Learning & memoryPub Date : 2023-10-06Print Date: 2023-10-01DOI: 10.1101/lm.053785.123
Anne Karine Bosetto Fiebrantz, Luana Felski Leite, Eduarda Dal Pisol Schwab, Juliana Sartori Bonini, Weber Cláudio da Silva
{"title":"On the participation of adenosinergic receptors in the reconsolidation of spatial long-term memory in male rats.","authors":"Anne Karine Bosetto Fiebrantz, Luana Felski Leite, Eduarda Dal Pisol Schwab, Juliana Sartori Bonini, Weber Cláudio da Silva","doi":"10.1101/lm.053785.123","DOIUrl":"10.1101/lm.053785.123","url":null,"abstract":"<p><p>To date, there is insufficient evidence to explain the role of adenosinergic receptors in the reconsolidation of long-term spatial memory. In this work, the role of the adenosinergic receptor family (A1, A2A, A2B, and A3) in this process has been elucidated. It was demonstrated that when infused bilaterally into the hippocampal CA1 region immediately after an early nonreinforced test session performed 24 h posttraining in the Morris water maze task, adenosine can cause anterograde amnesia for recent and late long-term spatial memory. This effect on spatial memory reconsolidation was blocked by A1 or A3 receptor antagonists and mimicked by A1 plus A3 receptor agonists, showing that this effect occurs through A1 and A3 receptors simultaneously. The A3 receptor alone participates only in the reconsolidation of late long-term spatial memory. When the memory to be reconsolidated was delayed (reactivation 5 d posttraining), the amnesic effect of adenosine became transient and did not occur in a test performed 5 d after the reactivation of the mnemonic trace. Finally, it has been shown that the amnesic effect of adenosine on spatial memory reconsolidation depends on the occurrence of protein degradation and that the amnesic effect of inhibition of protein synthesis on spatial memory reconsolidation is dependent on the activation of A3 receptors.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 10","pages":"260-270"},"PeriodicalIF":1.8,"publicationDate":"2023-10-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10561635/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41142255","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2023-10-06Print Date: 2023-10-01DOI: 10.1101/lm.053833.123
Robert J Hammack, Victoria E Fischer, Mary Ann Andrade, Glenn M Toney
{"title":"Presence of a remote fear memory engram in the central amygdala.","authors":"Robert J Hammack, Victoria E Fischer, Mary Ann Andrade, Glenn M Toney","doi":"10.1101/lm.053833.123","DOIUrl":"10.1101/lm.053833.123","url":null,"abstract":"<p><p>Fear memory formation and recall are highly regulated processes, with the central amygdala (CeA) contributing to fear memory-related behaviors. We recently reported that a remote fear memory engram is resident in the anterior basolateral amygdala (aBLA). However, the extent to which downstream neurons in the CeA participate in this engram is unknown. We tested the hypothesis that CeA neurons activated during fear memory formation are reactivated during remote memory retrieval such that a CeA engram participates in remote fear memory recall and its associated behavior. Using contextual fear conditioning in TRAP2;Ai14 mice, we identified, by persistent Cre-dependent tdTomato expression (i.e., \"TRAPing\"), CeA neurons that were <i>c-fos</i>-activated during memory formation. Twenty-one days later, we quantified neurons activated during remote memory recall using Fos immunohistochemistry. Dual labeling was used to identify the subpopulation of CeA neurons that was both activated during memory formation and reactivated during recall. Compared with their context-conditioned (no shock) controls, fear-conditioned (electric shock) mice (<i>n</i> = 5/group) exhibited more robust fear memory-related behavior (freezing) as well as larger populations of activated (tdTomato<sup>+</sup>) and reactivated (dual-labeled) CeA neurons. Most neurons in both groups were mainly located in the capsular CeA subdivision (CeAC). Notably, however, only the size of the TRAPed population distributed throughout the CeA was significantly correlated with time spent freezing during remote fear memory recall. Our findings indicate that fear memory formation robustly activates CeA neurons and that a subset located mainly in the CeAC may contribute to both remote fear memory storage/retrieval and the resulting fear-like behavior.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 10","pages":"250-259"},"PeriodicalIF":1.8,"publicationDate":"2023-10-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10561632/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41131789","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2023-09-28Print Date: 2023-09-01DOI: 10.1101/lm.053685.122
Katrina Rodheim, Kyle Kainec, Eunsol Noh, Bethany Jones, Rebecca M C Spencer
{"title":"Emotional memory consolidation during sleep is associated with slow oscillation-spindle coupling strength in young and older adults.","authors":"Katrina Rodheim, Kyle Kainec, Eunsol Noh, Bethany Jones, Rebecca M C Spencer","doi":"10.1101/lm.053685.122","DOIUrl":"10.1101/lm.053685.122","url":null,"abstract":"<p><p>Emotional memories are processed during sleep; however, the specific mechanisms are unclear. Understanding such mechanisms may provide critical insight into preventing and treating mood disorders. Consolidation of neutral memories is associated with the coupling of NREM sleep slow oscillations (SOs) and sleep spindles (SPs). Whether SO-SP coupling is likewise involved in emotional memory processing is unknown. Furthermore, there is an age-related emotional valence bias such that sleep consolidates and preserves reactivity to negative but not positive emotional memories in young adults and positive but not negative emotional memories in older adults. If SO-SP coupling contributes to the effect of sleep on emotional memory, then it may selectively support negative memory in young adults and positive memory in older adults. To address these questions, we examined whether emotional memory recognition and overnight change in emotional reactivity were associated with the strength of SO-SP coupling in young (<i>n</i> = 22) and older (<i>n</i> = 32) adults. In younger adults, coupling strength predicted negative but not positive emotional memory performance after sleep. In contrast, coupling strength predicted positive but not negative emotional memory performance after sleep in older adults. Coupling strength was not associated with emotional reactivity in either age group. Our findings suggest that SO-SP coupling may play a mechanistic role in sleep-dependent consolidation of emotional memories.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 9","pages":"237-244"},"PeriodicalIF":1.8,"publicationDate":"2023-09-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547370/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41134006","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2023-09-28Print Date: 2023-09-01DOI: 10.1101/lm.053660.122
Marit Petzka, Ondrej Zika, Bernhard P Staresina, Scott A Cairney
{"title":"Better late than never: sleep still supports memory consolidation after prolonged periods of wakefulness.","authors":"Marit Petzka, Ondrej Zika, Bernhard P Staresina, Scott A Cairney","doi":"10.1101/lm.053660.122","DOIUrl":"10.1101/lm.053660.122","url":null,"abstract":"<p><p>While the benefits of sleep for associative memory are well established, it is unclear whether single-item memories profit from overnight consolidation to the same extent. We addressed this question in a preregistered, online study and also investigated how the temporal proximity between learning and sleep influences overnight retention. Sleep relative to wakefulness improved retention of item and associative memories to similar extents irrespective of whether sleep occurred soon after learning or following a prolonged waking interval. Our findings highlight the far-reaching influences of sleep on memory that can arise even after substantial periods of wakefulness.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 9","pages":"245-249"},"PeriodicalIF":2.0,"publicationDate":"2023-09-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547377/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41132581","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2023-09-27Print Date: 2023-09-01DOI: 10.1101/lm.053834.123
Pedro A Feliciano-Ramos, Maria Galazo, Hector Penagos, Matthew Wilson
{"title":"Hippocampal memory reactivation during sleep is correlated with specific cortical states of the retrosplenial and prefrontal cortices.","authors":"Pedro A Feliciano-Ramos, Maria Galazo, Hector Penagos, Matthew Wilson","doi":"10.1101/lm.053834.123","DOIUrl":"10.1101/lm.053834.123","url":null,"abstract":"<p><p>Episodic memories are thought to be stabilized through the coordination of cortico-hippocampal activity during sleep. However, the timing and mechanism of this coordination remain unknown. To investigate this, we studied the relationship between hippocampal reactivation and slow-wave sleep up and down states of the retrosplenial cortex (RTC) and prefrontal cortex (PFC). We found that hippocampal reactivations are strongly correlated with specific cortical states. Reactivation occurred during sustained cortical Up states or during the transition from up to down state. Interestingly, the most prevalent interaction with memory reactivation in the hippocampus occurred during sustained up states of the PFC and RTC, while hippocampal reactivation and cortical up-to-down state transition in the RTC showed the strongest coordination. Reactivation usually occurred within 150-200 msec of a cortical Up state onset, indicating that a buildup of excitation during cortical Up state activity influences the probability of memory reactivation in CA1. Conversely, CA1 reactivation occurred 30-50 msec before the onset of a cortical down state, suggesting that memory reactivation affects down state initiation in the RTC and PFC, but the effect in the RTC was more robust. Our findings provide evidence that supports and highlights the complexity of bidirectional communication between cortical regions and the hippocampus during sleep.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 9","pages":"221-236"},"PeriodicalIF":1.8,"publicationDate":"2023-09-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547389/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41125698","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2023-09-19Print Date: 2023-09-01DOI: 10.1101/lm.053683.122
Anna Wick, Björn Rasch
{"title":"Targeted memory reactivation during slow-wave sleep vs. sleep stage N2: no significant differences in a vocabulary task.","authors":"Anna Wick, Björn Rasch","doi":"10.1101/lm.053683.122","DOIUrl":"10.1101/lm.053683.122","url":null,"abstract":"<p><p>Sleep supports memory consolidation, and slow-wave sleep (SWS) in particular is assumed to benefit the consolidation of verbal learning material. Re-exposure to previously learned words during SWS with a technique known as targeted memory reactivation (TMR) consistently benefits memory. However, TMR has also been successfully applied during sleep stage N2, though a direct comparison between words selectively reactivated during SWS versus N2 is still missing. Here, we directly compared the effects of N2 TMR and SWS TMR on memory performance in a vocabulary learning task in a within-subject design. Thirty-four healthy young participants (21 in the main sample and 13 in an additional sample) learned 120 Dutch-German word pairs before sleep. Participants in the main sample slept for ∼8 h during the night, while participants in the additional sample slept ∼3 h. We reactivated the Dutch words selectively during N2 and SWS in one single night. Forty words were not cued. Participants in the main sample recalled the German translations of the Dutch words after sleep in the morning, while those in the additional sample did so at 2:00 a.m. As expected, we observed no differences in recall performance between words reactivated during N2 and SWS. However, we failed to find an overall memory benefit of reactivated over nonreactivated words. Detailed time-frequency analyses showed that words played during N2 elicited stronger characteristic oscillatory responses in several frequency bands, including spindle and theta frequencies, compared with SWS. These oscillatory responses did not vary with the memory strengths of individual words. Our results question the robustness and replicability of the TMR benefit on memory using our Dutch vocabulary learning task. We discuss potential boundary conditions for vocabulary reactivation paradigms and, most importantly, see the need for further replication studies, ideally including multiple laboratories and larger sample sizes.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 9","pages":"192-200"},"PeriodicalIF":1.8,"publicationDate":"2023-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547374/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41135237","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2023-09-19Print Date: 2023-09-01DOI: 10.1101/lm.053787.123
Tamas Foldes, Lorena Santamaria, Penny Lewis
{"title":"Sleep-related benefits to transitive inference are modulated by encoding strength and joint rank.","authors":"Tamas Foldes, Lorena Santamaria, Penny Lewis","doi":"10.1101/lm.053787.123","DOIUrl":"10.1101/lm.053787.123","url":null,"abstract":"<p><p>Transitive inference is a measure of relational learning that has been shown to improve across sleep. Here, we examine this phenomenon further by studying the impact of encoding strength and joint rank. In experiment 1, participants learned adjacent premise pairs and were then tested on inferential problems derived from those pairs. In line with prior work, we found improved transitive inference performance after retention across a night of sleep compared with wake alone. Experiment 2 extended these findings using a within-subject design and found superior transitive inference performance on a hierarchy, consolidated across 27 h including sleep compared with just 3 h of wake. In both experiments, consolidation-related improvement was enhanced when presleep learning (i.e., encoding strength) was stronger. We also explored the interaction of these effects with the joint rank effect, in which items were scored according to their rank in the hierarchy, with more dominant item pairs having the lowest scores. Interestingly, the consolidation-related benefit was greatest for more dominant inference pairs (i.e., those with low joint rank scores). Overall, our findings provide further support for the improvement of transitive inference across a consolidation period that includes sleep. We additionally show that encoding strength and joint rank strongly modulate this effect.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 9","pages":"201-211"},"PeriodicalIF":1.8,"publicationDate":"2023-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547378/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41123438","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2023-09-19Print Date: 2023-09-01DOI: 10.1101/lm.053765.123
Dan Denis, Ryan Bottary, Tony J Cunningham, Mario-Cyriac Tcheukado, Jessica D Payne
{"title":"The influence of encoding strategy on associative memory consolidation across wake and sleep.","authors":"Dan Denis, Ryan Bottary, Tony J Cunningham, Mario-Cyriac Tcheukado, Jessica D Payne","doi":"10.1101/lm.053765.123","DOIUrl":"https://doi.org/10.1101/lm.053765.123","url":null,"abstract":"<p><p>Sleep benefits memory consolidation. However, factors present at initial encoding may moderate this effect. Here, we examined the role that encoding strategy plays in subsequent memory consolidation during sleep. Eighty-nine participants encoded pairs of words using two different strategies. Each participant encoded half of the word pairs using an integrative visualization technique, where the two items were imagined in an integrated scene. The other half were encoded nonintegratively, with each word pair item visualized separately. Memory was tested before and after a period of nocturnal sleep (<i>N</i> = 47) or daytime wake (<i>N</i> = 42) via cued recall tests. Immediate memory performance was significantly better for word pairs encoded using the integrative strategy compared with the nonintegrative strategy (<i>P</i> < 0.001). When looking at the change in recall across the delay, there was significantly less forgetting of integrated word pairs across a night of sleep compared with a day spent awake (<i>P</i> < 0.001), with no significant difference in the nonintegrated pairs (<i>P</i> = 0.19). This finding was driven by more forgetting of integrated compared with not-integrated pairs across the wake delay (<i>P</i> < 0.001), whereas forgetting was equivalent across the sleep delay (<i>P</i> = 0.26). Together, these results show that the strategy engaged in during encoding impacts both the immediate retention of memories and their subsequent consolidation across sleep and wake intervals.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 9","pages":"185-191"},"PeriodicalIF":2.0,"publicationDate":"2023-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547373/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41121819","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2023-09-19Print Date: 2023-09-01DOI: 10.1101/lm.053772.123
Lucia M Sweeney, Hatty Lara, Rebecca L Gómez
{"title":"Developmental changes in retention and generalization of nonadjacent dependencies over a period containing sleep in 18-mo-old infants.","authors":"Lucia M Sweeney, Hatty Lara, Rebecca L Gómez","doi":"10.1101/lm.053772.123","DOIUrl":"10.1101/lm.053772.123","url":null,"abstract":"<p><p>Sleep promotes the stabilization of memories in adulthood, with a growing literature on the benefits of sleep for memory in infants and children. In two studies, we examined the role of sleep in the retention and generalization of nonadjacent dependencies (NADs; e.g., a-X-b/c-X-d phrases) in an artificial language. Previously, a study demonstrated that over a delay of 4 h, 15 mo olds who nap after training retain a general memory of the NAD rule instead of memory for specific NADs heard during training. In experiment 1, we designed a replication of the nap condition used in the earlier study but tested 18-mo-old infants. Infants of this age retained veridical memory for specific NADs over a delay containing sleep, providing preliminary evidence of the development of memory processes (experiment 1). In experiment 2, we tested 18 mo olds' ability to generalize the NAD to new vocabulary, finding only infants who napped after training generalized their knowledge of the pattern to completely novel phrases. Overall, by 18 mo of age, children retain specific memories over a period containing sleep, and sleep promotes abstract memories to a greater extent than wakefulness.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 9","pages":"212-220"},"PeriodicalIF":1.8,"publicationDate":"2023-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547371/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41140071","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2023-09-19Print Date: 2023-09-01DOI: 10.1101/lm.053886.123
{"title":"Special issue on sleep and memory.","authors":"","doi":"10.1101/lm.053886.123","DOIUrl":"10.1101/lm.053886.123","url":null,"abstract":"","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 9","pages":"v"},"PeriodicalIF":1.8,"publicationDate":"2023-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547372/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41124751","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}