Social snails: the effect of social isolation on cognition is dependent on environmental context

Dalesman, Sarah; Lukowiak, Ken

doi:10.1242/jeb.064857

Cited by 15 publications

(7 citation statements)

References 43 publications

(54 reference statements)

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“…Previous work has shown that combining stressors with differing effects on phenotype may not alter memory formation in a predictable manner [5]. For example, by combining low calcium (as used here) with social isolation, which alone had no effect on memory, low calcium no-longer had a blocking effect on memory [5].…”

Section: Discussionmentioning

confidence: 81%

“…For example, by combining low calcium (as used here) with social isolation, which alone had no effect on memory, low calcium no-longer had a blocking effect on memory [5]. This was thought due to a reduction in calcium requirements in isolated animals as their drive to mate in the male role is increased [35], potentially decreasing the calcium they require for egg-laying [36].…”

Section: Discussionmentioning

confidence: 99%

“…blocking all memory processes, which may be due to the animal simply experiencing too much stress to pay attention to training. This was thought to be the reason why combining three different potential stressors, isolation, low calcium and predator kairomones, blocked the ability of Lymnaea to form LTM [5]. Alternatively, it may be specific to the type of stress experienced.…”

Section: Discussionmentioning

confidence: 99%

“…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; however, the way in which each of the stressors affects the central nervous system (CNS) may differ [3], [4], and therefore we cannot always make a priori predictions about how combining stressors will alter memory phenotype based on their individual effects [5]. Typically, in the laboratory the effects of individual stressors are determined in isolation, but in ‘real life’ multiple forms of stress may be experienced simultaneously.…”

Section: Introductionmentioning

confidence: 99%

“…We predicted based on their effect on ‘smart’ strains that crowding and low calcium availability may differ in how they alter activity in RPeD1 despite producing an identical phenotypic effect on memory formation in the Dutch strain. The effects of combined stressors may not be easily predicted from their individual properties [5], so we also assessed whether combining these stressors would produce additive results, blocking earlier memory processes.…”

Section: Introductionmentioning

confidence: 99%

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Combining Stressors That Individually Impede Long-Term Memory Blocks All Memory Processes

et al. 2013

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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.

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Section: Discussionmentioning

confidence: 81%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Combining Stressors That Individually Impede Long-Term Memory Blocks All Memory Processes

et al. 2013

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Training Lymnaea in the presence of a predator scent results in a long-lasting ability to form enhanced long-term memory

et al. 2016

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Lymnaea exposed to crayfish effluent (CE) gain an enhanced ability to form long-term memory (LTM). We test the hypothesis that a single CE exposure and operant conditioning training leads to long lasting changes in the capability of snails to form LTM when tested in pond water four weeks later. We trained both juvenile and adult snails with a single 0.5 h training session in CE and show that LTM was present 24 h later. Snails trained in a similar manner in just pond water show no LTM. We then asked if such training in CE conferred enhanced memory forming capabilities on these snails four weeks later. That is, would LTM be formed in these snails four weeks later following a single 0.5 h training session in pond water? We found that both adult and juvenile snails previously trained in CE one month previously had enhanced LTM formation abilities. The injection of a DNA methylation blocker, 5-AZA, prior to training in adult snails blocked enhanced LTM formation four weeks later. Finally, this enhanced LTM forming ability was not passed on to the next generation of snails.

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Social context shapes cognitive abilities: associative memories are modulated by fight outcome and social isolation in the crab Neohelice granulata

et al. 2021

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Cognitive abilities of an animal can be influenced by distinct social experiences. However, the extent of this modulation has not been addressed in different learning scenarios: are all tasks similarly affected by social experiences? In the present study, we analyzed the effect of social dominance in aversive and appetitive memory processes in the crab Neohelice granulata . In addition, we studied the influence of social isolation on memory ability. Social dominance experiments consisted of an agonistic phase immediately followed by a memory phase. During the agonistic phase, matched pairs of male crabs were staged in 10-min encounters and the dominant or subordinate condition of each member of the dyad was determined. During the memory phase, crabs were trained to acquire aversive or appetitive memory and tested 24 h later. Results showed that the agonistic encounter can modulate long-term memory according to the dominance condition in such a way that memory retention of subordinates results higher than their respective dominant. Remarkably, this result was found for both aversive and appetitive memory tasks. In addition, we found that isolated animals showed no memory retention when compared with animals that remained grouped. Altogether this work emphasizes the importance of social context as a modulator of cognitive abilities. Supplementary Information The online version contains supplementary material available at 10.1007/s10071-021-01492-6.

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Social snails: the effect of social isolation on cognition is dependent on environmental context

Cited by 15 publications

References 43 publications

Combining Stressors That Individually Impede Long-Term Memory Blocks All Memory Processes

Combining Stressors That Individually Impede Long-Term Memory Blocks All Memory Processes

Training Lymnaea in the presence of a predator scent results in a long-lasting ability to form enhanced long-term memory

Social context shapes cognitive abilities: associative memories are modulated by fight outcome and social isolation in the crab Neohelice granulata

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