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Oxytocin receptor disruption in Avil-expressing cells results in blunted sociability and increased inter-male aggression.

ABSTRACT: Social behaviors are foundational to society and quality of life while social behavior extremes are core symptoms in a variety of psychopathologies and developmental disabilities. Oxytocin (OXT) is a neuroactive hormone that regulates social behaviors through its receptor (OXTR), with all previously identified social behavior effects attributed to the central nervous system, which has developmental origins in the neural tube. However, OXTR are also present in neural crest-derived tissue including sensory ganglia of the peripheral nervous system. Avil encodes for the actin-binding protein ADVILLIN, is expressed in neural crest-derived cells, and was therefore used as a target in this study to knock out OXTR expression in neural-crest derived cells. Here, we tested if OXTRs specifically expressed in Avil positive neural crest-derived cells are necessary for species-typical adult social behaviors using a Cre-LoxP strategy. Genetically modified male and female mice lacking OXTR in Avil expressing cells (OXTRAvil KO) were tested for sociability and preference for social novelty. Males were also tested for resident intruder aggression. OXTRAvil KO males and females had reduced sociability compared to OXTRAvil WT controls. Additionally, OXTRAvil KO males had increased aggressive behaviors compared to controls. These data indicate that OXTRs in cells of neural crest origin are important regulators of typical social behaviors in C57BL/6J adult male and female mice and point to needed directions of future research.

SUBMITTER: Tabbaa M

PROVIDER: S-EPMC8631681 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Successfully navigating social interactions requires the precise and balanced integration of social and environmental cues. When such flexible information integration fails, maladaptive behavioral patterns arise, including excessive aggression, empathy deficits, and social withdrawal, as seen in disorders such as conduct disorder and autism spectrum disorder. One of the main hubs for the context-dependent regulation of behavior is cingulate cortex, specifically anterior cingulate cortex (ACC) and midcingulate cortex (MCC). While volumetric abnormalities of ACC and MCC have been demonstrated in patients, little is known about the exact structural changes responsible for the dysregulation of behaviors such as aggression and social withdrawal. Here, we demonstrate that the distribution of parvalbumin (PV) and somatostatin (SOM) interneurons across ACC and MCC differentially predicts aggression and social withdrawal in BALB/cJ mice. BALB/cJ mice were phenotyped for their social behavior (three-chamber task) and aggression (resident-intruder task) compared to control (BALB/cByJ) mice. In line with previous studies, BALB/cJ mice behaved more aggressively than controls. The three-chamber task revealed two sub-groups of highly-sociable versus less-sociable BALB/cJ mice. Highly-sociable BALB/cJ mice were as aggressive as the less-sociable group-in fact, they committed more acts of socially acceptable aggression (threats and harmless bites). PV and SOM immunostaining revealed that a lack of specificity in the distribution of SOM and PV interneurons across cingulate cortex coincided with social withdrawal: both control mice and highly-sociable BALB/cJ mice showed a differential distribution of PV and SOM interneurons across the sub-areas of cingulate cortex, while for less-sociable BALB/cJ mice, the distributions were near-flat. In contrast, both highly-sociable and less-sociable BALB/cJ mice had a decreased concentration of PV interneurons in MCC compared to controls, which was therefore linked to aggressive behavior. Together, these results suggest that the dynamic balance of excitatory and inhibitory activity across ACC and MCC shapes both social and aggressive behavior.

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Oxytocin receptor disruption in Avil-expressing cells results in blunted sociability and increased inter-male aggression.

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