Pub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053807.123
Andrew M Davidson, Toshihide Hige
Across animal species, dopamine-operated memory systems comprise anatomically segregated, functionally diverse subsystems. Although individual subsystems could operate independently to support distinct types of memory, the logical interplay between subsystems is expected to enable more complex memory processing by allowing existing memory to influence future learning. Recent comprehensive ultrastructural analysis of the Drosophila mushroom body revealed intricate networks interconnecting the dopamine subsystems-the mushroom body compartments. Here, we review the functions of some of these connections that are beginning to be understood. Memory consolidation is mediated by two different forms of network: A recurrent feedback loop within a compartment maintains sustained dopamine activity required for consolidation, whereas feed-forward connections across compartments allow short-term memory formation in one compartment to open the gate for long-term memory formation in another compartment. Extinction and reversal of aversive memory rely on a similar feed-forward circuit motif that signals omission of punishment as a reward, which triggers plasticity that counteracts the original aversive memory trace. Finally, indirect feed-forward connections from a long-term memory compartment to short-term memory compartments mediate higher-order conditioning. Collectively, these emerging studies indicate that feedback control and hierarchical connectivity allow the dopamine subsystems to work cooperatively to support diverse and complex forms of learning.
{"title":"Roles of feedback and feed-forward networks of dopamine subsystems: insights from <i>Drosophila</i> studies.","authors":"Andrew M Davidson, Toshihide Hige","doi":"10.1101/lm.053807.123","DOIUrl":"10.1101/lm.053807.123","url":null,"abstract":"<p><p>Across animal species, dopamine-operated memory systems comprise anatomically segregated, functionally diverse subsystems. Although individual subsystems could operate independently to support distinct types of memory, the logical interplay between subsystems is expected to enable more complex memory processing by allowing existing memory to influence future learning. Recent comprehensive ultrastructural analysis of the <i>Drosophila</i> mushroom body revealed intricate networks interconnecting the dopamine subsystems-the mushroom body compartments. Here, we review the functions of some of these connections that are beginning to be understood. Memory consolidation is mediated by two different forms of network: A recurrent feedback loop within a compartment maintains sustained dopamine activity required for consolidation, whereas feed-forward connections across compartments allow short-term memory formation in one compartment to open the gate for long-term memory formation in another compartment. Extinction and reversal of aversive memory rely on a similar feed-forward circuit motif that signals omission of punishment as a reward, which triggers plasticity that counteracts the original aversive memory trace. Finally, indirect feed-forward connections from a long-term memory compartment to short-term memory compartments mediate higher-order conditioning. Collectively, these emerging studies indicate that feedback control and hierarchical connectivity allow the dopamine subsystems to work cooperatively to support diverse and complex forms of learning.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199952/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306207","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}
Pub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053894.123
Hans V Alten
{"title":"The Phylogeny of the Hymenopteran Brain.","authors":"Hans V Alten","doi":"10.1101/lm.053894.123","DOIUrl":"10.1101/lm.053894.123","url":null,"abstract":"","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199943/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306210","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}
Pub Date : 2024-05-13Print Date: 2024-04-01DOI: 10.1101/lm.053891.123
Nina Becker, Simone Kühn, Andreas Olsson
Emotional stimuli are usually remembered with high confidence. Yet, it remains unknown whether-in addition to memory for the emotional stimulus itself-memory for a neutral stimulus encountered just after an emotional one can be enhanced. Further, little is known about the interplay between emotion elicited by a stimulus and emotion relating to affective dispositions. To address these questions, we examined (1) how emotional valence and arousal of a context image preceding a neutral item image affect memory of the item, and (2) how such memory modulation is affected by two hallmark features of emotional disorders: trait negative affect and tendency to worry. In two experiments, participants encoded a series of trials in which an emotional (negative, neutral, or positive) context image was followed by a neutral item image. In experiment 1 (n = 42), items presented seconds after negative context images were remembered better and with greater confidence compared to those presented after neutral and positive ones. Arousal ratings of negative context images were higher compared to neutral and positive ones and the likelihood of correctly recognizing an item image was related to higher arousal of the context image. In experiment 2 (n = 59), better item memory was related to lower trait negative affect. Participants with lower trait negative affect or tendency to worry displayed higher confidence compared to those with high negative affect or tendency to worry. Our findings describe an emotional "carry-over" effect elicited by a context image that enhances subsequent item memory on a trial-by-trial basis, however, not in individuals with high trait negative affect who seem to have a general memory disadvantage.
{"title":"How emotional contexts modulate item memory in individuals with high and low negative affect and worry.","authors":"Nina Becker, Simone Kühn, Andreas Olsson","doi":"10.1101/lm.053891.123","DOIUrl":"10.1101/lm.053891.123","url":null,"abstract":"<p><p>Emotional stimuli are usually remembered with high confidence. Yet, it remains unknown whether-in addition to memory for the emotional stimulus itself-memory for a neutral stimulus encountered just after an emotional one can be enhanced. Further, little is known about the interplay between emotion elicited by a stimulus and emotion relating to affective dispositions. To address these questions, we examined (1) how emotional valence and arousal of a context image preceding a neutral item image affect memory of the item, and (2) how such memory modulation is affected by two hallmark features of emotional disorders: trait negative affect and tendency to worry. In two experiments, participants encoded a series of trials in which an emotional (negative, neutral, or positive) context image was followed by a neutral item image. In experiment 1 (<i>n</i> = 42), items presented seconds after negative context images were remembered better and with greater confidence compared to those presented after neutral and positive ones. Arousal ratings of negative context images were higher compared to neutral and positive ones and the likelihood of correctly recognizing an item image was related to higher arousal of the context image. In experiment 2 (<i>n</i> = 59), better item memory was related to lower trait negative affect. Participants with lower trait negative affect or tendency to worry displayed higher confidence compared to those with high negative affect or tendency to worry. Our findings describe an emotional \"carry-over\" effect elicited by a context image that enhances subsequent item memory on a trial-by-trial basis, however, not in individuals with high trait negative affect who seem to have a general memory disadvantage.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 4","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-05-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11098457/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140916656","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}
Exposure-based therapy is effective in treating anxiety, but a return of fear in the form of relapse is common. Exposure is based on the extinction of Pavlovian fear conditioning. Both animal and human studies point to increased arousal during immediate compared to delayed extinction (>+24 h), which presumably impairs extinction learning and increases the subsequent return of fear. Impaired extinction learning under arousal might interfere with psychotherapeutic interventions. The aim of the present study was to investigate whether arousal before extinction differs between extinction groups and whether arousal before extinction predicts the return of fear in a later (retention) test. As a highlight, both the time between fear acquisition and extinction (immediate vs. delayed) and the time between extinction and test (early vs. late test) were systematically varied. We performed follow-up analyses on data from 103 young, healthy participants to test the above hypotheses. Subjective arousal ratings and physiological arousal measures of sympathetic and hypothalamic pituitary adrenal axis activation (tonic skin conductance and salivary cortisol) were collected. Increased pre-extinction arousal in the immediate extinction group was only confirmed for subjective arousal. In linear regression analyses, none of the arousal measures predicted a significant return of fear in the different experimental groups. Only when we aggregated across the two test groups, tonic skin conductance at the onset of extinction predicted the return of fear in skin conductance responses. The overall results provide little evidence that pre-extinction arousal affects subsequent extinction learning and memory. In terms of clinical relevance, there is no clear evidence that exposure could be improved by reducing subjective or physiological arousal.
{"title":"The impact of extinction timing on pre-extinction arousal and subsequent return of fear","authors":"Miriam Kampa, Rudolf Stark, Tim Klucken","doi":"10.1101/lm.053902.123","DOIUrl":"https://doi.org/10.1101/lm.053902.123","url":null,"abstract":"Exposure-based therapy is effective in treating anxiety, but a return of fear in the form of relapse is common. Exposure is based on the extinction of Pavlovian fear conditioning. Both animal and human studies point to increased arousal during immediate compared to delayed extinction (>+24 h), which presumably impairs extinction learning and increases the subsequent return of fear. Impaired extinction learning under arousal might interfere with psychotherapeutic interventions. The aim of the present study was to investigate whether arousal before extinction differs between extinction groups and whether arousal before extinction predicts the return of fear in a later (retention) test. As a highlight, both the time between fear acquisition and extinction (immediate vs. delayed) and the time between extinction and test (early vs. late test) were systematically varied. We performed follow-up analyses on data from 103 young, healthy participants to test the above hypotheses. Subjective arousal ratings and physiological arousal measures of sympathetic and hypothalamic pituitary adrenal axis activation (tonic skin conductance and salivary cortisol) were collected. Increased pre-extinction arousal in the immediate extinction group was only confirmed for subjective arousal. In linear regression analyses, none of the arousal measures predicted a significant return of fear in the different experimental groups. Only when we aggregated across the two test groups, tonic skin conductance at the onset of extinction predicted the return of fear in skin conductance responses. The overall results provide little evidence that pre-extinction arousal affects subsequent extinction learning and memory. In terms of clinical relevance, there is no clear evidence that exposure could be improved by reducing subjective or physiological arousal.","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"74 1","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140613208","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Much like recalling autobiographical memories, constructing imagined autobiographical events depends on episodic memory processes. The ability to imagine events contributes to several future-oriented behaviors (e.g., decision-making, problem solving), which relies, in part, on the ability to remember the imagined events. A factor affecting the memorability of such events is their adherence to event schemas—conceptualizations of how events generally unfold. In the current study, we examined how two aspects of event schemas—event expectancy and familiarity—affect the ability to recall imagined events. Participants first imagined and described in detail autobiographical events that either aligned with or deviated from an event, expected to occur in a context (e.g., a kitchen) that was either familiar or unfamiliar. This resulted in imaginations ranging from maximally schema-congruent (expected events in a familiar context) to maximally novel (unexpected events in an unfamiliar context). Twenty-four hours later, participants recalled these imagined events. Recollections were scored for the number of reinstated details from the imaginations and the number of newly added details. We found greater reinstatement of details for both the maximally congruent and maximally novel events, while maximally novel events were recalled more precisely than other events (i.e., fewer added details). Our results indicate a complementary benefit to remembering schematic and novel imagined events, which may guide equally important but distinct future-oriented behaviors.
{"title":"Remembering what we imagine: the role of event schemas in shaping how imagined autobiographical events are recalled","authors":"Can Fenerci, Bianca Adjei, Signy Sheldon","doi":"10.1101/lm.053993.124","DOIUrl":"https://doi.org/10.1101/lm.053993.124","url":null,"abstract":"Much like recalling autobiographical memories, constructing imagined autobiographical events depends on episodic memory processes. The ability to imagine events contributes to several future-oriented behaviors (e.g., decision-making, problem solving), which relies, in part, on the ability to remember the imagined events. A factor affecting the memorability of such events is their adherence to event schemas—conceptualizations of how events generally unfold. In the current study, we examined how two aspects of event schemas—event expectancy and familiarity—affect the ability to recall imagined events. Participants first imagined and described in detail autobiographical events that either aligned with or deviated from an event, expected to occur in a context (e.g., a kitchen) that was either familiar or unfamiliar. This resulted in imaginations ranging from maximally schema-congruent (expected events in a familiar context) to maximally novel (unexpected events in an unfamiliar context). Twenty-four hours later, participants recalled these imagined events. Recollections were scored for the number of reinstated details from the imaginations and the number of newly added details. We found greater reinstatement of details for both the maximally congruent and maximally novel events, while maximally novel events were recalled more precisely than other events (i.e., fewer added details). Our results indicate a complementary benefit to remembering schematic and novel imagined events, which may guide equally important but distinct future-oriented behaviors.","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"26 1","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140827492","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-03-25Print Date: 2024-03-01DOI: 10.1101/lm.053901.123
Hillary A Raab, Noam Goldway, Careen Foord, Catherine A Hartley
From early in life, we encounter both controllable environments, in which our actions can causally influence the reward outcomes we experience, and uncontrollable environments, in which they cannot. Environmental controllability is theoretically proposed to organize our behavior. In controllable contexts, we can learn to proactively select instrumental actions that bring about desired outcomes. In uncontrollable environments, Pavlovian learning enables hard-wired, reflexive reactions to anticipated, motivationally salient events, providing "default" behavioral responses. Previous studies characterizing the balance between Pavlovian and instrumental learning systems across development have yielded divergent findings, with some studies observing heightened expression of Pavlovian learning during adolescence and others observing a reduced influence of Pavlovian learning during this developmental stage. In this study, we aimed to investigate whether a theoretical model of controllability-dependent arbitration between learning systems might explain these seemingly divergent findings in the developmental literature, with the specific hypothesis that adolescents' action selection might be particularly sensitive to environmental controllability. To test this hypothesis, 90 participants, aged 8-27, performed a probabilistic-learning task that enables estimation of Pavlovian influence on instrumental learning, across both controllable and uncontrollable conditions. We fit participants' data with a reinforcement-learning model in which controllability inferences adaptively modulate the dominance of Pavlovian versus instrumental control. Relative to children and adults, adolescents exhibited greater flexibility in calibrating the expression of Pavlovian bias to the degree of environmental controllability. These findings suggest that sensitivity to environmental reward statistics that organize motivated behavior may be heightened during adolescence.
{"title":"Adolescents flexibly adapt action selection based on controllability inferences.","authors":"Hillary A Raab, Noam Goldway, Careen Foord, Catherine A Hartley","doi":"10.1101/lm.053901.123","DOIUrl":"10.1101/lm.053901.123","url":null,"abstract":"<p><p>From early in life, we encounter both controllable environments, in which our actions can causally influence the reward outcomes we experience, and uncontrollable environments, in which they cannot. Environmental controllability is theoretically proposed to organize our behavior. In controllable contexts, we can learn to proactively select instrumental actions that bring about desired outcomes. In uncontrollable environments, Pavlovian learning enables hard-wired, reflexive reactions to anticipated, motivationally salient events, providing \"default\" behavioral responses. Previous studies characterizing the balance between Pavlovian and instrumental learning systems across development have yielded divergent findings, with some studies observing heightened expression of Pavlovian learning during adolescence and others observing a reduced influence of Pavlovian learning during this developmental stage. In this study, we aimed to investigate whether a theoretical model of controllability-dependent arbitration between learning systems might explain these seemingly divergent findings in the developmental literature, with the specific hypothesis that adolescents' action selection might be particularly sensitive to environmental controllability. To test this hypothesis, 90 participants, aged 8-27, performed a probabilistic-learning task that enables estimation of Pavlovian influence on instrumental learning, across both controllable and uncontrollable conditions. We fit participants' data with a reinforcement-learning model in which controllability inferences adaptively modulate the dominance of Pavlovian versus instrumental control. Relative to children and adults, adolescents exhibited greater flexibility in calibrating the expression of Pavlovian bias to the degree of environmental controllability. These findings suggest that sensitivity to environmental reward statistics that organize motivated behavior may be heightened during adolescence.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 3","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-03-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11000582/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140288469","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}
Lapses in attention can negatively impact later memory of an experience. Attention and encoding resources are thought to decline as more experiences are encountered in succession, accounting for the primacy effect in which memory is better for items encountered early compared to late in a study list. However, accessing prior knowledge during study can facilitate subsequent memory, suggesting a potential avenue to counteract this decline. Here, we investigated the extent to which semantic associations—shared meaning between experiences—can counteract declines in encoding resources. Our hypothesis is that semantic associations restore neural encoding mechanisms, which in turn improves memory. We recorded scalp electroencephalography (EEG) while male and female human participants performed a delayed free recall task. Half of the items from late in each study list were semantically associated with an item presented earlier in the list. We find that semantic associations improve memory specifically for late list items and selectively modulate the neural signals engaged during the study of late list items. Relative to other recalled items, late list items that are subsequently semantically clustered—recalled consecutively with their semantic associate—elicit increased high-frequency activity and decreased low-frequency activity, a hallmark of successful encoding. Our findings demonstrate that semantic associations restore neural encoding mechanisms and improve later memory. More broadly, these findings suggest that prior knowledge modulates the orientation of attention to influence encoding mechanisms.
{"title":"Semantic associations restore neural encoding mechanisms","authors":"Isabelle L. Moore, Nicole M. Long","doi":"10.1101/lm.053996.124","DOIUrl":"https://doi.org/10.1101/lm.053996.124","url":null,"abstract":"Lapses in attention can negatively impact later memory of an experience. Attention and encoding resources are thought to decline as more experiences are encountered in succession, accounting for the primacy effect in which memory is better for items encountered early compared to late in a study list. However, accessing prior knowledge during study can facilitate subsequent memory, suggesting a potential avenue to counteract this decline. Here, we investigated the extent to which semantic associations—shared meaning between experiences—can counteract declines in encoding resources. Our hypothesis is that semantic associations restore neural encoding mechanisms, which in turn improves memory. We recorded scalp electroencephalography (EEG) while male and female human participants performed a delayed free recall task. Half of the items from late in each study list were semantically associated with an item presented earlier in the list. We find that semantic associations improve memory specifically for late list items and selectively modulate the neural signals engaged during the study of late list items. Relative to other recalled items, late list items that are subsequently semantically clustered—recalled consecutively with their semantic associate—elicit increased high-frequency activity and decreased low-frequency activity, a hallmark of successful encoding. Our findings demonstrate that semantic associations restore neural encoding mechanisms and improve later memory. More broadly, these findings suggest that prior knowledge modulates the orientation of attention to influence encoding mechanisms.","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"38 1","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140171566","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Shaghayegh Navabpour, Kayla Farrell, Shannon E. Kincaid, Nour Omar, Madeline Musaus, Yu Lin, Hehuang Xie, Timothy J. Jarome
Posttranslational modification of histone proteins is critical for memory formation. Recently, we showed that monoubiquitination of histone H2B at lysine 120 (H2Bub) is critical for memory formation in the hippocampus. However, the transcriptome controlled by H2Bub remains unknown. Here, we found that fear conditioning in male rats increased or decreased the expression of 86 genes in the hippocampus but, surprisingly, siRNA-mediated knockdown of the H2Bub ligase, Rnf20, abolished changes in all but one of these genes. These findings suggest that monoubiquitination of histone H2B is a crucial regulator of the transcriptome during memory formation.
{"title":"Monoubiquitination of histone H2B is a crucial regulator of the transcriptome during memory formation","authors":"Shaghayegh Navabpour, Kayla Farrell, Shannon E. Kincaid, Nour Omar, Madeline Musaus, Yu Lin, Hehuang Xie, Timothy J. Jarome","doi":"10.1101/lm.053912.123","DOIUrl":"https://doi.org/10.1101/lm.053912.123","url":null,"abstract":"Posttranslational modification of histone proteins is critical for memory formation. Recently, we showed that monoubiquitination of histone H2B at lysine 120 (H2Bub) is critical for memory formation in the hippocampus. However, the transcriptome controlled by H2Bub remains unknown. Here, we found that fear conditioning in male rats increased or decreased the expression of 86 genes in the hippocampus but, surprisingly, siRNA-mediated knockdown of the H2Bub ligase, <em>Rnf20</em>, abolished changes in all but one of these genes. These findings suggest that monoubiquitination of histone H2B is a crucial regulator of the transcriptome during memory formation.","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"59 1","pages":""},"PeriodicalIF":2.0,"publicationDate":"2024-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140585601","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-02-26Print Date: 2024-01-01DOI: 10.1101/lm.053892.123
Michelle Surets, Albit Caban-Murillo, Steve Ramirez
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.
{"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":2.0,"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}
Pub Date : 2024-01-29Print Date: 2024-01-01DOI: 10.1101/lm.053871.123
Timothy J Onofrychuk, Aiden E Glass, Quentin Greba, John G Howland
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.
{"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":2.0,"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}