Learning & memoryPub Date : 2023-09-19Print Date: 2023-09-01DOI: 10.1101/lm.053753.123
Xiu Miao, Carolin Müller, Nicolas D Lutz, Qing Yang, Florian Waszak, Jan Born, Karsten Rauss
{"title":"Sleep consolidates stimulus-response learning.","authors":"Xiu Miao, Carolin Müller, Nicolas D Lutz, Qing Yang, Florian Waszak, Jan Born, Karsten Rauss","doi":"10.1101/lm.053753.123","DOIUrl":"10.1101/lm.053753.123","url":null,"abstract":"<p><p>Performing a motor response to a sensory stimulus creates a memory trace whose behavioral correlates are classically investigated in terms of repetition priming effects. Such stimulus-response learning entails two types of associations that are partly independent: (1) an association between the stimulus and the motor response and (2) an association between the stimulus and the classification task in which it is encountered. Here, we tested whether sleep supports long-lasting stimulus-response learning on a task requiring participants (1) for establishing stimulus-classification associations to classify presented objects along two different dimensions (\"size\" and \"mechanical\") and (2) as motor response (action) to respond with either the left or right index finger. Moreover, we examined whether strengthening of stimulus-classification associations is preferentially linked to nonrapid eye movement (non-REM) sleep and strengthening of stimulus-action associations to REM sleep. We tested 48 healthy volunteers in a between-subjects design comparing postlearning retention periods of nighttime sleep versus daytime wakefulness. At postretention testing, we found that sleep supports consolidation of both stimulus-action and stimulus-classification associations, as indicated by increased reaction times in \"switch conditions\"; that is, when, at test, the acutely instructed classification task and/or correct motor response for a given stimulus differed from that during original learning. Polysomnographic recordings revealed that both kinds of associations were correlated with non-REM spindle activity. Our results do not support the view of differential roles for non-REM and REM sleep in the consolidation of stimulus-classification and stimulus-action associations, respectively.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 9","pages":"175-184"},"PeriodicalIF":1.8,"publicationDate":"2023-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547380/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41104162","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 : 2023-09-07Print Date: 2023-08-01DOI: 10.1101/lm.053842.123
Heidrun Schultz, Hanna Stoffregen, Roland G Benoit
{"title":"A reward effect on memory retention, consolidation, and generalization?","authors":"Heidrun Schultz, Hanna Stoffregen, Roland G Benoit","doi":"10.1101/lm.053842.123","DOIUrl":"10.1101/lm.053842.123","url":null,"abstract":"<p><p>Reward improves memory through both encoding and consolidation processes. In this preregistered study, we tested whether reward effects on memory generalize from high-rewarded items to low-rewarded but episodically related items. Fifty-nine human volunteers incidentally encoded associations between unique objects and repeated scenes. Some scenes typically yielded high reward, whereas others typically yielded low reward. Memory was tested immediately after encoding (<i>n</i> = 29) or the next day (<i>n</i> = 30). Overall, reward had only a limited influence on memory. It did not enhance consolidation and its effect did not generalize to episodically related stimuli. We thus contribute to understanding the boundary conditions of reward effects on memory.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 8","pages":"169-174"},"PeriodicalIF":1.8,"publicationDate":"2023-09-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10519399/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10252435","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 : 2023-08-24Print Date: 2023-08-01DOI: 10.1101/lm.053797.123
Leeza Kopaeva, Alexandrina Yakimov, Louise Urien, Elizabeth P Bauer
{"title":"Chemogenetic activation of the ventral subiculum-BNST pathway reduces context fear expression.","authors":"Leeza Kopaeva, Alexandrina Yakimov, Louise Urien, Elizabeth P Bauer","doi":"10.1101/lm.053797.123","DOIUrl":"10.1101/lm.053797.123","url":null,"abstract":"<p><p>An inability to reduce fear in nonthreatening environments characterizes many anxiety disorders. The pathway from the ventral subiculum (vSUB) to the bed nucleus of the stria terminalis (BNST) is more active in safe contexts than in aversive ones, as indexed by FOS expression. Here, we used chemogenetic techniques to specifically activate the vSUB-BNST pathway during both context and cued fear expression by expressing a Cre-dependent hM3D(Gq) receptor in BNST-projecting vSUB neurons. Activation of the vSUB-BNST pathway reduced context but not cued fear expression. These data suggest that the vSUB-BNST pathway contributes to behavioral responses to nonaversive contexts.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 8","pages":"164-168"},"PeriodicalIF":1.8,"publicationDate":"2023-08-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10519403/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10435030","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 : 2023-08-15Print Date: 2023-08-01DOI: 10.1101/lm.053782.123
Christopher N Wahlheim, Sydney T Smith, Sydney M Garlitch, Robert W Wiley
{"title":"Interpolated retrieval retroactively increases recall and promotes cross-episode memory interdependence.","authors":"Christopher N Wahlheim, Sydney T Smith, Sydney M Garlitch, Robert W Wiley","doi":"10.1101/lm.053782.123","DOIUrl":"10.1101/lm.053782.123","url":null,"abstract":"<p><p>Retrieving existing memories before new learning can lead to retroactive facilitation. Three experiments examined whether interpolated retrieval is associated with retroactive facilitation and memory interdependence that reflects integrative encoding. Participants studied two lists of cue-response word pairs that repeated across lists (A-B, A-B), appeared in list 1 (A-B, -), or included the same cues with changed responses in each list (A-B, A-C). For A-B, A-C pairs, the tasks interpolated between lists required recall of list 1 (B) responses (with or without feedback) or restudy of complete list 1 (A-B) pairs. In list 2, participants only studied pairs (experiment 1) or studied pairs, attempted to detect changed (C) responses, and attempted to recall list 1 responses for detected changes (experiments 2 and 3). On a final cued recall test, participants attempted to recall list 1 responses, indicated whether responses changed between lists, and if so, attempted to recall list 2 responses. Interpolated retrieval was associated with subsequent retroactive facilitation and greater memory interdependence for B and C responses. These correlational findings are compatible with the view that retrieval retroactively facilitates memories, promotes coactivation of existing memories and new learning, and enables integrative encoding that veridically binds information across episodes.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 8","pages":"151-163"},"PeriodicalIF":1.8,"publicationDate":"2023-08-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10519378/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10003475","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 : 2023-08-08Print Date: 2023-07-01DOI: 10.1101/lm.053781.123
Yanfang Xia, Jelena Wehrli, Samuel Gerster, Marijn Kroes, Maxime Houtekamer, Dominik R Bach
{"title":"Measuring human context fear conditioning and retention after consolidation.","authors":"Yanfang Xia, Jelena Wehrli, Samuel Gerster, Marijn Kroes, Maxime Houtekamer, Dominik R Bach","doi":"10.1101/lm.053781.123","DOIUrl":"10.1101/lm.053781.123","url":null,"abstract":"<p><p>Fear conditioning is a laboratory paradigm commonly used to investigate aversive learning and memory. In context fear conditioning, a configuration of elemental cues (conditioned stimulus [CTX]) predicts an aversive event (unconditioned stimulus [US]). To quantify context fear acquisition in humans, previous work has used startle eyeblink responses (SEBRs), skin conductance responses (SCRs), and verbal reports, but different quantification methods have rarely been compared. Moreover, preclinical intervention studies mandate recall tests several days after acquisition, and it is unclear how to induce and measure context fear memory retention over such a time interval. First, we used a semi-immersive virtual reality paradigm. In two experiments (<i>N</i> = 23 and <i>N</i> = 28), we found successful declarative learning and memory retention over 7 d but no evidence of other conditioned responses. Next, we used a configural fear conditioning paradigm with five static room images as CTXs in two experiments (<i>N</i> = 29 and <i>N</i> = 24). Besides successful declarative learning and memory retention after 7 d, SCR and pupil dilation in response to CTX onset differentiated CTX<sup>+</sup>/CTX<sup>-</sup> during acquisition training, and SEBR and pupil dilation differentiated CTX<sup>+</sup>/CTX<sup>-</sup> during the recall test, with medium to large effect sizes for the most sensitive indices (SEBR: Hedge's <i>g</i> = 0.56 and <i>g</i> = 0.69; pupil dilation: Hedge's <i>g</i> = 0.99 and <i>g</i> = 0.88). Our results demonstrate that with a configural learning paradigm, context fear memory retention can be demonstrated over 7 d, and we provide robust and replicable measurement methods to this end.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 7","pages":"139-150"},"PeriodicalIF":2.0,"publicationDate":"2023-08-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10519410/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10002973","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 : 2023-07-24Print Date: 2023-07-01DOI: 10.1101/lm.053795.123
Virginie Oberto, Hongying Gao, Ana Biondi, Susan J Sara, Sidney I Wiener
{"title":"Activation of prefrontal cortex and striatal regions in rats after shifting between rules in a T-maze.","authors":"Virginie Oberto, Hongying Gao, Ana Biondi, Susan J Sara, Sidney I Wiener","doi":"10.1101/lm.053795.123","DOIUrl":"10.1101/lm.053795.123","url":null,"abstract":"<p><p>Prefrontal cortical and striatal areas have been identified by inactivation or lesion studies to be required for behavioral flexibility, including selecting and processing of different types of information. In order to identify these networks activated selectively during the acquisition of new reward contingency rules, rats were trained to discriminate orientations of bars presented in pseudorandom sequence on two video monitors positioned behind the goal sites on a T-maze with return arms. A second group already trained in the visual discrimination task learned to alternate left and right goal arm visits in the same maze while ignoring the visual cues still being presented. In each experimental group, once the rats reached criterion performance, the brains were prepared after a 90-min delay for later processing for c-fos immunohistochemistry. While both groups extinguished a prior strategy and acquired a new rule, they differed by the identity of the strategies and previous learning experience. Among the 28 forebrain areas examined, there were significant increases in the relative density of c-fos immunoreactive cell bodies after learning the second rule in the prefrontal cortex cingulate, the prelimbic and infralimbic areas, the dorsomedial striatum and the core of the nucleus accumbens, the ventral subiculum, and the central nucleus of the amygdala. These largely correspond to structures previously identified in inactivation studies, and their neurons fire synchronously during learning and strategy shifts. The data suggest that this dynamic network may underlie reward-based selection for action-a type of cognitive flexibility.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 7","pages":"133-138"},"PeriodicalIF":1.8,"publicationDate":"2023-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10519402/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9940435","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 : 2023-07-24Print Date: 2023-07-01DOI: 10.1101/lm.053836.123
Niek Brosens, Sylvie L Lesuis, Ilse Bassie, Lara Reyes, Priya Gajadien, Paul J Lucassen, Harm J Krugers
{"title":"Elevated corticosterone after fear learning impairs remote auditory memory retrieval and alters brain network connectivity.","authors":"Niek Brosens, Sylvie L Lesuis, Ilse Bassie, Lara Reyes, Priya Gajadien, Paul J Lucassen, Harm J Krugers","doi":"10.1101/lm.053836.123","DOIUrl":"10.1101/lm.053836.123","url":null,"abstract":"<p><p>Glucocorticoids are potent memory modulators that can modify behavior in an adaptive or maladaptive manner. Elevated glucocorticoid levels after learning promote memory consolidation at recent time points, but their effects on remote time points are not well established. Here we set out to assess whether corticosterone (CORT) given after learning modifies remote fear memory. To that end, mice were exposed to a mild auditory fear conditioning paradigm followed by a single 2 mg/kg CORT injection, and after 28 d, auditory memory was assessed. Neuronal activation was investigated using immunohistochemistry for the immediate early gene <i>c</i>-<i>Fos</i>, and coactivation of brain regions was determined using a correlation matrix analysis. CORT-treated mice displayed significantly less remote auditory memory retrieval. While the net activity of studied brain regions was similar compared with the control condition, CORT-induced remote memory impairment was associated with altered correlated activity between brain regions. Specifically, connectivity of the lateral amygdala with the basal amygdala and the dorsal dentate gyrus was significantly reduced in CORT-treated mice, suggesting disrupted network connectivity that may underlie diminished remote memory retrieval. Elucidating the pathways underlying these effects could help provide mechanistic insight into the effects of stress on memory and possibly provide therapeutic targets for psychopathology.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 7","pages":"125-132"},"PeriodicalIF":1.8,"publicationDate":"2023-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10519398/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10244687","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 : 2023-07-13Print Date: 2023-05-01DOI: 10.1101/lm.053758.123
Robert D Hawkins, Lennart Brodin, Elvar Theodorsson, Ákos Végvári, Eric R Kandel, Tomas Hokfelt
{"title":"Distribution, cellular localization, and colocalization of several peptide neurotransmitters in the central nervous system of <i>Aplysia</i>.","authors":"Robert D Hawkins, Lennart Brodin, Elvar Theodorsson, Ákos Végvári, Eric R Kandel, Tomas Hokfelt","doi":"10.1101/lm.053758.123","DOIUrl":"10.1101/lm.053758.123","url":null,"abstract":"<p><p>Neuropeptides are widely used as neurotransmitters in vertebrates and invertebrates. In vertebrates, a detailed understanding of their functions as transmitters has been hampered by the complexity of the nervous system. The marine mollusk <i>Aplysia</i>, with a simpler nervous system and many large, identified neurons, presents several advantages for addressing this question and has been used to examine the roles of tens of peptides in behavior. To screen for other peptides that might also play roles in behavior, we observed immunoreactivity in individual neurons in the central nervous system of adult <i>Aplysia</i> with antisera raised against the <i>Aplysia</i> peptide FMRFamide and two mammalian peptides that are also found in <i>Aplysia</i>, cholecystokinin (CCK) and neuropeptide Y (NPY), as well as serotonin (5HT). In addition, we observed staining of individual neurons with antisera raised against mammalian somatostatin (SOM) and peptide histidine isoleucine (PHI). However, genomic analysis has shown that these two peptides are not expressed in the <i>Aplysia</i> nervous system, and we have therefore labeled the unknown peptides stained by these two antibodies as X<sub>SOM</sub> and X<sub>PHI</sub> There was an area at the anterior end of the cerebral ganglion that had staining by antisera raised against many different transmitters, suggesting that this may be a modulatory region of the nervous system. There was also staining for X<sub>SOM</sub> and, in some cases, FMRFamide in the bag cell cluster of the abdominal ganglion. In addition, these and other studies have revealed a fairly high degree of colocalization of different neuropeptides in individual neurons, suggesting that the peptides do not just act independently but can also interact in different combinations to produce complex functions. The simple nervous system of <i>Aplysia</i> is advantageous for further testing these ideas.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 5-6","pages":"116-123"},"PeriodicalIF":2.0,"publicationDate":"2023-07-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10353257/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9836040","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 : 2023-07-11Print Date: 2023-05-01DOI: 10.1101/lm.053760.123
Patrick A F Laing, Joseph E Dunsmoor
{"title":"Pattern separation of fear extinction memory.","authors":"Patrick A F Laing, Joseph E Dunsmoor","doi":"10.1101/lm.053760.123","DOIUrl":"10.1101/lm.053760.123","url":null,"abstract":"<p><p>While fear generalizes widely, extinction is stimulus-specific. Using a hybrid conditioning/episodic memory paradigm, subjects encoded nonrepeating category exemplars during fear conditioning and extinction. Twenty-four hours later, a surprise memory test included old, similar, and novel category exemplars. Results showed strong dissociation between pattern completion (generalization) and pattern separation (discrimination) in episodic memory for items encoded during fear conditioning versus extinction, respectively. These data suggest that directly threat-conditioned stimuli are better recognized at the expense of mnemonic precision, whereas discrimination is enhanced for extinguished stimuli. Overly precise extinction memory may be a contributing factor to fear relapse.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 5-6","pages":"110-115"},"PeriodicalIF":2.0,"publicationDate":"2023-07-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10353259/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9826242","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 : 2023-07-07Print Date: 2023-05-01DOI: 10.1101/lm.053710.122
Ruijing Ning, Beverly A Wright
{"title":"Evidence that anterograde learning interference depends on the stage of learning of the interferer: blocked versus interleaved training.","authors":"Ruijing Ning, Beverly A Wright","doi":"10.1101/lm.053710.122","DOIUrl":"10.1101/lm.053710.122","url":null,"abstract":"<p><p>Training on one task (task A) can disrupt learning on a subsequently trained task (task B), illustrating anterograde learning interference. We asked whether the induction of anterograde learning interference depends on the learning stage that task A has reached when the training on task B begins. To do so, we drew on previous observations in perceptual learning in which completing all training on one task before beginning training on another task (blocked training) yielded markedly different learning outcomes than alternating training between the same two tasks for the same total number of trials (interleaved training). Those blocked versus interleaved contrasts suggest that there is a transition between two differentially vulnerable learning stages that is related to the number of consecutive training trials on each task, with interleaved training presumably tapping acquisition, and blocked training tapping consolidation. Here, we used the blocked versus interleaved paradigm in auditory perceptual learning in a case in which blocked training generated anterograde-but not its converse, retrograde-learning interference (A→B, not B←A). We report that anterograde learning interference of training on task A (interaural time difference discrimination) on learning on task B (interaural level difference discrimination) occurred with blocked training and diminished with interleaved training, with faster rates of interleaving leading to less interference. This pattern held for across-day, within-session, and offline learning. Thus, anterograde learning interference only occurred when the number of consecutive training trials on task A surpassed some critical value, consistent with other recent evidence that anterograde learning interference only arises when learning on task A has entered the consolidation stage.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 5-6","pages":"101-109"},"PeriodicalIF":2.0,"publicationDate":"2023-07-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10353258/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10193700","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}