory formation at both the behavioural and individual neuron level (e.g. right pedal dorsal 1; RPeD1) [1,6].
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