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Naturally occurring low sociality in female rhesus monkeys: A tractable model for autism or not?
Molecular Autism ( IF 6.2 ) Pub Date : 2024-01-31 , DOI: 10.1186/s13229-024-00588-3
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

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. 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. 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. This study sample was small, and did not consider genetic, environmental, or other neurochemical measures that may be related to female mSRS-R scores. 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.

中文翻译:

雌性恒河猴天然存在的低社交性:是否是自闭症的易驯化模型?

自闭症谱系障碍 (ASD) 的特点是持续的社交互动障碍,并且患病率偏向男性。我们在雄性恒河猴中建立了自然发生的低社交性,作为自闭症谱系障碍社交特征的模型。低社会性的雄性猴子表现出社会互动减少和自闭症样特征负担增加,这两项指标都与低脑脊液(CSF)精氨酸加压素(AVP)浓度高度相关且密切相关。然而,人们对雌性恒河猴的行为和神经化学特征以及雌性恒河猴的低社交性是否是自闭症谱系障碍的易处理模型知之甚少。在非繁殖季节,对 N = 88 只户外饲养的雌性恒河猴进行了社会行为评估(行为学观察;反向翻译的自闭症特征测量量表,猕猴社会反应量表修订版 [mSRS-R])。从非社会行为频率分布的 N = 16 只猴子的子集中收集脑脊液和血液样本,并对 AVP 和催产素 (OXT) 浓度进行量化。使用一般线性模型分析数据。非社会行为频率和 mSRS-R 评分在一般雌性猴子群体中连续分布,正如之前在雄性猴子中发现的那样。然而,优势等级显着预测了雌性的 mSRS-R 分数,排名较高的个体表现出较少的自闭症样特征,这种关系以前在该群体的雄性中没有观察到。女性在其他几个方面与男性不同:社会行为频率与 mSRS-R 评分无关,AVP 浓度与任何社会行为指标无关。女性血液和脑脊液 AVP 浓度呈正相关;没有发现涉及任何 OXT 测量的显着关系。这项研究样本很小,并且没有考虑可能与女性 mSRS-R 评分相关的遗传、环境或其他神经化学指标。优势等级是雌性恒河猴中自闭症样特征最重要的预测因子,并且脑脊液神经肽浓度与雌性社会功能的测量无关(与先前在雄性恒河猴以及雄性和雌性自闭症儿童中的脑脊液 AVP 研究结果相反)。尽管是初步的,但这一证据表明,该物种强大的母系组织可能会限制雌性恒河猴作为自闭症谱系障碍模型的低社会性的有用性。
更新日期:2024-01-31
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