Endogenous Testosterone Modulates Prefrontal-Amygdala Connectivity during Social Emotional Behavior

Abstract

It is clear that the steroid hormone testosterone plays an important role in the regulation of social emotional behavior, but it remains unknown which neural circuits mediate these hormonal influences in humans. We investigated the modulatory effects of endogenous testosterone on the control of social emotional behavior by applying functional magnetic resonance imaging while healthy male participants performed a social approach–avoidance task. This task operationalized social emotional behavior by having participants approach and avoid emotional faces by pulling and pushing a joystick, respectively. Affect-congruent trials mapped the automatic tendency to approach happy faces and avoid angry faces. Affect-incongruent trials required participants to override those automatic action tendencies and select the opposite response (approach-angry, avoid-happy). The social emotional control required by affect-incongruent responses resulted in longer reaction times (RTs) and increased activity at the border of the ventrolateral prefrontal cortex and frontal pole (VLPFC/FP). We show that endogenous testosterone modulates these cerebral congruency effects through 2 mechanisms. First, participants with lower testosterone levels generate larger VLPFC/FP responses during affect-incongruent trials. Second, during the same trials, endogenous testosterone modulates the effective connectivity between the VLPFC/FP and the amygdala. These results indicate that endogenous testosterone influences local prefrontal activity and interregional connectivity supporting the control of social emotional behavior.

Neural Correlates of Alcohol-Approach Bias in Alcohol Addiction: the Spirit is Willing but the Flesh is Weak for Spirits

“…More activity in the dlPFC was expected in patients compared with controls, as previous studies found that the dlPFC is generally more active when stimulus and response are incongruent (Roelofs et al, 2009;Volman et al, 2011). In contrast, it may be that patients lack control to avoid alcohol and hence show reduced dlPFC activity in the avoid-alcohol contrast.…”

“…The dlPFC has been shown to be structurally and functionally impaired in drug addiction, and may be related to suboptimal cognitive control (Baler and Volkow, 2006;Bechara, 2005;Hayashi et al, 2013;Jentsch and Taylor, 1999;Park et al, 2010). Previous approach/avoidance studies on emotional processing showed that dlPFC is more active when stimulus and response are incongruent (approach sad faces) than congruent (approach happy faces; Roelofs et al, 2009;Volman et al, 2011). If patients indeed have an alcoholapproach bias (congruent), the dlPFC would be expected to be active while avoiding alcohol cues (incongruent).…”

Social deficits induced by peripubertal stress in rats are reversed by resveratrol

“…This receptor is typically translocated from the cytoplasm to the nucleus when bound by androgen ligands, testosterone or its metabolite, 5a-dihydrotestosterone. Androgens enotably testosterone-are known to play a key role in social behaviors, both in animals (Bluth e et al, 1993(Bluth e et al, , 1990) and humans (Dabbs et al, 2001), as well as with prefrontal cortex metabolism in a social context (Stanton et al, 2009;Volman et al, 2011). We thus investigated potential changes in the subcellular localization of the androgen receptor, finding an increase in the nuclear localization of the androgen receptor in the prelimbic cortex following resveratrol treatment.…”

Post-traumatic stress disorder: review of DSM criteria and functional neuroanatomy

“…4 Neurons within the prefrontal cortex (PFC) regulate conscious awareness and volitional control over emotions, attention, memory and behaviors. 5,6,7 Functional activity within the PFC can be localized to specific regions as follows: medial PFC regulates emotions and memory, orbital (ventral) PFC regulates behaviors, and lateral PFC regulates attention. 8 During the initial response to an environmental threat, neurons within the amygdala trigger defensive behaviors and physiological arousal (fear response).…”