Learning affective values for faces is expressed in amygdala and fusiform gyrus

Abstract

To monitor the environment for social threat humans must build affective evaluations of others. These evaluations are malleable and to a high degree shaped by responses engendered by specific social encounters. The precise neuronal mechanism by which these evaluations are constructed is poorly understood. We tested a hypothesis that conjoint activity in amygdala and fusiform gyrus would correlate with acquisition of social stimulus value. We tested this using a reinforcement learning algorithm, Q-learning, that assigned values to faces as a function of a history of pairing, or not pairing, with aversive shocks. Behaviourally, we observed a correlation between conditioning induced changes in skin conductance response (SCR) and subjective ratings for likeability of faces. Activity in both amygdala and fusiform gyrus (FG) correlated with the output of the reinforcement learning algorithm parameterized by these ratings. In amygdala, this effect was greater for averted than direct gaze faces. Furthermore, learning-related activity change in these regions correlated with SCR and subjective ratings. We conclude that amygdala and fusiform encode affective value in a manner that closely approximates a standard computational solution to learning.

Very early modulation of brain responses to neutral faces by a single prior association with an emotional context: Evidence from MEG

“…with the social and emotional nature of our stimuli. Indeed, several fMRI studies have observed effects related to emotional memory mechanisms in early visual areas (Damaraju et al, 2009;Fenker et al, 2005;Padmala and Pessoa, 2008;Petrovic et al, 2008). Furthermore, the amygdala is at the core of a network that processes emotional stimuli of both negative and positive valence (Sergerie et al, 2008; see also Morrison and Salzman, 2010;Paton et al, 2006) and it also plays a central role in emotional memory (Buchanan, 2007;Dolan, 2007;Phelps and LeDoux, 2005).…”

“…Recent neuroimaging studies have indeed shown that the emotional context associated with a neutral stimulus can influence the neural memory trace of that stimulus (Damaraju et al, 2009;Erk et al, 2005;Fenker et al, 2005;Galli et al, 2006;Keil et al, 2007;Padmala and Pessoa, 2008;Petrovic et al, 2008;Smith et al, 2005;Sterpenich et al, 2006;Stolarova et al, 2006;Todorov et al, 2007;Tsukiura and Cabeza, 2008). This influence has been observed throughout the visual processing stream, including striate and extrastriate regions (Damaraju et al, 2009;Fenker et al, 2005;Padmala and Pessoa, 2008;Petrovic et al, 2008) in line with the view that memory and perceptual processing are underpinned by the same mechanisms and involve shared neuronal systems (Brunel et al, 2009;Slotnick and Schacter, 2006; for a review see Graham et al, 2010). It is however unknown whether this reflects modulations of the earliest stages of visual processing: may an emotional influence be observed from the very first stages of visual processing?…”

Neural correlates of individual differences in fear learning

“…In the largest study yet published on the neural basis of individual differences in fear conditionability ( n = 27), Petrovic and colleagues [21] sought to investigate neural mechanisms underlying affective evaluations of social stimuli. To this end, participants viewed pictures of 4 different faces over the course of an experiment.…”

“…Two of the faces (CS+) were paired with mild electric shock (US) on 50% of trials; the other two faces (CS−) were never paired with shock. While they failed to observe an overall increase in SCR for the CS+ versus the CS−, Petrovic and colleagues [21] observed greater conditioning related increases in SCR from the second half of the experiment compared to the first half of the experiment that were positively correlated with BOLD activation in the bilateral amygdala, using a region of interest (ROI) approach focused on the amygdala and the fusiform gyrus, a region involved in face processing.…”

“…For example, it is unclear whether Schiller and Delgado [22] failed to observe a correlation between the amygdala and SCR because of a lack of power, and whether Petovic and colleagues [21] might have observed correlations between SCR and BOLD activation in other brain regions (e.g., the insula, ventral striatum) had they not limited their analysis to the amygdala and the fusiform gyrus. Further, both studies used faces as the CS stimuli, which might vary in their perceived affective salience across individuals [e.g., 26] and might therefore confound effects of social stimuli processing and fear conditioning.…”