Naturally occurring low sociality in female rhesus monkeys: A tractable model for autism or not?
Abstract Background Autism spectrum disorder (ASD) is characterized by persistent social interaction impairments and is male-biased in prevalence. We have established naturally occurring low sociality in male rhesus monkeys as a model for the social features of ASD. Low-social male monkeys exhibit r...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | Molecular Autism |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13229-024-00588-3 |
| _version_ | 1797274383789588480 |
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| author | Ozge Oztan Laura A. Del Rosso Sierra M. Simmons Duyen K. K. Nguyen Catherine F. Talbot John P. Capitanio Joseph P. Garner Karen J. Parker |
| author_facet | Ozge Oztan Laura A. Del Rosso Sierra M. Simmons Duyen K. K. Nguyen Catherine F. Talbot John P. Capitanio Joseph P. Garner Karen J. Parker |
| author_sort | Ozge Oztan |
| collection | DOAJ |
| description | Abstract Background Autism spectrum disorder (ASD) is characterized by persistent social interaction impairments and is male-biased in prevalence. We have established naturally occurring low sociality in male rhesus monkeys as a model for the social features of ASD. Low-social male monkeys exhibit reduced social interactions and increased autistic-like trait burden, with both measures highly correlated and strongly linked to low cerebrospinal fluid (CSF) arginine vasopressin (AVP) concentration. Little is known, however, about the behavioral and neurochemical profiles of female rhesus monkeys, and whether low sociality in females is a tractable model for ASD. Methods Social behavior assessments (ethological observations; a reverse-translated autistic trait measurement scale, the macaque Social Responsiveness Scale-Revised [mSRS-R]) were completed on N = 88 outdoor-housed female rhesus monkeys during the non-breeding season. CSF and blood samples were collected from a subset of N = 16 monkeys across the frequency distribution of non-social behavior, and AVP and oxytocin (OXT) concentrations were quantified. Data were analyzed using general linear models. Results Non-social behavior frequency and mSRS-R scores were continuously distributed across the general female monkey population, as previously found for male monkeys. However, dominance rank significantly predicted mSRS-R scores in females, with higher-ranking individuals showing fewer autistic-like traits, a relationship not previously observed in males from this colony. Females differed from males in several other respects: Social behavior frequencies were unrelated to mSRS-R scores, and AVP concentration was unrelated to any social behavior measure. Blood and CSF concentrations of AVP were positively correlated in females; no significant relationship involving any OXT measure was found. Limitations This study sample was small, and did not consider genetic, environmental, or other neurochemical measures that may be related to female mSRS-R scores. Conclusions Dominance rank is the most significant predictor of autistic-like traits in female rhesus monkeys, and CSF neuropeptide concentrations are unrelated to measures of female social functioning (in contrast to prior CSF AVP findings in male rhesus monkeys and male and female autistic children). Although preliminary, this evidence suggests that the strong matrilineal organization of this species may limit the usefulness of low sociality in female rhesus monkeys as a tractable model for ASD. |
| first_indexed | 2024-03-07T14:58:36Z |
| format | Article |
| id | doaj.art-92ecf179cbed4e238f0be28b93579e70 |
| institution | Directory Open Access Journal |
| issn | 2040-2392 |
| language | English |
| last_indexed | 2024-03-07T14:58:36Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Molecular Autism |
| spelling | doaj.art-92ecf179cbed4e238f0be28b93579e702024-03-05T19:19:07ZengBMCMolecular Autism2040-23922024-01-0115111110.1186/s13229-024-00588-3Naturally occurring low sociality in female rhesus monkeys: A tractable model for autism or not?Ozge Oztan0Laura A. Del Rosso1Sierra M. Simmons2Duyen K. K. Nguyen3Catherine F. Talbot4John P. Capitanio5Joseph P. Garner6Karen J. Parker7Department of Psychiatry and Behavioral Sciences, Stanford UniversityCalifornia National Primate Research CenterCalifornia National Primate Research CenterDepartment of Psychiatry and Behavioral Sciences, Stanford UniversityCalifornia National Primate Research CenterCalifornia National Primate Research CenterDepartment of Psychiatry and Behavioral Sciences, Stanford UniversityDepartment of Psychiatry and Behavioral Sciences, Stanford UniversityAbstract Background Autism spectrum disorder (ASD) is characterized by persistent social interaction impairments and is male-biased in prevalence. We have established naturally occurring low sociality in male rhesus monkeys as a model for the social features of ASD. Low-social male monkeys exhibit reduced social interactions and increased autistic-like trait burden, with both measures highly correlated and strongly linked to low cerebrospinal fluid (CSF) arginine vasopressin (AVP) concentration. Little is known, however, about the behavioral and neurochemical profiles of female rhesus monkeys, and whether low sociality in females is a tractable model for ASD. Methods Social behavior assessments (ethological observations; a reverse-translated autistic trait measurement scale, the macaque Social Responsiveness Scale-Revised [mSRS-R]) were completed on N = 88 outdoor-housed female rhesus monkeys during the non-breeding season. CSF and blood samples were collected from a subset of N = 16 monkeys across the frequency distribution of non-social behavior, and AVP and oxytocin (OXT) concentrations were quantified. Data were analyzed using general linear models. Results Non-social behavior frequency and mSRS-R scores were continuously distributed across the general female monkey population, as previously found for male monkeys. However, dominance rank significantly predicted mSRS-R scores in females, with higher-ranking individuals showing fewer autistic-like traits, a relationship not previously observed in males from this colony. Females differed from males in several other respects: Social behavior frequencies were unrelated to mSRS-R scores, and AVP concentration was unrelated to any social behavior measure. Blood and CSF concentrations of AVP were positively correlated in females; no significant relationship involving any OXT measure was found. Limitations This study sample was small, and did not consider genetic, environmental, or other neurochemical measures that may be related to female mSRS-R scores. Conclusions Dominance rank is the most significant predictor of autistic-like traits in female rhesus monkeys, and CSF neuropeptide concentrations are unrelated to measures of female social functioning (in contrast to prior CSF AVP findings in male rhesus monkeys and male and female autistic children). Although preliminary, this evidence suggests that the strong matrilineal organization of this species may limit the usefulness of low sociality in female rhesus monkeys as a tractable model for ASD.https://doi.org/10.1186/s13229-024-00588-3Animal modelArginine vasopressinAutism spectrum disorderCerebrospinal fluidDominance rankFemale |
| spellingShingle | Ozge Oztan Laura A. Del Rosso Sierra M. Simmons Duyen K. K. Nguyen Catherine F. Talbot John P. Capitanio Joseph P. Garner Karen J. Parker Naturally occurring low sociality in female rhesus monkeys: A tractable model for autism or not? Molecular Autism Animal model Arginine vasopressin Autism spectrum disorder Cerebrospinal fluid Dominance rank Female |
| title | Naturally occurring low sociality in female rhesus monkeys: A tractable model for autism or not? |
| title_full | Naturally occurring low sociality in female rhesus monkeys: A tractable model for autism or not? |
| title_fullStr | Naturally occurring low sociality in female rhesus monkeys: A tractable model for autism or not? |
| title_full_unstemmed | Naturally occurring low sociality in female rhesus monkeys: A tractable model for autism or not? |
| title_short | Naturally occurring low sociality in female rhesus monkeys: A tractable model for autism or not? |
| title_sort | naturally occurring low sociality in female rhesus monkeys a tractable model for autism or not |
| topic | Animal model Arginine vasopressin Autism spectrum disorder Cerebrospinal fluid Dominance rank Female |
| url | https://doi.org/10.1186/s13229-024-00588-3 |
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