Extra-hypothalamic oxytocin neurons drive stress-induced social vigilance and avoidance

Duque-Wilckens, Natalia; Torres, Lisette Y.; Yokoyama, Sae; Minie, Vanessa A.; Tran, A.; Petkova, Stela P.; Hao, Rebecca; Ramos-Maciel, Stephanie; Rioa, R.; Jackson, K. A.; Flores-Ramirez, Francisco J.; Garcia-Carachure, Israel; Iñiguez, Sergio D.; Grinevich, Valery; Trainor, Brian C.

doi:10.1101/2020.06.02.129981

Cited by 11 publications

(12 citation statements)

References 71 publications

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“…We also found that stressed males showed significantly more vigilance than control males (p=0.0003) and there was a significant difference for stressed males to exhibit less vigilance than stressed females (p=0.002) (Fig 2E). These analyses are consistent with previous work showing the effects of social stress on vigilance are stronger in females than males 37 .…”

Section: Resultssupporting

confidence: 92%

“…We know the BNST plays a main role in the presentation of social anxiety behavior, which is driven by the activity of BNST oxytocin neurons. An infusion of oxytocin into the BNST of unstressed, adult male or female California mice is sufficient to induce social anxiety behaviors in both sexes 37 , and a systemic injection of OTA will attenuate social anxiety behaviors in stressed adult females 32 . Here we found the same was true in stressed male and female juveniles, with a 5mg/kg systemic OTA injection increasing social approach and reducing vigilance.…”

Section: Discussionmentioning

confidence: 99%

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Sexual differentiation of neural mechanisms of stress sensitivity during puberty

Wright

Culkin

Sekar

et al. 2020

Preprint

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Adolescence is an important developmental period during which anxiety-related behaviors differentiate in males and females. In humans anxiety prevalence increases to a greater degree in women than men after puberty, but the mechanism is unknown. We used social defeat stress to model anxiety behaviors in California mouse, a species in which aggressive females allow for comparison of social anxiety behaviors across sex. Adult female California mice show reduced social approach and increased social vigilance after exposure to stress, while these changes are weaker in males. Here we show that in juveniles, social defeat reduces social approach and increases social vigilance in both males and females. Next, we show that prepubertal castration sensitizes adult males to social defeat. However, when pubertal castration was paired with either testosterone or dihydrostesterone replacement, effects of defeat on social approach and vigilance were blunted in adult males. We also showed that effects of defeat on social behavior in juveniles were oxytocin receptor dependent, as has been described for adult females. This work highlights the importance of pubertal testosterone to the development of sex differences in anxiety behavior, and provides evidence that androgen receptors play an important role in the development of neural circuits of anxiety.

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Section: Resultssupporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Sexual differentiation of neural mechanisms of stress sensitivity during puberty

Wright

Culkin

Sekar

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Thus, it is possible that the relative activity of approach-driving and avoidance-driving cells in the NAc determines the final behavior output. It is worth noting that the BLA-NAc pathway is likely not the only pathway to drive defeat-induced social avoidance; other pathways involving the BNST and hypothalamus may also play a role (Diaz and Lin, 2020;Duque-Wilckens et al, 2020;Steinman et al, 2019).…”

Section: Neural Mechanism Mediating the Plasticity Of Social Behaviorsmentioning

confidence: 99%

Neural circuits of social behaviors: Innate yet flexible

Wei

Talwar

Lin

2021

Neuron

120

103

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“…On P21, one male and one female offspring per litter from each pre-versus postnatal housing condition was habituated to an open field arena for three-minutes (40 cm × 40 cm × 28 cm; Duque-Wilckens et al, 2020;Williams et al, 2020, n = 7-8). Behavior was recorded and videos scored using an automated behavioral monitoring software program (Cleversys TopScan, Reston, VA) to determine total distance traveled (cm) and percent of time spent in the center of the arena.…”

Section: Open Field and Social Preference Testsmentioning

confidence: 99%

Milking it for all it’s worth: The effects of environmental enrichment on maternal nurturance, lactation quality, and offspring social behavior

DeRosa

Tran

Kentner

2021

Preprint

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While alterations in the neonatal environment can have dramatic effects on offspring outcomes, the mechanisms that drive this phenomenon remain unclear. Breastfeeding confers robust benefits to offspring development, including those related to growth, immunity, and neurophysiology. Similarly, improving environmental complexity (i.e., environmental enrichment; EE) contributes developmental advantages to both humans and laboratory animal models. However, the impact of environmental context on maternal care and milk quality has not been thoroughly evaluated, nor are the biological underpinnings of EE on offspring development understood. Here, Sprague-Dawley rats were housed and bred in either EE or standard-housed (SD) conditions. Although EE dams gave birth to a larger number of pups, litters were standardized and cross-fostered across groups on postnatal day (P)1. Maternal milk samples were then collected on P1 (transitional milk phase) and P10 (mature milk phase) for analysis. While EE dams spent less time nursing, postnatal enrichment exposure was associated with heavier offspring bodyweights. Moreover, milk from EE dams had increased triglyceride levels compared to SD dams. Milk from EE mothers also contained a greater microbiome diversity and a significantly higher abundance of bacterial families related to bodyweight and energy metabolism. In addition to changes in lactational quality, we observed sex- and time-dependent effects of EE on offspring social behavior. Specifically, prenatal EE exposure was associated with greater sociability in females, while postnatal EE was associated with greater sociability in male offspring. Together, these results underscore the multidimensional impact of the combined neonatal and maternal environments on offspring development. These data also identify potential deficiencies in the quality of the "gold standard" laboratory housing condition and its impact on the welfare and design of translationally relevant animal models in biomedical research.

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Extra-hypothalamic oxytocin neurons drive stress-induced social vigilance and avoidance

Cited by 11 publications

References 71 publications

Sexual differentiation of neural mechanisms of stress sensitivity during puberty

Sexual differentiation of neural mechanisms of stress sensitivity during puberty

Neural circuits of social behaviors: Innate yet flexible

Milking it for all it’s worth: The effects of environmental enrichment on maternal nurturance, lactation quality, and offspring social behavior

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