Megan Kelly, Merrick Garner, Emily M Cooper, Caitlin A Orsini
{"title":"Cholinergic regulation of decision making under risk of punishment.","authors":"Megan Kelly, Merrick Garner, Emily M Cooper, Caitlin A Orsini","doi":"10.1016/j.nlm.2024.108018","DOIUrl":"https://doi.org/10.1016/j.nlm.2024.108018","url":null,"abstract":"<p><p>The ability to choose between options that differ in their risks and rewards depends on brain regions within the mesocorticolimbic circuit and regulation of their activity by neurotransmitter systems. Dopamine neurotransmission in particular plays a critical role in modulating such risk-taking behavior; however, the contribution of other major modulatory neurotransmitters, such as acetylcholine, is not as well-defined, especially for decision making in which the risk associated with more rewarding outcomes involves adverse consequences. Consequently, the goal of the current experiments was to examine how cholinergic signaling influences decision making involving risk of explicit punishment. Male and female rats were trained in a decision-making task in which they chose between a small safe food reward and a larger food reward accompanied by a risk of footshock punishment. After training in this task, the effects of nicotinic and muscarinic agonists and antagonists on risk-taking performance were evaluated. Neither nicotine, a nicotinic receptor agonist, nor mecamylamine, a nicotinic receptor antagonist, affected preference for the risky lever, although mecamylamine did alter latencies to press the risky lever and the percentage of omissions. The muscarinic receptor agonist oxotremorine decreased preference for the large, risky lever; similar effects on behavior were observed with the administration of the muscarinic receptor antagonist scopolamine. Control experiments were therefore conducted in which these same muscarinic receptor ligands were administered prior to testing in a reward discrimination task. These experiments revealed that the effects of oxotremorine and scopolamine on risk taking may be due to altered motivational processes rather than to changes in sensitivity to risk of punishment. Importantly, there were no sex differences in the effects of cholinergic manipulations on preference for the large, risky lever. Collectively, these findings suggest that in both males and females, cholinergic signaling via muscarinic receptors is involved in decision making involving risk of explicit punishment, with a specific role in modulating sensitivity to differences in reward magnitude. Future studies will expand upon this work by exploring whether targeting cholinergic receptors has therapeutic potential for psychiatric conditions in which risk taking is pathologically altered.</p>","PeriodicalId":19102,"journal":{"name":"Neurobiology of Learning and Memory","volume":" ","pages":"108018"},"PeriodicalIF":2.2,"publicationDate":"2024-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142877509","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Grace L Minnes, Anna J Wiener, Audrey S Pisahl, Elizabeth A Duecker, Boula A Baskhairoun, Sharoderick C Lowe, Nicholas W Simon
{"title":"Effects of maternal separation on punishment-driven risky decision making in adolescence and adulthood.","authors":"Grace L Minnes, Anna J Wiener, Audrey S Pisahl, Elizabeth A Duecker, Boula A Baskhairoun, Sharoderick C Lowe, Nicholas W Simon","doi":"10.1016/j.nlm.2024.108016","DOIUrl":"10.1016/j.nlm.2024.108016","url":null,"abstract":"<p><p>Early life adversity (ELA) is associated with a multitude of neural and behavioral aberrations. To develop treatments to mitigate the effects of ELA, it is critical to determine which aspects of cognition are affected and when these disturbances manifest across the lifespan. Here, we tested the effects of maternal separation, an established rodent model of ELA, on punishment-driven risky decision-making longitudinally in both adolescence (25-55 days old) and adulthood (80-100 days old). Risk-taking was assessed with the Risky Decision-making Task, wherein rats choose between a small, safe reward and a large reward accompanied by an escalating risk of punishment (foot shock). We observed that rats exposed to maternal separation were more prone to risk-taking than controls during adolescence, and demonstrated reduced latency to make both risky and safe decisions. Interestingly, this augmented risk-taking was no longer evident in adulthood. Males and females displayed comparable levels of risk-taking during adolescence then diverged in adulthood, with adult males displaying a sharp increase in risk-taking. Finally, we observed that risk-taking changed across the lifespan in rats exposed to maternal separation, but not in control rats. Collectively, these data reveal that ELA engenders risk-taking in adolescence but not adulthood, and that sex differences in risky decision-making are not evident until adulthood. This has important implications for the development of both behavioral and biological treatments to improve decision-making during the vulnerable adolescent period.</p>","PeriodicalId":19102,"journal":{"name":"Neurobiology of Learning and Memory","volume":" ","pages":"108016"},"PeriodicalIF":2.2,"publicationDate":"2024-12-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142872700","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Olivia S O'Neill, Karley V George, Emily P Minard, Boyer D Winters
{"title":"Overcoming boundary conditions for object location memory destabilization in male rats involves dopamine D1 receptor activation.","authors":"Olivia S O'Neill, Karley V George, Emily P Minard, Boyer D Winters","doi":"10.1016/j.nlm.2024.108017","DOIUrl":"10.1016/j.nlm.2024.108017","url":null,"abstract":"<p><p>Consolidated long-term memories can undergo strength or content modification via protein synthesis-dependent reconsolidation. This is the process by which a reminder cue initiates reactivation of the memory trace, triggering destabilization. Older and more strongly encoded spatial memories can resist destabilization due to biological boundary conditions. The present study investigated the role of dopamine (DA) at D1 receptors (D1Rs) in object location memory destabilization and overcoming boundary conditions for older (\"remote\"; tested with a 48-h rather than a 24-h delay between sample and reactivation) memory destabilization. Using male rats in a modified object location task, we found that administering the D1R antagonist SCH23390 (0.1 mg/kg, i.p.) prior to reactivation blocked destabilization of recently encoded memories, as well as novelty-induced destabilization of remote memories. Using remote parameters, systemically administered D1R agonist SKF38393 (5 mg/kg, i.p.) induced destabilization of remote object location memories in the absence of salient novelty. Intra-dorsal hippocampus administration of SCH23390 (2 μg/μL) also blocked destabilization of remote object location memories when a salient novel cue was present. These results are consistent with previous findings implicating DA in memory destabilization as well as demonstrate a role for D1-receptor activation in the destabilization of boundary condition protected-object location memories.</p>","PeriodicalId":19102,"journal":{"name":"Neurobiology of Learning and Memory","volume":" ","pages":"108017"},"PeriodicalIF":2.2,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142854708","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Shoko Arai, Krzysztof A Sypniewski, Constantine Pavlides
{"title":"Differential roles of medial/lateral entorhinal cortex in spatial/object memory and contribution to hippocampal functional neuronal organization.","authors":"Shoko Arai, Krzysztof A Sypniewski, Constantine Pavlides","doi":"10.1016/j.nlm.2024.108015","DOIUrl":"10.1016/j.nlm.2024.108015","url":null,"abstract":"<p><p>Episodic memory is subserved by interactions between entorhinal cortex (EC) and hippocampus. Within EC, a functional dissociation has been proposed for medial (MEC) and lateral (LEC) subregions, whereby, MEC processes spatial information while LEC processes information about objects and their location in space. Most of these studies, however, used classical methods which lack both spatial and temporal specificity, thus, the precise role of MEC/LEC in memory could use further clarification. First, we show a possible functional dissociation of MEC/LEC for place/object fear memory, by optogenetic suppression of these areas during memory acquisition. The main output of EC is to the hippocampus. MEC projects mainly towards proximal/superficial CA1 and deep CA3 while LEC towards distal/deep CA1 and superficial CA3. Dentate gyrus (DG), terminations of MEC/LEC are dissociated septotemporally. A functional dissociation has also been proposed for subregions of the hippocampus. Previous studies reported that proximal/distal CA1 process spatial/nonspatial information, respectively. For the second part of the study, we used the immediate-early gene Zif-268 to map neuronal activity in CA1. We first show enhanced Zif-268 expression and cluster-type organization in the proximal CA1 by place exposure and enhanced Zif-268 expression/cluster organization in distal CA1 following object exposure. Second, direct optogenetic stimulation of MEC/LEC, produced a similar enhancement/cluster-type organization in the same areas. Enhanced Zif-268 expression was also observed in CA3 and DG. These results substantiate previous findings and are proof positive that the hippocampus is organized in clusters to encode information generally ascribed to this structure.</p>","PeriodicalId":19102,"journal":{"name":"Neurobiology of Learning and Memory","volume":" ","pages":"108015"},"PeriodicalIF":2.2,"publicationDate":"2024-12-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142846744","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Evan J. Ciacciarelli , Scott D. Dunn , Taqdees Gohar , T. Joseph Sloand , Mark Niedringhaus , Elizabeth A. West
{"title":"Medial prefrontal cortex to nucleus reuniens circuit is critical for performance in an operant delayed nonmatch to position task","authors":"Evan J. Ciacciarelli , Scott D. Dunn , Taqdees Gohar , T. Joseph Sloand , Mark Niedringhaus , Elizabeth A. West","doi":"10.1016/j.nlm.2024.108007","DOIUrl":"10.1016/j.nlm.2024.108007","url":null,"abstract":"<div><div>Working memory refers to the temporary retention of a small amount of information used in the execution of a cognitive task. The prefrontal cortex and its connections with thalamic subregions are thought to mediate specific aspects of working memory, including engaging with the hippocampus to mediate memory retrieval. We used an operant delayed-non match to position task, which does not require the hippocampus, to determine roles of the rodent medial prefrontal cortex (mPFC), the nucleus reuniens thalamic region (RE), and their connection. We found that transient inactivation of the mPFC and RE using the GABA-A agonist muscimol led to a delay-independent reduction in behavioral performance in the delayed non-match to position paradigm. We used a chemogenetic approach to determine the directionality of the necessary circuitry for behavioral performance reliant on working memory. Specifically, when we targeted mPFC neurons that project to the RE (mPFC-RE) we found a delay-independent reduction in the delayed non-match to position task, but not when we targeted RE neurons that project to the mPFC (RE-mPFC). Our results suggest a broader role for the mPFC-RE circuit in mediating working memory beyond the connection with the hippocampus.</div></div>","PeriodicalId":19102,"journal":{"name":"Neurobiology of Learning and Memory","volume":"217 ","pages":"Article 108007"},"PeriodicalIF":2.2,"publicationDate":"2024-11-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142716750","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sophie Jano , Alex Chatburn , Zachariah R. Cross , Matthias Schlesewsky , Ina Bornkessel-Schlesewsky
{"title":"How predictability and individual alpha frequency shape memory: Insights from an event-related potential investigation","authors":"Sophie Jano , Alex Chatburn , Zachariah R. Cross , Matthias Schlesewsky , Ina Bornkessel-Schlesewsky","doi":"10.1016/j.nlm.2024.108006","DOIUrl":"10.1016/j.nlm.2024.108006","url":null,"abstract":"<div><div>Prediction and memory are strongly intertwined, with predictions relying on memory retrieval, whilst also influencing memory encoding. However, it is unclear how predictability influences explicit memory performance, and how individual neural factors may modulate this relationship. The current study sought to investigate the effect of predictability on memory processing with an analysis of the N400 event-related potential in a context extending beyond language. Participants (<em>N</em> = 48, females = 33) completed a study-test paradigm where they first viewed predictable and unpredictable four-item ‘ABCD’ sequences of outdoor scene images, whilst their brain activity was recorded using electroencephalography. Subsequently, their memory for the images was tested, and N400 patterns during learning were compared with memory outcomes. Behavioural results revealed better memory for images in predictable sequences in contrast to unpredictable sequences. Memory was also strongest for predictable images in the ‘B’ position, suggesting that when processing longer sequences, the brain may prioritise the data deemed most informative. Strikingly, greater N400 amplitudes during learning were associated with enhanced memory at test for individuals with low versus high individual alpha frequencies. In light of the relationship between the N400 and stimulus predictability, this finding may imply that predictive processing differs between individuals to influence the extent of memory encoding. Finally, exploratory analyses provided evidence for a later positivity that was predictive of subsequent memory performance. Ultimately, the results highlight the complex and interconnected relationship between predictive processing and memory, whilst shedding light on the accumulation of predictions across longer sequences.</div></div>","PeriodicalId":19102,"journal":{"name":"Neurobiology of Learning and Memory","volume":"216 ","pages":"Article 108006"},"PeriodicalIF":2.2,"publicationDate":"2024-11-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142682474","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Dev Laxman Subramanian, Adam M.P. Miller, David M. Smith
{"title":"The retrosplenial cortical role in delayed spatial alternation","authors":"Dev Laxman Subramanian, Adam M.P. Miller, David M. Smith","doi":"10.1016/j.nlm.2024.108005","DOIUrl":"10.1016/j.nlm.2024.108005","url":null,"abstract":"<div><div>The retrosplenial cortex (RSC) plays an important role in spatial cognition. RSC neurons exhibit a variety of spatial firing patterns and lesion studies have found that the RSC is necessary for spatial working memory tasks. However, little is known about how RSC neurons might encode spatial memory during a delay period. In the present study, we trained control rats and rats with excitotoxic lesions of the RSC on spatial alternation task with varying delay durations and in a separate group of rats, we recorded RSC neuronal activity as the rats performed the alternation task. We found that RSC lesions significantly impaired alternation performance, particularly at the longest delay duration. We also found that RSC neurons exhibited reliably different firing patterns throughout the delay periods preceding left and right trials, consistent with a working memory signal. These differential firing patterns were absent during the delay periods preceding errors. We also found that many RSC neurons exhibit a large spike in firing rate leading up to the start of the trial. Many of these trial start responses also differentiated left and right trials, suggesting that they could play a role in priming the ‘go left’ or ‘go right’ behavioral responses. Our results suggest that these firing patterns represent critical memory information that underlies the RSC role in spatial working memory.</div></div>","PeriodicalId":19102,"journal":{"name":"Neurobiology of Learning and Memory","volume":"216 ","pages":"Article 108005"},"PeriodicalIF":2.2,"publicationDate":"2024-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142624624","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Victoria R. Heimer-McGinn , Taylor B. Wise , Emma R. Halter , Dominique Martin , Victoria L. Templer
{"title":"Attentional processing in the rat dorsal posterior parietal cortex","authors":"Victoria R. Heimer-McGinn , Taylor B. Wise , Emma R. Halter , Dominique Martin , Victoria L. Templer","doi":"10.1016/j.nlm.2024.108004","DOIUrl":"10.1016/j.nlm.2024.108004","url":null,"abstract":"<div><div>The human posterior parietal cortex (PPC) is known to support sustained attention. Specifically, top-down attention is generally processed in dorsal regions while bottom-up regulation occurs more ventrally. In rodent models, however, it is still unclear whether the PPC is required for sustained attention, or whether there is a similar functional dissociation between anatomical regions. Consequently, the aim of this study was to investigate the contribution of the rodent dorsal PPC (dPPC) in sustained attention. We used the five-choice serial reaction time task (5CSRTT) and compared rats with neurotoxic dPPC lesions to sham operated rats. We found that rats with dPPC lesions were less accurate and took longer to make correct choices, indicating impaired attention and reduced processing speed. This effect, however, was limited to the first few days of post-operative testing. After an apparent recovery, omissions became elevated in the lesion group, which, in the absence of reduced motivation and mobility, can also be interpreted as impaired attention. In subsequent challenge probes, the lesion group displayed globally elevated latency to make a correct response, indicating reduced processing speed. No differences in premature responses or perseverative responses were observed at any time, demonstrating that dPPC lesions did not affect impulsivity and compulsivity. This pattern of behavior suggests that while intact dPPC supports goal-driven (top-down) modulation of attention, it likely does not play a central role in processing stimulus-driven (bottom-up) attention. Furthermore, compensatory mechanisms can support sustained attention in the absence of a fully functioning dPPC, although this occurs at the expense of processing speed. Our results inform the literature by confirming that rodent PPC is involved in regulating sustained attention and providing preliminary evidence for a functional dissociation between top-down and bottom-up attentional processing.</div></div>","PeriodicalId":19102,"journal":{"name":"Neurobiology of Learning and Memory","volume":"216 ","pages":"Article 108004"},"PeriodicalIF":2.2,"publicationDate":"2024-10-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142564803","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Yvonne Y. Chen , Kathryn J.M. Lambert , Christopher R. Madan , Anthony Singhal
{"title":"Motor-related oscillations reveal the involvement of sensorimotor processes during recognition memory","authors":"Yvonne Y. Chen , Kathryn J.M. Lambert , Christopher R. Madan , Anthony Singhal","doi":"10.1016/j.nlm.2024.108003","DOIUrl":"10.1016/j.nlm.2024.108003","url":null,"abstract":"<div><div>Certain object properties may render an item as more memorable than others. One such property is manipulability, or the extent to which an object can be interacted with using our hands. This study sought to determine if the manipulability of an item modulates memory task performance on both a behavioural and neural level. We recorded electroencephalography (EEG) from a large sample of right-handed individuals (N = 53) during a visual item recognition memory task. The task contained stimuli of both high and low manipulability. Analysis focused on activity in the theta rhythm (3.5–7 Hz), which has been implicated in sensorimotor integration, and the mu rhythm (8–14 Hz), the primary oscillation associated with sensorimotor related behaviours. At both encoding and retrieval, theta oscillations were greater over the left motor region for high manipulability stimuli, suggesting that an item’s sensorimotor properties are assessed immediately upon presentation. Manipulability did not affect activity in the mu rhythm. However, mu oscillations over the left motor region were lower during the retrieval of old versus new items and response time was faster for old items, aligning with the cortical reinstatement hypothesis. These results collectively reveal an association between motor oscillations and memory processes, highlight the involvement of sensorimotor processing at both encoding and retrieval.</div></div>","PeriodicalId":19102,"journal":{"name":"Neurobiology of Learning and Memory","volume":"216 ","pages":"Article 108003"},"PeriodicalIF":2.2,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142558324","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Pattern separation during encoding and Subsequent Memory Effect","authors":"Laura García-Rueda , Claudia Poch , Pablo Campo","doi":"10.1016/j.nlm.2024.107995","DOIUrl":"10.1016/j.nlm.2024.107995","url":null,"abstract":"<div><div>Memory retrieval has been extensively studied in relation to the encoding processes that precede access to stored information. Event related potentials (ERP) research has compared brain potentials elicited during the study phase of successful and unsuccessful retrieval, finding greater activation for the subsequent retrieval information. In this work we were interested in exploring the neural markers associated to subsequent recognition when similar memories are subsequently encoded. We used a Subsequent Memory paradigm in which we manipulated the number of similar items within a category (2 or 6) that participants encoded. Manipulating the number of similar encoded items within a category allowed us to test whether encoding markers of subsequent recognition depend solely on memory trace strength or, on the contrary, successful recognition is influenced by subsequently presented similar memories, and consequently may not be reflected in higher activation in such cases. After a 20-minute period, participants performed a recognition task providing one of a three-option judgement: “old”, “similar” and “new”, which allowed us to test if the amplitude of ERP waveforms varied based on the similarity judgement of the unrecognized encoded item. We did not observe a significant parietal subsequent memory effect, however, old hits and similar false alarms were both significantly different from similar correct rejections and old false alarms in ERP retrieval. These findings suggest that differences in brain responses between conditions are specifically related to the retrieval process and not the encoding process, indicating potential differential effects on memory during retrieval. Moreover, it is also possible that differences in brain responses develop or change over the rest time between phases, influencing how these conditions manifest across different stages of information processing.</div></div>","PeriodicalId":19102,"journal":{"name":"Neurobiology of Learning and Memory","volume":"216 ","pages":"Article 107995"},"PeriodicalIF":2.2,"publicationDate":"2024-10-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142470769","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}