Selective processing of social stimuli in the superficial amygdala

Abstract

The human amygdala plays a pivotal role in the processing of socially significant information. Anatomical studies show that the human amygdala is not a single homogeneous structure but is composed of segregable subregions. These have recently been functionally delineated by using a combination of functional magnetic resonance imaging (fMRI) and cytoarchitectonically defined probabilistic maps. However, the response characteristics and individual contribution of these subregions to the processing of social-emotional stimuli are little understood. Here, we used this novel technique to segregate intra-amygdalar responses to facial expressions and nonsocial control stimuli. We localized facial expression-evoked signal changes bilaterally in the superficial amygdala, which suggests that this subregion selectively extracts the social value of incoming sensory information.

Effects of emotion regulation strategy on brain responses to the valence and social content of visual scenes

“…This pattern is consistent with data from several previous experiments describing preferential amygdala activation to SOC stimuli including faces, pictures, or film-clips (e.g., Britton et al, 2006;Goossens et al, 2009;Hariri et al, 2002;Norris et al, 2004). These results also accord with recent proposals that the amygdala might be particularly tuned to the intrinsic salience or biological importance of SOC stimuli (Sander, Grafman, & Zalla, 2003), rather than to threat or other specific emotion categories.…”

“…All findings for significant effects are summarized in Table 4. As expected, social scenes produced greater activation in widespread brain networks including extrastriate visual cortex, temporal lobe, and ventromedial prefrontal areas, all previously associated with face and body perception, person recognition, mentalizing, and/or social cognition (Britton et al, 2006;Goossens et al, 2009;Norris et al, 2004;. Conversely, nonsocial scenes produced greater activation in visual regions associated with object and place recognition, as well as insula, anterior cingulate, and more lateral areas in prefrontal cortex (see Table 1 and Fig.…”

“…Although exposure times of 2 s or even less are standard in fMRI research involving emotional stimuli and effective to activate relevant brain structures (e.g., Britton et al, 2006;Goossens et al, 2009;Hariri et al, 2002;Norris et al, 2004), may paradigms in the field of emotion regulation have employed longer picture viewing times (e.g., Beauregard et al, 2001;Kim & Hamann, 2007;Koenigsberg et al, 2010;Levesque et al, 2003;Mak et al, 2009;Ochsner et al, 2002;Ochsner, Ray et al, 2004). However, in contrast to these investigations where regulation strategies alternate on a trial-by-trial basis and hence require the search for imagespecific adjustments (e.g., re-interpretations during REAP), here we applied a blocked design where regulation could be implemented in a more sustained manner (as already used elsewhere, e.g., Harenski & Hamann, 2006;Phan et al, 2005) and was guided by controlled instructions (e.g., "pretend unreal" for the REAP strategy) for all stimulus conditions and all participants.…”

“…Yet, this study did not compare brain activations elicited by social negative to comparable nonsocial negative scenes. This lack of systematic investigation of ER as a function of the content of emotion-eliciting stimuli is regrettable given many other findings which point to major differences in emotional reactions (and their corresponding neural signatures) depending on the social versus nonsocial nature of information (Britton et al, 2006;Frewen et al, 2010;Goossens et al, 2009;Hariri, Tessitore, Mattay, Fera, & Weinberger, 2002;Norris, Chen, Zhu, Small, & Cacioppo, 2004;Sander, Koenig, Georgieff, Terra, & Franck, 2005;Scharpf, Wendt, Lotze, & Hamm, 2010). In addition, there is evidence that the activation of some limbic brain areas (e.g., the amygdala) is more sensitive to social and thus interpersonal aspects rather than to nonsocial dimensions of emotion-eliciting situations (Killgore & YurgelunTodd, 2005;Vrtička, Andersson, Grandjean, Sander, & Vuilleumier, 2008).…”

“…We predicted changes in activations related to the differential encoding of valence (negative vs. positive) and/or stimulus content (social vs. nonsocial) in brain networks that are selectively tuned to social and affective information (Lieberman, 2007), including in particular the amygdala which has previously been shown to be sensitive to social cues (Britton et al, 2006;Frewen et al, 2010;Goossens et al, 2009;Hariri et al, 2002;Norris et al, 2004;Sander et al, 2005;Scharpf et al, 2010;Vrtička et al, 2008) and modulated by different ER strategies (Killgore & Yurgelun-Todd, 2005;Kim & Hamann, 2007;Koenigsberg et al, 2010;Levesque et al, 2003;Ochsner et al, 2002;Ochsner, Ray et al, 2004). Other differences were expected in prefrontal cortical areas that have been implicated in controlling emotion processing during different ER strategies (Goldin et al, 2008;Kim & Hamann, 2007;Levesque et al, 2003;Ochsner et al, 2002;Ochsner, Ray et al, 2004).…”