Neural activation in the “reward circuit” shows a nonlinear response to facial attractiveness

Abstract

Positive behavioral responses to attractive faces have led neuroscientists to investigate underlying neural mechanisms in a “reward circuit” that includes brain regions innervated by dopamine pathways. Using male faces ranging from attractive to extremely unattractive, disfigured ones, this study is the first to demonstrate heightened responses to both rewarding and aversive faces in numerous areas of this putative reward circuit. Parametric analyses employing orthogonal linear and nonlinear regressors revealed positive nonlinear effects in anterior cingulate cortex, lateral orbital frontal cortex (LOFC), striatum (nucleus accumbens, caudate, putamen), and ventral tegmental area, in addition to replicating previously documented linear effects in medial orbital frontal cortex (MOFC) and LOFC and nonlinear effects in amygdala and MOFC. The widespread nonlinear responses are consistent with single cell recordings in animals showing responses to both rewarding and aversive stimuli, and with some human fMRI investigations of non-face stimuli. They indicate that the reward circuit does not process face valence with any simple dissociation of function across structures. Perceiver gender modulated some responses to our male faces: Women showed stronger linear effects, and men showed stronger nonlinear effects, which may have functional implications. Our discovery of nonlinear responses to attractiveness throughout the reward circuit echoes the history of amygdala research: Early work indicated a linear response to threatening stimuli, including faces; later work also revealed a nonlinear response with heightened activation to affectively salient stimuli regardless of valence. The challenge remains to determine how such dual coding influences feelings, such as pleasure and pain, and guides goal-related behavioral responses, such as approach and avoidance.

Keywords:

• Facial attractiveness
• FMRI
• Reward circuit

This work was supported by the National Institutes of Mental Health Grants (grant numbers MH066836 and K02MH072603) and National Science Foundation Grant (grant number 0315307) to LAZ.

Notes

¹The other face categories were included to examine the neural substrate for babyface overgeneralization in behavioral responses to faces that vary in their resemblance to babies (Zebrowitz, Luevano, Bronstad, & Aharon, 2009), and to examine the neural substrate for the categorical and dimensional differentiation of emotion expressions (Liang, Zebrowitz, & Aharon, 2009).

²Randomizing the order of face categories across runs resulted in the blocks of attractive and average faces and attractive and disfigured faces preceding and following each other an equal number of times (three runs each). The block of unattractive faces preceded disfigured faces in four runs and followed in two runs.

³In whole-brain level analysis, using minimum cluster-size threshold determined by Alphasim with voxel level threshold of p < 0.05, we also found gender modulation of positive nonlinear effects of attractiveness in the following regions (both left and right) for which we had no a prior predictions: lingual gyrus, precentral gyrus, precuneus, and superior temporal gyrus.