Amygdalostriatal coupling underpins positive but not negative coloring of ambiguous affect
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Amygdalostriatal coupling underpins positive but not negative coloring of ambiguous affect M. Justin Kim 1
&
Alison M. Mattek 2 & Jin Shin 3
# The Psychonomic Society, Inc. 2020
Abstract Humans routinely integrate affective information from multiple sources. For example, we rarely interpret an emotional facial expression devoid of context. In this paper, we describe the neural correlates of an affective computation that involves integrating multiple sources, by leveraging the ambiguity and subtle feature-based valence signals found in surprised faces. Using functional magnetic resonance imaging, participants reported the valence of surprised faces modulated by positive or negative sentences. Amygdala activity corresponded to the valence value assigned to each contextually modulated face, with greater activity reflecting more negative ratings. Amygdala activity did not track the valence of the faces or sentences per se. Moreover, the amygdala was functionally coupled with the nucleus accumbens only during face trials preceded by positive contextual cues. These data suggest 1) valence-related amygdala activity reflects the integrated valence values rather than the valence values of each individual component, and 2) amygdalostriatal coupling underpins positive but not negative coloring of ambiguous affect. Keywords Emotion . Valence . Ambiguity . Context . Feature . Amygdala
Introduction Affective valence—the degree of positivity-negativity or pleasantness-unpleasantness—is one of the core dimensions that underpins any emotional stimulus, event, or experience (Russell, 1980; Cacioppo et al., 1986; Lang, Bradley, & Cuthbert, 1998). Neural encoding of valence is traditionally known to occur in several brain regions centered on the limbic system and its interconnected network of cortical areas, which includes the amygdala-prefrontal circuitry. For example, single-cell recording studies of nonhuman primates showed that neurons in the amygdala (Belova, Paton, & Salzman, 2008; Paton et al., 2006), as well as the orbitofrontal cortex (OFC) (Morrison & Salzman, 2009) encode negative and positive valence. Human neuroimaging research also found that activity of the amygdala (Anders et al., 2008; Comte et al., 2016; Costafreda et al., 2008;
* M. Justin Kim [email protected] 1
Department of Psychology, Sungkyunkwan University, Seoul, South Korea
2
Department of Psychology, University of Oregon, Eugene, OR, USA
3
Department of Psychological & Brain Sciences, Washington University in St. Louis, St. Louis, MO, USA
Cunningham, Van Bavel, & Johnsen., 2008; Jin et al., 2015; Kim et al., 2017b; Phelps & LeDoux, 2005), ventromedial prefrontal cortex (vmPFC)/OFC (Chikazoe et al., 2014; Clithero & Rangel, 2013; Gottfried, O’Doherty, & Dolan, 2002), and the dorsomedial prefrontal cortex (dmPFC) (Etkin, Egner, & Kalisch, 2011; Skerry & Saxe, 2014) was associated with the valence value of emotional stimuli. Furthermore, studies utilizing multivoxel pattern analysis (MVPA) of functional magnetic resonance imaging (fMRI) data and me
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