Latent memory facilitates relearning through molecular signaling mechanisms that are distinct from original learning

Menges, Steven; Riepe, Joshua R.; Philips, Gary T.

doi:10.1016/j.nlm.2015.04.013

Cited by 9 publications

(7 citation statements)

References 44 publications

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“…Animals were trained with four TSs (120 mA for 1.5 sec, ITI ¼ 10 min), and then the central nervous system chamber, which contains the tail sensory neurons, was exposed to U0126 or U0124 (20 mM) for 3 h. This duration was chosen because it represents the time period during which post-training MAPK activation is sustained in tail SNs (Sharma et al 2003b). Importantly, previous work has shown that U0126 treatment does not disrupt baseline responding as assessed for up to 20 h after treatment (Sharma et al 2003b;Menges et al 2015). After training and drug incubation, the preparations were tested the next day (18-20 h) for LTM.…”

Section: Ltm Requires Mapk Activity During Consolidationmentioning

confidence: 99%

“…Thus, we examined, in turn, whether persistent MAPK activation required translation and transcription. Ring ganglia were preincubated with the general protein synthesis inhibitor emetine (100 mM; Sutton et al 2001;Menges et al 2015) or vehicle (ASW) for 1 h and then trained (four tail-nerve shocks, ITI ¼ 10 min) in the presence of drug. We harvested sensory neuron clusters at either 5 min or 1 h post-training.…”

Section: Sustained But Not Immediate Post-training Mapk Activation mentioning

confidence: 99%

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Transforming growth factor β recruits persistent MAPK signaling to regulate long-term memory consolidation in Aplysia californica

2016

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In this study, we explore the mechanistic relationship between growth factor signaling and kinase activity that supports the protein synthesis-dependent phase of long-term memory (LTM) consolidation for sensitization of Aplysia. Specifically, we examine LTM for tail shock-induced sensitization of the tail-elicited siphon withdrawal (T-SW) reflex, a form of memory that requires both (i) extracellular signal-regulated kinase (ERK1/2; MAPK) activity within identified sensory neurons (SNs) that mediate the T-SW and (ii) the activation of transforming growth factor b (TGFb) signaling. We now report that repeated tail shocks that induce intermediate-term (ITM) and LTM for sensitization, also induce a sustained post-training phase of MAPK activity in SNs (lasting at least 1 h). We identified two mechanistically distinct phases of post-training MAPK: (i) an immediate phase that does not require ongoing protein synthesis or TGFb signaling, and (ii) a sustained phase that requires both protein synthesis and extracellular TGFb signaling. We find that LTM consolidation requires sustained MAPK, and is disrupted by inhibitors of protein synthesis and TGFb signaling during the consolidation window. These results provide strong evidence that TGFb signaling sustains MAPK activity as an essential mechanistic step for LTM consolidation.

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Section: Ltm Requires Mapk Activity During Consolidationmentioning

confidence: 99%

Section: Sustained But Not Immediate Post-training Mapk Activation mentioning

confidence: 99%

Transforming growth factor β recruits persistent MAPK signaling to regulate long-term memory consolidation in Aplysia californica

2016

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“…Savings is when a memory that seems completely forgotten (via recall tests) can nevertheless be re-acquired more rapidly or easily, indicating that some aspect of the original memory persisted. Savings has been documented across a wide range of learning tasks (Nelson, 1985) and species (Antzoulatos, Wainwright, Cleary, & Byrne, 2006; Menges, Riepe, & Philips, 2015; Philips, Tzvetkova, Marinesco, & Carew, 2006). Similarly, reminders and contextual cues can rescue recall not only from time-dependent forgetting but also from amnestic interventions such as electroconvulsive shock and the disruption of protein synthesis (reviewed in Riccio & Richardson, 1984).…”

Section: Introductionmentioning

confidence: 99%

Transcriptional changes before and after forgetting of a long-term sensitization memory in Aplysia californica

Patel

Perez

Farrell

et al. 2018

Neurobiology of Learning and Memory

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Most long-term memories are forgotten, becoming progressively less likely to be recalled. Still, some memory fragments may persist, as savings memory (easier relearning) can be detected long after recall has become impossible. What happens to a memory trace during forgetting that makes it inaccessible for recall and yet still effective to spark easier re-learning? We are addressing this question by tracking the transcriptional changes that accompany learning and then forgetting of a long-term sensitization memory in the tail-elicited siphon withdrawal reflex of Aplysia californica. First, we tracked savings memory. We found that even though recall of sensitization fades completely within 1 week of training, savings memory is still detectable at 2 weeks post training. Next, we tracked the time-course of regulation of 11 transcripts we previously identified as potentially being regulated after recall has become impossible. Remarkably, 3 transcripts still show strong regulation 2 weeks after training and an additional 4 are regulated for at least 1 week. These long-lasting changes in gene expression always begin early in the memory process, within 1 day of training. We present a synthesis of our results tracking gene expression changes accompanying sensitization and provide a testable model of how sensitization memory is forgotten.

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“…He found that it always took less training to re-learn the lists compared with the original acquisition. Since that pioneering demonstration, savings memory has been demonstrated with multiple learning paradigms ( Nelson, 1985 ) and in a variety of species ( Antzoulatos et al, 2006 ; Philips et al, 2006 ; Menges et al, 2015 ), suggesting that it is a core feature of long-term memory.…”

Section: Introductionmentioning

confidence: 99%

Registered Report: Transcriptional Analysis of Savings Memory Suggests Forgetting is Due to Retrieval Failure

Rosiles

Nguyen

Duron

et al. 2020

eNeuro

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There is fundamental debate about the nature of forgetting: some have argued that it represents the decay of the memory trace, others that the memory trace persists but becomes inaccessible because of retrieval failure. These different accounts of forgetting lead to different predictions about savings memory, the rapid re-learning of seemingly forgotten information. If forgetting is because of decay, then savings requires re-encoding and should thus involve the same mechanisms as initial learning. If forgetting is because of retrieval failure, then savings should be mechanistically distinct from encoding. In this registered report, we conducted a preregistered and rigorous test between these accounts of forgetting. Specifically, we used microarray to characterize the transcriptional correlates of a new memory (1 d after training), a forgotten memory (8 d after training), and a savings memory (8 d after training but with a reminder on day 7 to evoke a long-term savings memory) for sensitization in Aplysia californica ( n = 8 samples/group). We found that the reactivation of sensitization during savings does not involve a substantial transcriptional response. Thus, savings is transcriptionally distinct relative to a newer (1-d-old) memory, with no coregulated transcripts, negligible similarity in regulation-ranked ordering of transcripts, and a negligible correlation in training-induced changes in gene expression ( r = 0.04 95% confidence interval (CI) [–0.12, 0.20]). Overall, our results suggest that forgetting of sensitization memory represents retrieval failure.

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Latent memory facilitates relearning through molecular signaling mechanisms that are distinct from original learning

Cited by 9 publications

References 44 publications

Transforming growth factor β recruits persistent MAPK signaling to regulate long-term memory consolidation in Aplysia californica

Transforming growth factor β recruits persistent MAPK signaling to regulate long-term memory consolidation in Aplysia californica

Transcriptional changes before and after forgetting of a long-term sensitization memory in Aplysia californica

Registered Report: Transcriptional Analysis of Savings Memory Suggests Forgetting is Due to Retrieval Failure

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