Heat stress enhances LTM formation in<i>Lymnaea</i>: role of HSPs and DNA methylation

Sunada, Hiroshi; Riaz, Hamza; Freitas, Emily de; Lukowiak, Ken; Swinton, Cayley; Swinton, Erin; Protheroe, Amy; Shymansky, Tamila; Komatsuzaki, Yoshimasa

doi:10.1242/jeb.134296

Cited by 42 publications

(35 citation statements)

References 44 publications

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“…After 1 h at 30°C, the snails were trained using the standard operant conditioning procedure, in room-temperature pond water (∼20°C). This procedure is consistent with previous thermal stress protocols used in operant conditioning of L. stagnalis (Foster et al, 2015;Sunada et al, 2016).…”

Section: Thermalsupporting

confidence: 87%

“…In previous studies, it was shown that a 1 h exposure to 30°C pond water 1 h before training results in enhancement of memory in 'average' Dutch snails (Teskey et al, 2012;Sunada et al, 2016). Thus, a single 0.5 h training session is now sufficient for LTM memory formation.…”

Section: Thermal Stressmentioning

confidence: 91%

“…For example, snails may experience temperatures close to freezing during an autumn night and temperatures close to 30°C during a warm summer day (Brown, 1979; K.L., personal observations). Thus, in L. stagnalis, temperature acts as an environmentally relevant stressor that affects memory formation (Teskey et al, 2012;Foster et al, 2015;Sunada et al, 2016).…”

Section: Thermalmentioning

confidence: 99%

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Strain-specific differences of the effects of stress on memory in Lymnaea

Hughes

Shymansky

Swinton

et al. 2017

Journal of Experimental Biology

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Stress alters the ability to form, recall and maintain memory according to the Yerkes-Dodson/Hebb (YDH) law. The effects of environmentally relevant stressors, such as low environmental calcium and crowding, on learning and memory have previously been described in a laboratory-reared 'average' strain of Lymnaea stagnalis (i.e. the Dutch strain) as well as two strains of freshly collected L. stagnalis with enhanced memory formation abilities (i.e. 'smart' snails). Here, we use L. stagnalis to study the effects of other environmentally relevant stressors on memory formation in two other strains of freshly collected snails, one 'smart' and one 'average'. The stressors we examined are thermal, resource restriction combined with food odour, predator detection and, for the first time, tissue injury (shell damage). We show that the same stressor has significantly different effects on memory formation depending on whether snails are 'smart' or 'average'. Specifically, our data suggest that a stressor or a combination of stressors act to enhance memory in 'average' snails but obstruct memory formation in 'smart' snails. These results are consistent with the YDH law and our hypothesis that 'smart' snails are more easily stressed than 'average' snails.

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Section: Thermalsupporting

confidence: 87%

Section: Thermal Stressmentioning

confidence: 91%

Section: Thermalmentioning

confidence: 99%

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Strain-specific differences of the effects of stress on memory in Lymnaea

Hughes

Shymansky

Swinton

et al. 2017

Journal of Experimental Biology

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“…It has previously been demonstrated that impairing DNA methylation one hour before exposure to a thermal stress, obstructs memory enhancement in Lymnaea 10 . In this study, we aimed to examine whether memory enhancement would still be impaired when DNA methylation was blocked 24 hours before this same stress exposure.…”

Section: Resultsmentioning

confidence: 94%

Impairing DNA methylation obstructs memory enhancement for at least 24 hours inLymnaea

Rothwell

Lukowiak

2017

Communicative & Integrative Biology

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Stressor-induced memory enhancement has previously been shown to involve DNA methylation in the mollusc Lymnaea stagnalis. Specifically, injection of the DNA methylation inhibitor 5-AZA one hour before exposure to a memory-enhancing stressor obstructs memory augmentation. However, the duration of the influence of 5-AZA on this memory enhancement has not yet been examined. In this study, 2 memory-enhancing stressors (a thermal stress and exposure to the scent of a predator) were used to examine whether injection of the DNA methylation inhibitor 5-AZA 24 hours before stress exposure would still impair memory enhancement. Indeed, it was observed that memory is still obstructed when 5-AZA is injected 24 hours before exposure to either of these stressors in Lymnaea. Understanding that 5-AZA still effectively impairs memory enhancement after a period of 24 hours is valuable because it indicates that experimental manipulations do not need to be made within one hour after the injection of this DNA methylation inhibitor and can instead be made within one day (i.e. 24 hours). These results will allow for a future examination of the possible involvement of DNA methylation in memory enhancement related to longer-term stressors or environmental changes. This study further elucidates the involvement of epigenetic changes in memory enhancement in Lymnaea, providing insight into the process of memory formation in this mollusc.

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“…4 weeks later) form LTM following a single 0.5 h training session. The Forest et al (2016) study as well as a study by Sunada et al (2016) showed that the long-lasting changes in the nervous system brought about by predator detection or other stressors are the result of epigenetic changes.…”

Section: Introductionmentioning

confidence: 99%

Juveniles ofLymnaeasmart snails do not perseverate and have the capacity to form LTM

Shymansky

Protheroe

Hughes

et al. 2016

Journal of Experimental Biology

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Previously, it was concluded that the nervous systems of juvenile snails were not capable of mediating long-term memory (LTM). However, exposure and training of those juvenile snails in the presence of a predator cue significantly altered their ability to learn and form LTM. In addition, there are some strains of Lymnaea which have been identified as 'smart'. These snails form LTM significantly better than the lab-bred strain. Here, we show that juveniles of two smart snail strains not only are capable of associative learning but also have the capacity to form LTM following a single 0.5 h training session. We also show that freshly collected 'wild' 'average' juveniles are also not able to form LTM. Thus, the smart snail phenotype in these strains is expressed in juveniles.

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Heat stress enhances LTM formation inLymnaea: role of HSPs and DNA methylation

Cited by 42 publications

References 44 publications

Strain-specific differences of the effects of stress on memory in Lymnaea

Strain-specific differences of the effects of stress on memory in Lymnaea

Impairing DNA methylation obstructs memory enhancement for at least 24 hours inLymnaea

Juveniles ofLymnaeasmart snails do not perseverate and have the capacity to form LTM

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