Look at Me! The socio-neuro-endocrinology of eye-contact, dominance and status

Abstract

The terms approach and avoidance are used to describe appetitive motivation and fear of punishment. In a social context fear is indeed linked to avoidance, but approach motivation is also expressed with anger and aggression as means to achieve goals at the expense, or through social correction, of others. Therefore, in the social competition of most mammalian species approach-avoidance is strongly linked to dominance-submissiveness, whereby the motivation to dominate others reflects appetitive motivation as well as socially aggressive tendencies. The steroid testosterone is a social hormone that is heavily involved in approach-avoidance and dominance-submissiveness, and is in many species associated with reduced fear and increased reactive social aggression. Recent evidence indicates, however, that testosterone can also promote fairness in humans. In this thesis we first describe a neural framework rooted in animal research and based on a study in five human subjects with selective brain damage in the basolateral amygdala, in which we show that this structure is heavily involved in the inhibition of fear-vigilance. Next, we use several newly developed interactive eye-tracking paradigms to show that anger is indeed related to reward sensitivity, and anxiety to threat avoidance. Furthermore, when confronted with angry facial expressions, submissiveness predicts rapid gaze aversion from eye-contact, and dominance motives as well as testosterone administration lead to reflexive preservation of eye-contact. In sum, dominance-submissiveness seems to involve reflexive mechanisms, and testosterone induces reactive dominance behavior. In the next part of this thesis we show that testosterone also influences cognitive behavior and decision-making in the absence of a direct status-threat. Earlier research already showed that testosterone can reduce cognitive empathy, and here we show that testosterone adaptively reduces trust, but can also increase social cooperative behavior. Translating evidence from rodent and primate research, we argue therefore that reactive-reflexive dominance, and deliberate social cooperation are both approach behaviors by which testosterone promotes survival and reproduction through an increase of social status. First, testosterone inhibits basal fear responsivity at the level of the basolateral amygdala and hypothalamus providing for a general fearlessness that facilitates approach oriented behavior. Second, when social status is directly challenged testosterone promotes reactive aggression and reflexive dominance by upregulating vasopressin gene-expression in the central-medial amygdala. Third, testosterone reduces cortical control over the amygdala, resulting in the general social vigilance that underlies conscious decision making that is beneficial to social status. In sum, testosterone boosts unconscious-reflexive dominance, but can also increase cooperative behaviors depending on the social context. However, both on the level of this reflexive behavior and in conscious decision making, testosterone promotes approach oriented behavior that helps to defend and increase social status