Erica A Cross, Johnathan M Borland, Emma K Shaughnessy, Susan D Lee, Vivian Vu, Elizabeth A Sambor, Robert L Meisel, Kim L Huhman, H Elliott Albers
{"title":"中边缘多巴胺系统中不同的亚回路编码社会刺激的显著性和效价。","authors":"Erica A Cross, Johnathan M Borland, Emma K Shaughnessy, Susan D Lee, Vivian Vu, Elizabeth A Sambor, Robert L Meisel, Kim L Huhman, H Elliott Albers","doi":"10.1007/s00213-025-06793-z","DOIUrl":null,"url":null,"abstract":"<p><strong>Rationale: </strong>The mesolimbic dopamine (DA) system (MDS) is the canonical \"reward\" pathway that has been studied extensively in the context of the rewarding properties of food and drugs of abuse. In contrast, little is known about the role of the MDS in the processing of the rewarding and aversive properties of social stimuli.</p><p><strong>Objective: </strong>Social interactions can be characterized by their salience (i.e., importance) and their rewarding or aversive properties (i.e., valence). Here, we test the novel hypothesis that projections from the medial ventral tegmental area (VTA) to the nucleus accumbens (NAc) core code the salience of social stimuli through phasic release of DA in response to rewarding and aversive social stimuli. In contrast, lateral VTA (lVTA) projections to the NAc shell are proposed to encode social valence, with increased tonic DA signaling rewarding interactions and decreased tonic DA signaling aversive ones.</p><p><strong>Methods: </strong>Using DA amperometry, which monitors DA signaling with a high degree of temporal and anatomical resolution, we measured DA release in the NAc core or shell during rewarding and aversive social interactions. Anatomical and functional studies were conducted utilizing retrograde tracing and immunohistochemistry.</p><p><strong>Results: </strong>These studies support the hypothesis that distinct MDS subcircuits (i.e., mVTA to NAc core and lVTA to NAc shell) signal the salience and valence, respectively, of social stimuli.</p><p><strong>Conclusion: </strong>Together, these data provide a novel conceptualization of how functional and anatomical heterogeneity within the MDS detect and distinguish between social salience, social reward, and social aversion.</p>","PeriodicalId":20783,"journal":{"name":"Psychopharmacology","volume":" ","pages":""},"PeriodicalIF":3.5000,"publicationDate":"2025-04-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Distinct subcircuits within the mesolimbic dopamine system encode the salience and valence of social stimuli.\",\"authors\":\"Erica A Cross, Johnathan M Borland, Emma K Shaughnessy, Susan D Lee, Vivian Vu, Elizabeth A Sambor, Robert L Meisel, Kim L Huhman, H Elliott Albers\",\"doi\":\"10.1007/s00213-025-06793-z\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Rationale: </strong>The mesolimbic dopamine (DA) system (MDS) is the canonical \\\"reward\\\" pathway that has been studied extensively in the context of the rewarding properties of food and drugs of abuse. In contrast, little is known about the role of the MDS in the processing of the rewarding and aversive properties of social stimuli.</p><p><strong>Objective: </strong>Social interactions can be characterized by their salience (i.e., importance) and their rewarding or aversive properties (i.e., valence). Here, we test the novel hypothesis that projections from the medial ventral tegmental area (VTA) to the nucleus accumbens (NAc) core code the salience of social stimuli through phasic release of DA in response to rewarding and aversive social stimuli. In contrast, lateral VTA (lVTA) projections to the NAc shell are proposed to encode social valence, with increased tonic DA signaling rewarding interactions and decreased tonic DA signaling aversive ones.</p><p><strong>Methods: </strong>Using DA amperometry, which monitors DA signaling with a high degree of temporal and anatomical resolution, we measured DA release in the NAc core or shell during rewarding and aversive social interactions. Anatomical and functional studies were conducted utilizing retrograde tracing and immunohistochemistry.</p><p><strong>Results: </strong>These studies support the hypothesis that distinct MDS subcircuits (i.e., mVTA to NAc core and lVTA to NAc shell) signal the salience and valence, respectively, of social stimuli.</p><p><strong>Conclusion: </strong>Together, these data provide a novel conceptualization of how functional and anatomical heterogeneity within the MDS detect and distinguish between social salience, social reward, and social aversion.</p>\",\"PeriodicalId\":20783,\"journal\":{\"name\":\"Psychopharmacology\",\"volume\":\" \",\"pages\":\"\"},\"PeriodicalIF\":3.5000,\"publicationDate\":\"2025-04-18\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Psychopharmacology\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1007/s00213-025-06793-z\",\"RegionNum\":3,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"NEUROSCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Psychopharmacology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1007/s00213-025-06793-z","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
Distinct subcircuits within the mesolimbic dopamine system encode the salience and valence of social stimuli.
Rationale: The mesolimbic dopamine (DA) system (MDS) is the canonical "reward" pathway that has been studied extensively in the context of the rewarding properties of food and drugs of abuse. In contrast, little is known about the role of the MDS in the processing of the rewarding and aversive properties of social stimuli.
Objective: Social interactions can be characterized by their salience (i.e., importance) and their rewarding or aversive properties (i.e., valence). Here, we test the novel hypothesis that projections from the medial ventral tegmental area (VTA) to the nucleus accumbens (NAc) core code the salience of social stimuli through phasic release of DA in response to rewarding and aversive social stimuli. In contrast, lateral VTA (lVTA) projections to the NAc shell are proposed to encode social valence, with increased tonic DA signaling rewarding interactions and decreased tonic DA signaling aversive ones.
Methods: Using DA amperometry, which monitors DA signaling with a high degree of temporal and anatomical resolution, we measured DA release in the NAc core or shell during rewarding and aversive social interactions. Anatomical and functional studies were conducted utilizing retrograde tracing and immunohistochemistry.
Results: These studies support the hypothesis that distinct MDS subcircuits (i.e., mVTA to NAc core and lVTA to NAc shell) signal the salience and valence, respectively, of social stimuli.
Conclusion: Together, these data provide a novel conceptualization of how functional and anatomical heterogeneity within the MDS detect and distinguish between social salience, social reward, and social aversion.
期刊介绍:
Official Journal of the European Behavioural Pharmacology Society (EBPS)
Psychopharmacology is an international journal that covers the broad topic of elucidating mechanisms by which drugs affect behavior. The scope of the journal encompasses the following fields:
Human Psychopharmacology: Experimental
This section includes manuscripts describing the effects of drugs on mood, behavior, cognition and physiology in humans. The journal encourages submissions that involve brain imaging, genetics, neuroendocrinology, and developmental topics. Usually manuscripts in this section describe studies conducted under controlled conditions, but occasionally descriptive or observational studies are also considered.
Human Psychopharmacology: Clinical and Translational
This section comprises studies addressing the broad intersection of drugs and psychiatric illness. This includes not only clinical trials and studies of drug usage and metabolism, drug surveillance, and pharmacoepidemiology, but also work utilizing the entire range of clinically relevant methodologies, including neuroimaging, pharmacogenetics, cognitive science, biomarkers, and others. Work directed toward the translation of preclinical to clinical knowledge is especially encouraged. The key feature of submissions to this section is that they involve a focus on clinical aspects.
Preclinical psychopharmacology: Behavioral and Neural
This section considers reports on the effects of compounds with defined chemical structures on any aspect of behavior, in particular when correlated with neurochemical effects, in species other than humans. Manuscripts containing neuroscientific techniques in combination with behavior are welcome. We encourage reports of studies that provide insight into the mechanisms of drug action, at the behavioral and molecular levels.
Preclinical Psychopharmacology: Translational
This section considers manuscripts that enhance the confidence in a central mechanism that could be of therapeutic value for psychiatric or neurological patients, using disease-relevant preclinical models and tests, or that report on preclinical manipulations and challenges that have the potential to be translated to the clinic. Studies aiming at the refinement of preclinical models based upon clinical findings (back-translation) will also be considered. The journal particularly encourages submissions that integrate measures of target tissue exposure, activity on the molecular target and/or modulation of the targeted biochemical pathways.
Preclinical Psychopharmacology: Molecular, Genetic and Epigenetic
This section focuses on the molecular and cellular actions of neuropharmacological agents / drugs, and the identification / validation of drug targets affecting the CNS in health and disease. We particularly encourage studies that provide insight into the mechanisms of drug action at the molecular level. Manuscripts containing evidence for genetic or epigenetic effects on neurochemistry or behavior are welcome.