Chronic intranasal oxytocin increases acoustic eavesdropping and adult neurogenesis

• Published in: Hormones and behavior 2023-11, Vol.156, p.105443, Article 105443
• Main Authors: Monari, Patrick K., Herro, Zachary J., Bymers, Jessica, Marler, Catherine A.
• Format: Article
• Language: English
• Subjects: Acoustic eavesdropping; Administration, Intranasal; Adult neurogenesis; Aggression; Animals; Anxiety; Chronic intranasal oxytocin; Dentate gyrus; Female; hippocampus; Hippocampus - metabolism; Male; Mice; Neurogenesis; Oxytocin; Oxytocin - pharmacology; Peromyscus californicus; Receptors, Oxytocin - metabolism; Social approach; Social decision-making
• ISSN: 0018-506X; 1095-6867; 1095-6867
• DOI: 10.1016/j.yhbeh.2023.105443

Social information gathering is a complex process influenced by neuroendocrine-modulated neural plasticity. Oxytocin (OXT) is a key regulator of social decision-making processes such as information gathering, as it contextually modulates social salience and can induce long-term structural plasticity, including neurogenesis. Understanding the link between OXT-induced plasticity and communicative awareness is crucial, particularly because OXT is being considered for treatment of social pathologies. We investigated the role of chronic OXT-dependent plasticity in attention to novel social information by manipulating the duration of time following cessation of intranasal treatment to allow for the functional integration of adult-born neurons resulting from OXT treatment. Following a 3-week delay, chronic intranasal OXT (IN-OXT) increased approach behavior of both female and male mice towards aggressive vocal playbacks of two unseen novel conspecifics, while no effect was observed after a 3-day delay. Immature neurons increased in the ventral hippocampus of females and males treated with chronic IN-OXT after the 3-week delay, indicating a potential association between ventral hippocampal neurogenesis and approach/acoustic eavesdropping. The less the mouse approached, the higher the level of neurogenesis. Contrary to expectations, the correlation between ventral hippocampal neurogenesis and approach behavior was not affected by IN-OXT, suggesting that other plasticity mechanisms underlie the long-term effects of chronic OXT on social approach. Furthermore, we found a negative correlation between ventral hippocampal neurogenesis and freezing behavior. Overall, our results demonstrate that chronic IN-OXT-induced long-term plasticity can influence approach to vocal information and we further reinforced the link between neurogenesis and anxiety. [Display omitted] •Chronic IN-OXT increased approach/acoustic eavesdropping following a 3-week delay.•Chronic IN-OXT increased ventral neurogenesis following a 3-week delay.•Ventral neurogenesis negatively correlated with both social approach and freezing.•Multiple plasticity mechanisms likely mediate social information gathering.