Learning & memoryPub Date : 2024-02-26Print Date: 2024-01-01DOI: 10.1101/lm.053892.123
Michelle Surets, Albit Caban-Murillo, Steve Ramirez
{"title":"Prelimbic cortex ensembles promote appetitive learning-associated behavior.","authors":"Michelle Surets, Albit Caban-Murillo, Steve Ramirez","doi":"10.1101/lm.053892.123","DOIUrl":"10.1101/lm.053892.123","url":null,"abstract":"<p><p>Memories of prior rewards bias our actions and future decisions. To determine the neural correlates of an appetitive associative learning task, we trained male mice to discriminate a reward-predicting cue over the course of 7 d. Encoding, recent recall, and remote recall were investigated to determine the areas of the brain recruited at each stage of learning. Using cFos as a proxy for neuronal activity, we found unique brain-wide patterns of activity across days that seem to correlate with distinct stages of learning. In particular, the prelimbic (PL) cortex was significantly recruited during the encoding of a novel association presentation, but its activity decreases as learning continues. To causally dissect the role of the PL in a reward memory across days, we chemogenetically inhibited first the PL entirely and then only tagged memory-bearing cells that were active during encoding in two stages of learning: early and late. Both nonspecific and specific PL inhibition experiments indicate that the PL drives behavior during late stages of learning to facilitate appropriate cue-driven behavior. Overall, our work underscores memory's role in discriminative reward seeking, and points to the PL as a target for modulating disorders in which impaired reward processing is a core component.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 1-2","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-02-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10903945/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139972523","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 : 2024-01-29Print Date: 2024-01-01DOI: 10.1101/lm.053871.123
Timothy J Onofrychuk, Aiden E Glass, Quentin Greba, John G Howland
{"title":"Evidence for novelty reward cross-cueing in the odor span task in rats: implications for odor-based reward-motivated tasks.","authors":"Timothy J Onofrychuk, Aiden E Glass, Quentin Greba, John G Howland","doi":"10.1101/lm.053871.123","DOIUrl":"10.1101/lm.053871.123","url":null,"abstract":"<p><p>The odor span task (OST) infers working memory capacity (WMC) by requiring rodents to discriminate between previously presented and session-novel odors to obtain a hidden food reward. Here, rats' responses to session-novel odors and food rewards were assessed to determine whether rats use mitigating strategies in the OST. Rats accurately responded to session-novel odors but also reliably responded to the food reward alone and performed at chance when both a session-novel odor and food reward were presented in separate locations. The inclusion of unscented sand in the cups holding the food reward significantly reduced the rats' responses to the food reward alone. Collectively, these results demonstrate the need for rigorous tests of potential mitigating strategies and hold wide implications for rodent odor discrimination-based behavioral tasks.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 1-2","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10903935/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139575724","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 : 2024-01-29Print Date: 2024-01-01DOI: 10.1101/lm.053895.123
James F Briggs, Kaitlyn M McMullen
{"title":"Retrograde amnesia for the stress-induced impairment of extinction: time-dependent and not so forgotten.","authors":"James F Briggs, Kaitlyn M McMullen","doi":"10.1101/lm.053895.123","DOIUrl":"10.1101/lm.053895.123","url":null,"abstract":"<p><p>We investigated whether retrograde amnesia for the stress-induced impairment of extinction retrieval shares similar characteristics with original acquisition memories. The first experiment demonstrated that cycloheximide administered shortly after a single restraint stress session alleviated the impairment of extinction retrieval but not when administered following a longer delay (i.e., the amnesia for stress is time-dependent). A second experiment showed that the retrograde amnesia for stress could be alleviated by a second brief exposure to the stressor. These results demonstrating that amnesia for stress shares characteristics similar to original memories are explained using a retrieval-based memory integration model of retrograde amnesia.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 1-2","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10903941/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139575682","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 : 2023-12-19Print Date: 2023-12-01DOI: 10.1101/lm.053893.123
Fei Wang, Xu Chen, Binshi Bo, Tianfu Zhang, Kaiyuan Liu, Jun Jiang, Yonggang Wang, Hong Xie, Zhifeng Liang, Ji-Song Guan
{"title":"State-dependent memory retrieval: insights from neural dynamics and behavioral perspectives.","authors":"Fei Wang, Xu Chen, Binshi Bo, Tianfu Zhang, Kaiyuan Liu, Jun Jiang, Yonggang Wang, Hong Xie, Zhifeng Liang, Ji-Song Guan","doi":"10.1101/lm.053893.123","DOIUrl":"10.1101/lm.053893.123","url":null,"abstract":"<p><p>Memory retrieval is strikingly susceptible to external states (environment) and internal states (mood states and alcohol), yet we know little about the underlying mechanisms. We examined how internally generated states influence successful memory retrieval using the functional magnetic resonance imaging (fMRI) of laboratory mice during memory retrieval. Mice exhibited a strong tendency to perform memory retrieval correctly only in the reinstated mammillary body-inhibited state, in which mice were trained to discriminate auditory stimuli in go/no-go tasks. fMRI revealed that distinct auditory cues engaged differential brain regions, which were primed by internal state. Specifically, a cue associated with a reward activated the lateral amygdala, while a cue signaling no reward predominantly activated the postsubiculum. Modifying these internal states significantly altered the neural activity balance between these regions. Optogenetic inhibition of those regions in the precue period blocked the retrieval of type-specific memories. Our findings suggest that memory retrieval is under the control of two interrelated neural circuits underlying the neural basis of state-dependent memory retrieval.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 12","pages":"325-337"},"PeriodicalIF":1.8,"publicationDate":"2023-12-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10750866/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138794926","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 : 2023-12-06Print Date: 2023-12-01DOI: 10.1101/lm.053792.123
D Gregory Sullens, Phuoc Nguyen, Kayla Gilley, Madison B Wiffler, Melanie J Sekeres
{"title":"Hippocampal motor memory network reorganization depends on familiarity, not time.","authors":"D Gregory Sullens, Phuoc Nguyen, Kayla Gilley, Madison B Wiffler, Melanie J Sekeres","doi":"10.1101/lm.053792.123","DOIUrl":"10.1101/lm.053792.123","url":null,"abstract":"<p><p>There is debate as to whether a time-dependent transformation of the episodic-like memory network is observed for nonepisodic tasks, including procedural motor memory. To determine how motor memory networks reorganize with time and practice, mice performed a motor task in a straight alley maze for 1 d (recent), 20 d of continuous training (continuous), or testing 20 d after the original training (remote), and then regional c-Fos expression was assessed. Elevated hippocampal c-Fos accompanied remote, but not continuous, motor task retrieval after 20 d, suggesting that the hippocampus remains engaged for nonhabitual remote motor memory retrieval.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 12","pages":"320-324"},"PeriodicalIF":2.0,"publicationDate":"2023-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10750863/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138498776","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 : 2023-11-17Print Date: 2023-12-01DOI: 10.1101/lm.053840.123
Kyle M Roddick, Heather M Schellinck, Richard E Brown
{"title":"Serial reversal learning in an olfactory discrimination task in 3xTg-AD mice.","authors":"Kyle M Roddick, Heather M Schellinck, Richard E Brown","doi":"10.1101/lm.053840.123","DOIUrl":"10.1101/lm.053840.123","url":null,"abstract":"<p><p>Male and female 3xTg-AD mice between 5 and 24 mo of age and their B6129F2/J wild-type controls were tested on a series of 18 olfactory discrimination and reversal tasks in an operant olfactometer. All mice learned the odor discriminations and reversals to a criterion of 85% correct, but the 3xTg-AD mice made fewer errors than the B6129F2/J mice in the odor discriminations and in the first six reversal learning tasks. Many mice showed evidence of near errorless learning, and on the reversal tasks the 3xTg-AD mice showed more instances of near errorless learning than the B6129F2/J mice. There was no evidence of an age effect on odor discrimination, but there was a decrease in errorless reversal learning in aged B6129F2/J mice. In long-term memory tests, there was an increase in the number of errors made but no genotype difference. The high level of performance indicates that the mice were able to develop a \"learning to learn\" strategy. The finding that the 3xTg-AD mice outperformed their littermate controls provides an example of paradoxical functional facilitation in these mice.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 12","pages":"310-319"},"PeriodicalIF":1.8,"publicationDate":"2023-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10750865/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136398063","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 : 2023-11-03Print Date: 2023-11-01DOI: 10.1101/lm.053838.123
Caroline Chwiesko, John Janecek, Stephanie Doering, Martina Hollearn, Liv McMillan, Joachim Vandekerckhove, Michael D Lee, Roger Ratcliff, Michael A Yassa
{"title":"Parsing memory and nonmemory contributions to age-related declines in mnemonic discrimination performance: a hierarchical Bayesian diffusion decision modeling approach.","authors":"Caroline Chwiesko, John Janecek, Stephanie Doering, Martina Hollearn, Liv McMillan, Joachim Vandekerckhove, Michael D Lee, Roger Ratcliff, Michael A Yassa","doi":"10.1101/lm.053838.123","DOIUrl":"10.1101/lm.053838.123","url":null,"abstract":"<p><p>The mnemonic discrimination task (MDT) is a widely used cognitive assessment tool. Performance in this task is believed to indicate an age-related deficit in episodic memory stemming from a decreased ability to pattern-separate among similar experiences. However, cognitive processes other than memory ability might impact task performance. In this study, we investigated whether nonmnemonic decision-making processes contribute to the age-related deficit in the MDT. We applied a hierarchical Bayesian version of the Ratcliff diffusion model to the MDT performance of 26 younger and 31 cognitively normal older adults. It allowed us to decompose decision behavior in the MDT into different underlying cognitive processes, represented by specific model parameters. Model parameters were compared between groups, and differences were evaluated using the Bayes factor. Our results suggest that the age-related decline in MDT performance indicates a predominantly mnemonic deficit rather than differences in nonmnemonic decision-making processes. In addition, this mnemonic deficit might also involve a slowing in processes related to encoding and retrieval strategies, which are relevant for successful memory as well. These findings help to better understand what cognitive processes contribute to the age-related decline in MDT performance and may help to improve the diagnostic value of this popular task.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 11","pages":"296-309"},"PeriodicalIF":1.8,"publicationDate":"2023-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10631138/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"71483155","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 : 2023-11-03Print Date: 2023-11-01DOI: 10.1101/lm.053777.123
Puyuan Zhang, Hui Chen, Shelley Xiuli Tong
{"title":"Cue predictiveness and uncertainty determine cue representation during visual statistical learning.","authors":"Puyuan Zhang, Hui Chen, Shelley Xiuli Tong","doi":"10.1101/lm.053777.123","DOIUrl":"10.1101/lm.053777.123","url":null,"abstract":"<p><p>This study investigated how humans process probabilistic-associated information when encountering varying levels of uncertainty during implicit visual statistical learning. A novel probabilistic cueing validation paradigm was developed to probe the representation of cues with high (75% probability), medium (50%), low (25%), or zero levels of predictiveness in response to preceding targets that appeared with high (75%), medium (50%), or low (25%) transitional probabilities (TPs). Experiments 1 and 2 demonstrated a significant negative association between cue probe identification accuracy and cue predictiveness when these cues appeared after high-TP but not medium-TP or low-TP targets, establishing exploration-like cue processing triggered by lower-uncertainty rather than high-uncertainty inputs. Experiment 3 ruled out the confounding factor of probe repetition and extended this finding by demonstrating (1) enhanced representation of low-predictive and zero-predictive but not high-predictive cues across blocks after high-TP targets and (2) enhanced representation of high-predictive but not low-predictive and zero-predictive cues across blocks after low-TP targets for learners who exhibited above-chance awareness of cue-target transition. These results suggest that during implicit statistical learning, input characteristics alter cue-processing mechanisms, such that exploration-like and exploitation-like mechanisms are triggered by lower-uncertainty and higher-uncertainty cue-target sequences, respectively.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 11","pages":"282-295"},"PeriodicalIF":2.0,"publicationDate":"2023-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10631146/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"71483154","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 : 2023-10-18Print Date: 2023-11-01DOI: 10.1101/lm.053867.123
Miryam Levy, Jian Jing, Abraham J Susswein
{"title":"An in vitro analog of learning that food is inedible in <i>Aplysia</i>: decreased responses to a transmitter signaling food after pairing with transmitters signaling failed swallowing.","authors":"Miryam Levy, Jian Jing, Abraham J Susswein","doi":"10.1101/lm.053867.123","DOIUrl":"10.1101/lm.053867.123","url":null,"abstract":"<p><p>An in vitro analog of learning that a food is inedible provided insight into mechanisms underlying the learning. <i>Aplysia</i> learn to stop responding to a food when they attempt but fail to swallow it. Pairing a cholinergic agonist with an NO donor or histamine in the <i>Aplysia</i> cerebral ganglion produced significant decreases in fictive feeding in response to the cholinergic agonist alone. Acetylcholine (ACh) is the transmitter of chemoreceptors sensing food touching the lips. Nitric oxide (NO) and histamine (HA) signal failed attempts to swallow food. Reduced responses to the cholinergic agonist after pairing with NO or HA indicate that learning partially arises via a decreased response to ACh in the cerebral ganglion.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 11","pages":"278-281"},"PeriodicalIF":1.8,"publicationDate":"2023-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10631127/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"49679140","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.053771.123
Renee Y Chasse, Peter A Perrino, Ruth M McLeod, Gerry T M Altmann, R Holly Fitch
{"title":"A novel approach to the assessment of higher-order rule learning in male mice.","authors":"Renee Y Chasse, Peter A Perrino, Ruth M McLeod, Gerry T M Altmann, R Holly Fitch","doi":"10.1101/lm.053771.123","DOIUrl":"10.1101/lm.053771.123","url":null,"abstract":"<p><p>Historically, the development of valid and reliable methods for assessing higher-order cognitive abilities (e.g., rule learning and transfer) has been difficult in rodent models. To date, limited evidence supports the existence of higher cognitive abilities such as rule generation and complex decision-making in mice, rats, and rabbits. To this end, we sought to develop a task that would require mice to learn and transfer a rule. We trained mice to visually discriminate a series of images (image set, six total) of increasing complexity following three stages: (1) learn a visual target, (2) learn a rule (ignore any new images around the target), and finally (3) apply this rule in abstract form to a comparable but new image set. To evaluate learning for each stage, we measured (1) days (and performance by day) to discriminate the original target at criterion, (2) days (and performance by day) to get back to criterion when images in the set were altered by the introduction of distractors (rule learning), and (3) overall days (and performance by day) to criterion when experienced versus naïve cohorts of mice were tested on the same image set (rule transfer). Twenty-seven wild-type male C57 mice were tested using Bussey-Saksida touchscreen operant conditioning boxes (Lafayette Instruments). Two comparable black-white image sets were delivered sequentially (counterbalanced for order) to two identical cohorts of mice. Results showed that all mice were able to effectively learn their initial target image and could recall it >80 d later. We also found that mice were able to quickly learn and apply a \"rule\" : Ignore new distractors and continue to identify their visual target embedded in more complex images. The presence of rule learning was supported because performance criterion thresholds were regained much faster than initial learning when distractors were introduced. On the other hand, mice appeared unable to transfer this rule to a new set of stimuli. This is supported because visual discrimination curves for a new image set were no better than an initial (naïve) learning by a matched cohort of mice. Overall results have important implications for phenotyping research and particularly for the modeling of complex disorders in mice.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"30 10","pages":"271-277"},"PeriodicalIF":2.0,"publicationDate":"2023-10-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10561631/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41135457","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}