The Changing Role of Testosterone in the Maturation of Social-Emotional Behavior

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The gonadal hormone testosterone is known to play a crucial role in the regulation of social and emotional behavior by influencing approach and avoidance actions.

However, the function of testosterone undergoes significant changes during puberty, leading to seemingly opposing effects between adolescents and adults. While higher levels of pubertal testosterone have been associated with increased anterior prefrontal (aPFC) emotion control in mid-adolescence, in adult populations, higher testosterone levels have been linked to reduced aPFC emotion control.

This paradoxical effect of testosterone is particularly relevant for understanding the development of social approach-avoidance behavior.

Understanding the maturation of the human prefrontal cortex and its regulation of social-emotional behavior, as well as the changing role of testosterone in this process, is of utmost importance. This article aims to explore the existing research and provide insights into the complex relationship between testosterone, brain development, and social-emotional behavior.

Testosterone and Social-Emotional Behavior in Adolescence

Numerous studies have demonstrated that pubertal testosterone influences executive control and reward processing networks in humans. It has been linked to the maturation of cognitive control over social-emotional actions, a skill that undergoes refinement during puberty.

In mid-adolescence, individuals with higher levels of testosterone tend to exhibit more mature emotion control, relying on the aPFC. In contrast, less mature individuals at the same age rely on pulvino-amygdala interactions to regulate their emotional action tendencies. This reliance on pulvino-amygdala interactions is considered a precursor to the aPFC-amygdala circuit typically observed in adults.

However, the effects of testosterone in adults differ significantly. In adult populations, testosterone transiently activates dominance and status-seeking behaviors, promoting social behavior. Adults with high testosterone levels rely less on the aPFC and exhibit reduced aPFC-amygdala coupling during emotion action control.

Insights from Animal Studies

Animal studies provide further insights into the shifts in testosterone’s role during adolescence. In rodents, testosterone transitions from a developmental agent of neural organization to a hormone that transiently activates socio-sexual behavioral and neural responses during adolescence.

Pubertal testosterone is crucial for inducing long-lasting changes in social behavior programming. Animal experiments have shown that castrated animals can display typical socio-sexual and territorial behavior as adults only if they receive testosterone-replacement treatment in the pre- and mid-adolescent phase, but not later in the post-adolescent phase.

Similar effects have been observed in the maturation of social learning and adaptive sexual approach behavior. These findings suggest that gonadal hormones, such as testosterone, play a significant role in the context-dependent social approach-avoidance motivation during adolescence.

The Longitudinal Study and Approach-Avoidance Task

To explore the changes in testosterone’s function during human adolescence, a longitudinal study was conducted to investigate emotion action control using an approach-avoidance (AA) task. The AA task assesses behavioral and neural components of emotion action control in both adolescents and adults.

During this task, participants evaluate the emotional expressions of faces and respond by pulling a joystick toward themselves (approach) or pushing it away (avoidance). The task involves automatic ‘affect-congruent’ stimulus-response mappings, as well as ‘affect-incongruent’ conditions that require overriding emotion tendencies and selecting alternative goal-directed actions.

The Role of aPFC, Amygdala, and Pulvinar

Previous research has established the importance of the aPFC, amygdala, and pulvinar in social emotional control. The aPFC is crucial for emotion control and down-regulating amygdala reactivity. In this study, the researchers focused on examining the change in congruency effect over time, which refers to the difference between affect-incongruent and affect-congruent trials, in association with testosterone levels at different ages.

Hypotheses and Future Directions

Based on the organizational-activation hypothesis of gonadal hormones in rodents, the researchers hypothesized that the modulating effect of testosterone on aPFC emotion control would decrease between middle and late adolescence and eventually switch to negative modulation by young adulthood. By investigating the association between testosterone levels and the congruency effect in the aPFC, amygdala, and pulvinar, this study aims to shed light on the maturation process of social-emotional behavior and its relationship with testosterone during adolescence and young adulthood.

Understanding the changing role of testosterone during adolescence is crucial for comprehending both adaptive and maladaptive developmental processes. Insights gained from this research could potentially contribute to the understanding and treatment of psychopathology, including anxiety and aggression-related disorders.

Conclusion

The role of testosterone in the regulation of social-emotional behavior undergoes significant changes during puberty and into adulthood. While higher levels of pubertal testosterone are associated with increased aPFC emotion control in mid-adolescence, the effects in adults are quite different, with higher testosterone levels linked to reduced aPFC emotion control. Animal studies provide additional evidence for the role of testosterone in social behavior programming during adolescence.

The longitudinal study discussed in this article aims to investigate the changing role of testosterone in emotion action control using an approach-avoidance task. By examining the engagement of the aPFC, amygdala, and pulvinar in relation to testosterone levels at different ages, researchers hope to gain a deeper understanding of the maturation of social-emotional behavior and its relationship with testosterone.

This research has the potential to contribute to our understanding of adaptive development, as well as maladaptive processes that may lead to various psychopathological conditions. By unraveling the intricate interplay between hormones, brain development, and behavior, future studies may pave the way for more targeted interventions and treatments for individuals experiencing difficulties in social-emotional regulation.


reference link : https://onlinelibrary.wiley.com/doi/10.1111/desc.13415

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