Wildtype peers rescue social play and 50-kHz ultrasonic vocalization deficits in juvenile female Cacna1c heterozygous rats
BackgroundHealthy brain development depends on early social practices and experiences. The risk gene CACNA1C is implicated in numerous neuropsychiatric disorders, in which key characteristics include deficits in social functioning and communication. Recently, we reported sex-dependent impairments in...
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| Format: | Article |
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Frontiers Media S.A.
2023-08-01
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| Series: | Frontiers in Behavioral Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnbeh.2023.1190272/full |
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| author | Rebecca Bogdan Rukhshona Kayumova Rainer K. W. Schwarting Rainer K. W. Schwarting Markus Wöhr Markus Wöhr Markus Wöhr Markus Wöhr Theresa M. Kisko Theresa M. Kisko Theresa M. Kisko Theresa M. Kisko |
| author_facet | Rebecca Bogdan Rukhshona Kayumova Rainer K. W. Schwarting Rainer K. W. Schwarting Markus Wöhr Markus Wöhr Markus Wöhr Markus Wöhr Theresa M. Kisko Theresa M. Kisko Theresa M. Kisko Theresa M. Kisko |
| author_sort | Rebecca Bogdan |
| collection | DOAJ |
| description | BackgroundHealthy brain development depends on early social practices and experiences. The risk gene CACNA1C is implicated in numerous neuropsychiatric disorders, in which key characteristics include deficits in social functioning and communication. Recently, we reported sex-dependent impairments in social behavior and ultrasonic vocalizations (USV) in juvenile heterozygous Cacna1c+/− (HET) rats. Specifically, HET females displayed increases in rough-and-tumble play that eliminated the typically observed sex difference between male and female rats. Interestingly, female wild-type Cacna1c+/+ (WT) pairs also showed a similar increase in social play when housed with HET females, suggesting their behavior may be influenced by HET cage mates. This indicates that the genetic makeup of the social environment related to Cacna1c can influence social play, yet systematic studies are lacking.MethodsIn the present study, we housed juvenile females in MIXED- or SAME-genotype cages and tested them in a social play paradigm with a same- and opposite-genotype partner.ResultsThe results show that the early social environment and the genotype of the play partner influence social play and 50-kHz USV emission. Experience with a WT play partner appears necessary for HET females to show comparable levels of play and 50-kHz USV emission. Same-genotype HET pairs played less and emitted fewer 50-kHz USV than same-genotype WT or opposite-genotype pairs; however, we found that the decrease in social play and 50-kHz USV in HET pairs can be rescued by playing with a WT partner. The effect was particularly prominent when the first play partner was WT, as we found it increased play and 50-kHz USV emission in all subsequent interactions with ensuing partners.ConclusionThese findings suggest that the genetic makeup related to the social environment and/or social peers influences social play in Cacna1c+/− haploinsufficient rats. Specifically, our results show that WT peers can rescue behavior and communication alterations in Cacna1c female rats. Our findings have important implications because they show that the genetic makeup of the social environment can divulge phenotypic changes in genetic rat models of neuropsychiatric disorders. |
| first_indexed | 2024-03-12T17:43:51Z |
| format | Article |
| id | doaj.art-96b96acaaf6e43cd8c0c5f612a8553c6 |
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| issn | 1662-5153 |
| language | English |
| last_indexed | 2024-03-12T17:43:51Z |
| publishDate | 2023-08-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Behavioral Neuroscience |
| spelling | doaj.art-96b96acaaf6e43cd8c0c5f612a8553c62023-08-03T23:16:09ZengFrontiers Media S.A.Frontiers in Behavioral Neuroscience1662-51532023-08-011710.3389/fnbeh.2023.11902721190272Wildtype peers rescue social play and 50-kHz ultrasonic vocalization deficits in juvenile female Cacna1c heterozygous ratsRebecca Bogdan0Rukhshona Kayumova1Rainer K. W. Schwarting2Rainer K. W. Schwarting3Markus Wöhr4Markus Wöhr5Markus Wöhr6Markus Wöhr7Theresa M. Kisko8Theresa M. Kisko9Theresa M. Kisko10Theresa M. Kisko11Behavioral Neuroscience, Experimental and Biological Psychology, Faculty of Psychology, Philipps-University Marburg, Marburg, GermanyBehavioral Neuroscience, Experimental and Biological Psychology, Faculty of Psychology, Philipps-University Marburg, Marburg, GermanyBehavioral Neuroscience, Experimental and Biological Psychology, Faculty of Psychology, Philipps-University Marburg, Marburg, GermanyCentre for Mind, Brain, and Behavior (CMBB), Philipps-University Marburg, Marburg, GermanyBehavioral Neuroscience, Experimental and Biological Psychology, Faculty of Psychology, Philipps-University Marburg, Marburg, GermanyCentre for Mind, Brain, and Behavior (CMBB), Philipps-University Marburg, Marburg, GermanySocial and Affective Neuroscience Research Group, Laboratory of Biological Psychology, Research Unit Brain and Cognition, Faculty of Psychology and Educational Sciences, KU Leuven, Leuven, BelgiumLeuven Brain Institute, KU Leuven, Leuven, BelgiumBehavioral Neuroscience, Experimental and Biological Psychology, Faculty of Psychology, Philipps-University Marburg, Marburg, GermanyCentre for Mind, Brain, and Behavior (CMBB), Philipps-University Marburg, Marburg, GermanySocial and Affective Neuroscience Research Group, Laboratory of Biological Psychology, Research Unit Brain and Cognition, Faculty of Psychology and Educational Sciences, KU Leuven, Leuven, BelgiumLeuven Brain Institute, KU Leuven, Leuven, BelgiumBackgroundHealthy brain development depends on early social practices and experiences. The risk gene CACNA1C is implicated in numerous neuropsychiatric disorders, in which key characteristics include deficits in social functioning and communication. Recently, we reported sex-dependent impairments in social behavior and ultrasonic vocalizations (USV) in juvenile heterozygous Cacna1c+/− (HET) rats. Specifically, HET females displayed increases in rough-and-tumble play that eliminated the typically observed sex difference between male and female rats. Interestingly, female wild-type Cacna1c+/+ (WT) pairs also showed a similar increase in social play when housed with HET females, suggesting their behavior may be influenced by HET cage mates. This indicates that the genetic makeup of the social environment related to Cacna1c can influence social play, yet systematic studies are lacking.MethodsIn the present study, we housed juvenile females in MIXED- or SAME-genotype cages and tested them in a social play paradigm with a same- and opposite-genotype partner.ResultsThe results show that the early social environment and the genotype of the play partner influence social play and 50-kHz USV emission. Experience with a WT play partner appears necessary for HET females to show comparable levels of play and 50-kHz USV emission. Same-genotype HET pairs played less and emitted fewer 50-kHz USV than same-genotype WT or opposite-genotype pairs; however, we found that the decrease in social play and 50-kHz USV in HET pairs can be rescued by playing with a WT partner. The effect was particularly prominent when the first play partner was WT, as we found it increased play and 50-kHz USV emission in all subsequent interactions with ensuing partners.ConclusionThese findings suggest that the genetic makeup related to the social environment and/or social peers influences social play in Cacna1c+/− haploinsufficient rats. Specifically, our results show that WT peers can rescue behavior and communication alterations in Cacna1c female rats. Our findings have important implications because they show that the genetic makeup of the social environment can divulge phenotypic changes in genetic rat models of neuropsychiatric disorders.https://www.frontiersin.org/articles/10.3389/fnbeh.2023.1190272/fullCav1.2calciumrough-and-tumble playultrasonic communicationsocial environmentdevelopment |
| spellingShingle | Rebecca Bogdan Rukhshona Kayumova Rainer K. W. Schwarting Rainer K. W. Schwarting Markus Wöhr Markus Wöhr Markus Wöhr Markus Wöhr Theresa M. Kisko Theresa M. Kisko Theresa M. Kisko Theresa M. Kisko Wildtype peers rescue social play and 50-kHz ultrasonic vocalization deficits in juvenile female Cacna1c heterozygous rats Frontiers in Behavioral Neuroscience Cav1.2 calcium rough-and-tumble play ultrasonic communication social environment development |
| title | Wildtype peers rescue social play and 50-kHz ultrasonic vocalization deficits in juvenile female Cacna1c heterozygous rats |
| title_full | Wildtype peers rescue social play and 50-kHz ultrasonic vocalization deficits in juvenile female Cacna1c heterozygous rats |
| title_fullStr | Wildtype peers rescue social play and 50-kHz ultrasonic vocalization deficits in juvenile female Cacna1c heterozygous rats |
| title_full_unstemmed | Wildtype peers rescue social play and 50-kHz ultrasonic vocalization deficits in juvenile female Cacna1c heterozygous rats |
| title_short | Wildtype peers rescue social play and 50-kHz ultrasonic vocalization deficits in juvenile female Cacna1c heterozygous rats |
| title_sort | wildtype peers rescue social play and 50 khz ultrasonic vocalization deficits in juvenile female cacna1c heterozygous rats |
| topic | Cav1.2 calcium rough-and-tumble play ultrasonic communication social environment development |
| url | https://www.frontiersin.org/articles/10.3389/fnbeh.2023.1190272/full |
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