Abstract

In the past, the amygdala has generally been conceptualized as a fear-processing module. Recently, however, it has been proposed to respond to all stimuli that are relevant with respect to the current needs, goals, and values of an individual. This raises the question of whether the human amygdala may differentiate between separate kinds of relevance. A distinction between emotional (vs. neutral) and social (vs. non-social) relevance is supported by previous studies showing that the human amygdala preferentially responds to both emotionally and socially significant information, and these factors might even display interactive encoding properties. However, no investigation has yet probed a full 2 (positive vs. negative valence) × 2 (social vs. non-social content) processing pattern, with neutral images as an additional baseline. Applying such an extended orthogonal factorial design, our fMRI study demonstrates that the human amygdala is (1) more strongly activated for neutral social vs. non-social information, (2) activated at a similar level when viewing social positive or negative images, but (3) displays a valence effect (negative vs. positive) for non-social images. In addition, this encoding pattern is not influenced by cognitive or behavioral emotion regulation mechanisms, and displays a hemispheric lateralization with more pronounced effects on the right side. Finally, the same valence × social content interaction was found in three additional cortical regions, namely the right fusiform gyrus, right anterior superior temporal gyrus, and medial orbitofrontal cortex. Overall, these findings suggest that valence and social content processing represent distinct kinds of relevance that interact within the human amygdala as well as in a more extensive cortical network, likely subserving a key role in relevance detection.

Highlights

  • Thanks to the advancement of neuroimaging techniques and paradigms, our knowledge on human amygdala function has steadily increased during the last two decades

  • The same valence × social content interaction was found in three additional cortical regions, namely the right fusiform gyrus, right anterior superior temporal gyrus, and medial orbitofrontal cortex. These findings suggest that valence and social content processing represent distinct kinds of relevance that interact within the human amygdala as well as in a more extensive cortical network, likely subserving a key role in relevance detection

  • Women were included in order to avoid any potential sex differences that could have modulated the effects of interest. functional magnetic resonance imaging (fMRI) data from the same study were previously reported in Vrticka et al (2011) and Vrticka et al (2012a), but the latter focused on whole-brain results comparing specific emotion regulation strategies and distinct attachment styles

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Summary

Introduction

Thanks to the advancement of neuroimaging techniques and paradigms, our knowledge on human amygdala function has steadily increased during the last two decades. The amygdala would either represent a general arousal indicator or valence processor Besides these traditional accounts respectively derived from basic (Ekman, 1999) or bi-dimensional (Russell, 1980) theories of emotion, recent experimental evidence revealed amygdala activation to be determined by many additional factors (not confounded by arousal), such as eye gaze (N’Diaye et al, 2009; Sato et al, 2010), novelty (Blackford et al, 2010; Weierich et al, 2010; Balderston et al, 2011), social content (Norris et al, 2004; Britton et al., 2006; Goossens et al, 2009; Scharpf et al, 2010), context (Kim et al, 2003, 2004; Vrticka et al, 2008), personal impact (Ewbank et al, 2009), or individual differences in subjective evaluation (Schiller et al, 2009), motivational state (Canli et al, 2001; LaBar et al, 2001; Morris and Dolan, 2001) as well as various psychological traits (Canli et al, 2001; Bishop et al, 2004; Etkin et al, 2004; Sabatinelli et al, 2005; Dickie and Armony, 2008; Vrticka et al, 2008, 2012a; Vrticka and Vuilleumier, 2012). This concept of relevance detection has its origins in emotion psychology (Sander et al, 2003), in particular in appraisal theories of emotion (Sander et al, 2005), and refers to the preferential processing of events that are (biologically) relevant to major concerns/goals/needs and values of an individual at a specific moment in time (see Frijda, 2009; Reisenzein, 2009)

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