In confirmation of our first hypothesis, amygdala BOLD responses to anger faces in both tasks were negatively correlated with endogenous testosterone levels in men. We also found that vmPFC BOLD responses to anger faces in the passive viewing task were positively correlated with endogenous testosterone levels in men, which confirmed our second hypothesis. In confirmation of our third hypothesis, testosterone levels were not associated with amygdala or vmPFC BOLD responses to anger faces in women. Lastly, our fourth hypothesis that testosterone levels would not be associated with Wernicke’s area BOLD responses to anger faces in men or women in either task was also confirmed.
Our results complement findings in males of mammalian species that have revealed functional links between testosterone and the amygdala and vmPFC in mediating dominance and aggressive behavior (Ambar & Chiavegatto, in press
; Delville et al., 1996
; Ferris & Delville, 1994
). Several researchers have argued strongly that anger faces represent interpersonal dominance signals (Hess et al., 2000
; Knutson, 1996
; Oosterhof & Todorov, 2008
). Our results provide evidence in humans of neural substrates where testosterone may drive differential activation patterns in the brain in response to dominance signals and challenges. We speculate that the negative correlation between testosterone and men’s amygdala response to anger suggests that high-testosterone men are less threatened by dominance challenges, and hence stimuli that are indicative of such challenges are perhaps less salient or aversive to them than to low-testosterone men. There is converging behavioral evidence showing that high-testosterone individuals show less behavioral aversion to angry faces in an instrumental learning task (Wirth & Schultheiss, 2007
). This is also supported by the observation that testosterone reduces individuals’ ability to recognize anger in facial expressions of emotion (van Honk & Schutter, 2007
). This lack of perceived threat may make high-testosterone men more likely to engage in testosterone-facilitated dominance behavior and approach dominance challenges.
We chose two tasks (passive-viewing and oddball) to test our hypotheses due to conflicting literature regarding whether the brain responds more to facial expressions of emotion when participants are focused on the emotion or when they are performing a “distraction” task (Critchley et al., 2000
, Lieberman, 2003
; Lieberman et al., 2007
; Quirk, et al., 2003
; Taylor, et al. 2003
). The consistency of our findings showing a bilateral, negative correlation between amygdala BOLD response and testosterone levels in both tasks strengthens the conclusions that we drew from the data, because the effect is similar regardless of the presumed level of attention paid to the stimuli2
The presently reported negative correlation between testosterone-related amygdala BOLD response and testosterone-related vmPFC BOLD response in the passive viewing task corroborates past research showing that amygdala responses and vmPFC responses to affective stimuli tend to be negatively correlated (cf. Blair, 2008
), specifically in the context of perceiving anger faces (Nomura et al., 2004
). Moreover, past research has shown that participants’ conscious attention to emotional components of stimuli leads to PFC activation that subsequently attenuates amygdala activation (Hariri et al., 2003
; Lieberman et al., 2007
). In the passive viewing task, subjects were not distracted by engaging in a simultaneous task and could pay greater attention to the emotional components of the anger faces. We speculate that the negative correlation between amygdala and vmPFC BOLD responses could possibly reflect high-testosterone participants paying greater attention to the anger stimulus, since they find anger faces to be less aversive (Wirth & Schultheiss, 2007
), and this yielded a strong vmPFC BOLD response and corresponding attenuation of the amygdala BOLD response for high-testosterone men.
Our failure to find a relationship between amygdala or vmPFC BOLD response to anger faces and testosterone levels in women corroborates behavioral research that has failed to document a consistent relationship between testosterone and dominance in women (Mazur & Booth, 1998
; Stanton & Schultheiss, 2007
). Estradiol, which has been implicated in dominance motivation and responses to dominance contests in female primates and recently in women, also acts on the amygdala and could be examined in future research on women’s neural responses to dominance signals (Cottingham & Pfaff, 1986
; Michael & Zumpe, 1993
; Stanton & Schultheiss, 2007
Although the present research has established a highly significant negative correlation between men’s endogenous testosterone levels and amygdala BOLD response to dominance signals and a highly significant positive correlation between men’s endogenous testosterone levels and vmPFC BOLD response to dominance signals, our study is not without its limitations. We cannot draw causal inferences regarding the effects of testosterone on amygdala and vmPFC BOLD response. Future research could also explore the relationships between testosterone and amygdala and vmPFC BOLD responses for several classes of emotional expressions as well as using trait measures of dominance as predictors of BOLD response to emotions. Additionally, our sample size is relatively small and replication studies are therefore particularly important. Despite these limitations, we think that our current findings are robust and provide a foundation for further research on endogenous testosterone levels’ associations with brain responses to emotional and dominance-related stimuli.