Studies of Pavlovian conditioning in both nonhuman animals (LeDoux 1996
; Davis and Whalen 2001
) and humans (Buchel et al. 1998
; LaBar et al. 1998
; Morris et al. 2001
; Gottfried et al. 2002
; Phelps et al. 2004
) suggest that the amygdala plays an important role in learning the predictive value of biologically relevant stimuli. Facial expressions of emotion have also been shown to elicit increases in amygdala activity, presumably because they are salient, biologically relevant stimuli that have predicted important events in our environment (Whalen 1998
). Indeed, the amygdala is more responsive to facial expressions embedded within an associative learning context than when presented in isolation (Hooker et al. 2006
). Moreover, patients with bilateral amygdala damage judge strangers as being more approachable and trustworthy than controls (Adolphs et al. 1998) suggesting that the amygdala plays an important role in representing the social reinforcement value of other individuals (Adolphs 2001). Given that we form preferences for other people based on our previous experiences with them, the goal of the present study was to characterize the human amygdala's role in social conditioning, defined here as the associative process whereby we learn to identify individuals that have predicted threats or rewards in the past.
Work in nonhuman animals suggests that subnuclei within the amygdaloid complex differentially contribute to associative learning (see Discussion), and functional magnetic resonance imaging (fMRI) research has begun to use functional response profiles to spatially dissociate regions of the human amygdaloid complex. For example, Morris et al. (2001)
showed that although responses within a ventral region of the amygdala did not habituate across trials during a traditional Pavlovian conditioning study, responses in a dorsal region did. These findings could be consistent with animal data showing that although some cells in the amygdala show early and transient increases in activity during learning, other cells maintain sustained representations of conditioned stimuli (Repa et al. 2001
; Radwanska et al. 2002
). In a separate line of inquiry, Whalen and colleagues reported that a lateral ventral portion of the human amygdala showed the greatest responses to facial expressions communicating negative valence, whereas responses in a medial ventral and a dorsal amygdala region were equally responsive to facial expressions communicating both positive and negative valence (Kim et al. 2003
). These data were interpreted to suggest that different portions of the human amygdaloid complex show greater specialization for processing valence versus arousal, respectively.
Taken together, these studies predict that it should be possible to dissociate regional differences in responses across the human amygdaloid complex during learning at routinely utilized fMRI spatial resolutions. In this experiment, we monitored these regional differences in amygdala response during a social conditioning paradigm. We chose this modification of more traditional Pavlovian conditioning paradigms for several reasons. Our primary aim was to relate an extensive literature on the amygdala's role in associative learning tasks (i.e., Pavolovian conditioning) to a growing literature that implicates the amygdala in human social and emotional learning (Ohman and Mineka 2001
; Hooker et al. 2006
; Olsson et al. 2007
; Olsson and Phelps 2007
; Schiller et al. 2009
). In humans, the ability to identify individual faces based on the social outcomes they have predicted in the past constitutes a critical form of association that, at a very basic level, mirrors other learning processes such as associating certain cues with biologically relevant outcomes. Moreover, the social reinforcers employed in the current paradigm allow us to manipulate valence while controlling for arousal. This is more difficult to do in traditional Pavlovian learning studies because primary reinforcers (such as the presence or absence of shock) elicit different levels of emotional arousal, making it difficult to dissociate amygdala response to valence vs. arousal.