Activation of oxytocin receptors, but not arginine-vasopressin V1a receptors, in the ventral tegmental area of male Syrian hamsters is essential for the reward-like properties of social interactions
•Social interaction between adult male Syrian hamsters reduces a place avoidance.•Inhibition of oxytocin receptors (OTR) in the VTA enhances a place avoidance.•Both oxytocin and AVP can activate OTRs in the VTA to reduce a place avoidance.•Activation and inhibition of AVP V1aRs in the VTA do not alt...
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description | •Social interaction between adult male Syrian hamsters reduces a place avoidance.•Inhibition of oxytocin receptors (OTR) in the VTA enhances a place avoidance.•Both oxytocin and AVP can activate OTRs in the VTA to reduce a place avoidance.•Activation and inhibition of AVP V1aRs in the VTA do not alter place preference/avoidance.
Social reward plays a fundamental role in shaping human and animal behavior. The rewarding nature of many forms of social behavior including sexual behavior, parental behavior, and social play has been revealed using well-established procedures such as the conditioned place preference test. Many motivated social behaviors are regulated by the nonapeptides oxytocin (OT) and arginine vasopressin (AVP) through their actions in multiple brain structures. Interestingly, there are few data on whether OT or AVP might contribute to the rewarding properties of social interaction by their actions within brain structures that play a key role in reward mechanisms such as the ventral tegmental area (VTA). The goal of the present study was to investigate the role of OT and AVP in the VTA in regulating the reward-like properties of social interactions. Social interactions between two male hamsters reduced a spontaneous place avoidance in hamsters injected with saline control. Interestingly, however, OT and AVP injected into the VTA induced a significant two-fold reduction in place avoidance for the social interaction chamber when compared to control injections of vehicle. Finally, because OT and AVP can act on each other’s receptors to influence social behavior, we also injected highly selective OTR and V1aR agonists and antagonists to determine whether OT or AVP V1a receptors were responsible for mediating the effects of these neuropeptides on social reward. Our results not only demonstrated that OT and AVP activate OTRs and not V1aRs to mediate social reward, they also demonstrated that the activation of OT receptors in the VTA is essential for the expression of the rewarding properties of social interactions. |
doi_str_mv | 10.1016/j.psyneuen.2016.09.001 |
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Social reward plays a fundamental role in shaping human and animal behavior. The rewarding nature of many forms of social behavior including sexual behavior, parental behavior, and social play has been revealed using well-established procedures such as the conditioned place preference test. Many motivated social behaviors are regulated by the nonapeptides oxytocin (OT) and arginine vasopressin (AVP) through their actions in multiple brain structures. Interestingly, there are few data on whether OT or AVP might contribute to the rewarding properties of social interaction by their actions within brain structures that play a key role in reward mechanisms such as the ventral tegmental area (VTA). The goal of the present study was to investigate the role of OT and AVP in the VTA in regulating the reward-like properties of social interactions. Social interactions between two male hamsters reduced a spontaneous place avoidance in hamsters injected with saline control. Interestingly, however, OT and AVP injected into the VTA induced a significant two-fold reduction in place avoidance for the social interaction chamber when compared to control injections of vehicle. Finally, because OT and AVP can act on each other’s receptors to influence social behavior, we also injected highly selective OTR and V1aR agonists and antagonists to determine whether OT or AVP V1a receptors were responsible for mediating the effects of these neuropeptides on social reward. Our results not only demonstrated that OT and AVP activate OTRs and not V1aRs to mediate social reward, they also demonstrated that the activation of OT receptors in the VTA is essential for the expression of the rewarding properties of social interactions.</description><identifier>ISSN: 0306-4530</identifier><identifier>EISSN: 1873-3360</identifier><identifier>DOI: 10.1016/j.psyneuen.2016.09.001</identifier><identifier>PMID: 27632574</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Animals ; Antidiuretic Hormone Receptor Antagonists - pharmacology ; Arginine Vasopressin - administration & dosage ; Arginine Vasopressin - pharmacology ; Arginine Vasopressin - physiology ; Behavior, Animal - physiology ; Conditioned place preference ; Cricetinae ; Dopamine ; Male ; Mesocricetus - metabolism ; Mesocricetus - physiology ; Mesolimbic dopamine system ; Neuropeptides ; Oxytocin - administration & dosage ; Oxytocin - pharmacology ; Oxytocin - physiology ; Receptors, Oxytocin - agonists ; Receptors, Oxytocin - antagonists & inhibitors ; Receptors, Oxytocin - physiology ; Receptors, Vasopressin - agonists ; Receptors, Vasopressin - physiology ; Reward ; Social Behavior ; Social interaction ; Social motivation ; Social salience ; Ventral Tegmental Area - drug effects ; Ventral Tegmental Area - metabolism ; Ventral Tegmental Area - physiology</subject><ispartof>Psychoneuroendocrinology, 2016-12, Vol.74, p.164-172</ispartof><rights>2016 Elsevier Ltd</rights><rights>Copyright © 2016 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c401t-53ef2a543f51e830f326e912af40936974e57948dd63cb1309201bbad289afb93</citedby><cites>FETCH-LOGICAL-c401t-53ef2a543f51e830f326e912af40936974e57948dd63cb1309201bbad289afb93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0306453016306357$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65534</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27632574$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Song, Zhimin</creatorcontrib><creatorcontrib>Borland, Johnathan M.</creatorcontrib><creatorcontrib>Larkin, Tony E.</creatorcontrib><creatorcontrib>O’Malley, Maureen</creatorcontrib><creatorcontrib>Albers, H. Elliott</creatorcontrib><title>Activation of oxytocin receptors, but not arginine-vasopressin V1a receptors, in the ventral tegmental area of male Syrian hamsters is essential for the reward-like properties of social interactions</title><title>Psychoneuroendocrinology</title><addtitle>Psychoneuroendocrinology</addtitle><description>•Social interaction between adult male Syrian hamsters reduces a place avoidance.•Inhibition of oxytocin receptors (OTR) in the VTA enhances a place avoidance.•Both oxytocin and AVP can activate OTRs in the VTA to reduce a place avoidance.•Activation and inhibition of AVP V1aRs in the VTA do not alter place preference/avoidance.
Social reward plays a fundamental role in shaping human and animal behavior. The rewarding nature of many forms of social behavior including sexual behavior, parental behavior, and social play has been revealed using well-established procedures such as the conditioned place preference test. Many motivated social behaviors are regulated by the nonapeptides oxytocin (OT) and arginine vasopressin (AVP) through their actions in multiple brain structures. Interestingly, there are few data on whether OT or AVP might contribute to the rewarding properties of social interaction by their actions within brain structures that play a key role in reward mechanisms such as the ventral tegmental area (VTA). The goal of the present study was to investigate the role of OT and AVP in the VTA in regulating the reward-like properties of social interactions. Social interactions between two male hamsters reduced a spontaneous place avoidance in hamsters injected with saline control. Interestingly, however, OT and AVP injected into the VTA induced a significant two-fold reduction in place avoidance for the social interaction chamber when compared to control injections of vehicle. Finally, because OT and AVP can act on each other’s receptors to influence social behavior, we also injected highly selective OTR and V1aR agonists and antagonists to determine whether OT or AVP V1a receptors were responsible for mediating the effects of these neuropeptides on social reward. Our results not only demonstrated that OT and AVP activate OTRs and not V1aRs to mediate social reward, they also demonstrated that the activation of OT receptors in the VTA is essential for the expression of the rewarding properties of social interactions.</description><subject>Animals</subject><subject>Antidiuretic Hormone Receptor Antagonists - pharmacology</subject><subject>Arginine Vasopressin - administration & dosage</subject><subject>Arginine Vasopressin - pharmacology</subject><subject>Arginine Vasopressin - physiology</subject><subject>Behavior, Animal - physiology</subject><subject>Conditioned place preference</subject><subject>Cricetinae</subject><subject>Dopamine</subject><subject>Male</subject><subject>Mesocricetus - metabolism</subject><subject>Mesocricetus - physiology</subject><subject>Mesolimbic dopamine system</subject><subject>Neuropeptides</subject><subject>Oxytocin - administration & dosage</subject><subject>Oxytocin - pharmacology</subject><subject>Oxytocin - physiology</subject><subject>Receptors, Oxytocin - agonists</subject><subject>Receptors, Oxytocin - antagonists & inhibitors</subject><subject>Receptors, Oxytocin - physiology</subject><subject>Receptors, Vasopressin - agonists</subject><subject>Receptors, Vasopressin - physiology</subject><subject>Reward</subject><subject>Social Behavior</subject><subject>Social interaction</subject><subject>Social motivation</subject><subject>Social salience</subject><subject>Ventral Tegmental Area - drug effects</subject><subject>Ventral Tegmental Area - metabolism</subject><subject>Ventral Tegmental Area - physiology</subject><issn>0306-4530</issn><issn>1873-3360</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk1v1DAQhi0EokvhL1Q-ciBhHCdOckFUFV9SJQ58XC3Hmex6SexgO1v2D_K7cNi2KidOHtvPvDMev4RcMMgZMPF6n8_haHFBmxdpn0ObA7BHZMOammecC3hMNsBBZGXF4Yw8C2EPAKIRxVNyVtSCF1VdbsjvSx3NQUXjLHUDdb-O0WljqUeNc3Q-vKLdEql1kSq_NdZYzA4quNljCIn7ztRDNp3EHdID2ujVSCNupxSmSHlUa4FJjUi_HL1Rlu7UFCL6QE2gSS2BJpGD8381PN4o32ej-YF09m5GHw2GVSOkDhNobEpWem09PCdPBjUGfHG7npNv7999vfqYXX_-8Onq8jrTJbCYVRyHQlUlHyqGDYeBFwJbVqihhJaLti6xqtuy6XvBdcc4tGm4Xaf6omnV0LX8nLw56c5LN2GvT--UszeT8kfplJH_3lizk1t3kKJkdQU8Cby8FfDu54IhyskEjeOoLLolSNbwilcAdZFQcUK1dyF4HO7LMJCrCeRe3plAriaQ0MpkgpR48bDJ-7S7X0_A2xOAaVQHg14GbdBq7E36yyh7Z_5X4w86Gs2g</recordid><startdate>20161201</startdate><enddate>20161201</enddate><creator>Song, Zhimin</creator><creator>Borland, Johnathan M.</creator><creator>Larkin, Tony E.</creator><creator>O’Malley, Maureen</creator><creator>Albers, H. Elliott</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20161201</creationdate><title>Activation of oxytocin receptors, but not arginine-vasopressin V1a receptors, in the ventral tegmental area of male Syrian hamsters is essential for the reward-like properties of social interactions</title><author>Song, Zhimin ; Borland, Johnathan M. ; Larkin, Tony E. ; O’Malley, Maureen ; Albers, H. Elliott</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c401t-53ef2a543f51e830f326e912af40936974e57948dd63cb1309201bbad289afb93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Antidiuretic Hormone Receptor Antagonists - pharmacology</topic><topic>Arginine Vasopressin - administration & dosage</topic><topic>Arginine Vasopressin - pharmacology</topic><topic>Arginine Vasopressin - physiology</topic><topic>Behavior, Animal - physiology</topic><topic>Conditioned place preference</topic><topic>Cricetinae</topic><topic>Dopamine</topic><topic>Male</topic><topic>Mesocricetus - metabolism</topic><topic>Mesocricetus - physiology</topic><topic>Mesolimbic dopamine system</topic><topic>Neuropeptides</topic><topic>Oxytocin - administration & dosage</topic><topic>Oxytocin - pharmacology</topic><topic>Oxytocin - physiology</topic><topic>Receptors, Oxytocin - agonists</topic><topic>Receptors, Oxytocin - antagonists & inhibitors</topic><topic>Receptors, Oxytocin - physiology</topic><topic>Receptors, Vasopressin - agonists</topic><topic>Receptors, Vasopressin - physiology</topic><topic>Reward</topic><topic>Social Behavior</topic><topic>Social interaction</topic><topic>Social motivation</topic><topic>Social salience</topic><topic>Ventral Tegmental Area - drug effects</topic><topic>Ventral Tegmental Area - metabolism</topic><topic>Ventral Tegmental Area - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Song, Zhimin</creatorcontrib><creatorcontrib>Borland, Johnathan M.</creatorcontrib><creatorcontrib>Larkin, Tony E.</creatorcontrib><creatorcontrib>O’Malley, Maureen</creatorcontrib><creatorcontrib>Albers, H. Elliott</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Psychoneuroendocrinology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Song, Zhimin</au><au>Borland, Johnathan M.</au><au>Larkin, Tony E.</au><au>O’Malley, Maureen</au><au>Albers, H. Elliott</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Activation of oxytocin receptors, but not arginine-vasopressin V1a receptors, in the ventral tegmental area of male Syrian hamsters is essential for the reward-like properties of social interactions</atitle><jtitle>Psychoneuroendocrinology</jtitle><addtitle>Psychoneuroendocrinology</addtitle><date>2016-12-01</date><risdate>2016</risdate><volume>74</volume><spage>164</spage><epage>172</epage><pages>164-172</pages><issn>0306-4530</issn><eissn>1873-3360</eissn><abstract>•Social interaction between adult male Syrian hamsters reduces a place avoidance.•Inhibition of oxytocin receptors (OTR) in the VTA enhances a place avoidance.•Both oxytocin and AVP can activate OTRs in the VTA to reduce a place avoidance.•Activation and inhibition of AVP V1aRs in the VTA do not alter place preference/avoidance.
Social reward plays a fundamental role in shaping human and animal behavior. The rewarding nature of many forms of social behavior including sexual behavior, parental behavior, and social play has been revealed using well-established procedures such as the conditioned place preference test. Many motivated social behaviors are regulated by the nonapeptides oxytocin (OT) and arginine vasopressin (AVP) through their actions in multiple brain structures. Interestingly, there are few data on whether OT or AVP might contribute to the rewarding properties of social interaction by their actions within brain structures that play a key role in reward mechanisms such as the ventral tegmental area (VTA). The goal of the present study was to investigate the role of OT and AVP in the VTA in regulating the reward-like properties of social interactions. Social interactions between two male hamsters reduced a spontaneous place avoidance in hamsters injected with saline control. Interestingly, however, OT and AVP injected into the VTA induced a significant two-fold reduction in place avoidance for the social interaction chamber when compared to control injections of vehicle. Finally, because OT and AVP can act on each other’s receptors to influence social behavior, we also injected highly selective OTR and V1aR agonists and antagonists to determine whether OT or AVP V1a receptors were responsible for mediating the effects of these neuropeptides on social reward. Our results not only demonstrated that OT and AVP activate OTRs and not V1aRs to mediate social reward, they also demonstrated that the activation of OT receptors in the VTA is essential for the expression of the rewarding properties of social interactions.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>27632574</pmid><doi>10.1016/j.psyneuen.2016.09.001</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Antidiuretic Hormone Receptor Antagonists - pharmacology Arginine Vasopressin - administration & dosage Arginine Vasopressin - pharmacology Arginine Vasopressin - physiology Behavior, Animal - physiology Conditioned place preference Cricetinae Dopamine Male Mesocricetus - metabolism Mesocricetus - physiology Mesolimbic dopamine system Neuropeptides Oxytocin - administration & dosage Oxytocin - pharmacology Oxytocin - physiology Receptors, Oxytocin - agonists Receptors, Oxytocin - antagonists & inhibitors Receptors, Oxytocin - physiology Receptors, Vasopressin - agonists Receptors, Vasopressin - physiology Reward Social Behavior Social interaction Social motivation Social salience Ventral Tegmental Area - drug effects Ventral Tegmental Area - metabolism Ventral Tegmental Area - physiology |
title | Activation of oxytocin receptors, but not arginine-vasopressin V1a receptors, in the ventral tegmental area of male Syrian hamsters is essential for the reward-like properties of social interactions |
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