Elsevier

NeuroImage

Volume 31, Issue 1, 15 May 2006, Pages 397-409
NeuroImage

Neural correlates of social and nonsocial emotions: An fMRI study

https://doi.org/10.1016/j.neuroimage.2005.11.027Get rights and content

Abstract

Common theories of emotion emphasize valence and arousal dimensions or alternatively, specific emotions, and the search for the underlying neurocircuitry is underway. However, it is likely that other important dimensions for emotional neurocircuitry exist, and one of them is sociality. A social dimension may code whether emotions are addressing an individual's biological/visceral need versus more remote social goals involving semantic meaning or intentionality. Thus, for practical purposes, social emotions may be distinguished from nonsocial emotions based in part on the presence of human forms. In the current fMRI study, we aimed to compare regional coding of the sociality dimension of emotion (nonsocial versus social) versus the valence dimension of emotion (positive versus negative). Using a novel fMRI paradigm, film and picture stimuli were combined to induce and maintain four emotions varying along social and valence dimensions. Nonsocial emotions of positively valenced appetite and negatively valenced disgust and social emotions of positively valenced joy/amusement and negatively valenced sadness were studied. All conditions activated the thalamus. Appetite and disgust activated posterior insula and visual cortex, whereas joy/amusement and sadness activated extended amygdala, superior temporal gyrus, hippocampus, and posterior cingulate. Activations within the anterior cingulate, nucleus accumbens, orbitofrontal cortex, and amygdala were modulated by both social and valence dimensions. Overall, these findings highlight that sociality has a key role in processing emotional valence, which may have implications for patient populations with social and emotional deficits.

Introduction

Emotions are often social, but a social dimension of emotional processing is seldom addressed. Common theories of emotion emphasize different dimensions (e.g., valence, arousal, approach/withdrawal); however, given the obvious role of emotion in transacting social behavior, sociality may be another important dimension of emotional functioning. Along an affective valence dimension, positive and negative emotions occupy two ends of the spectrum. Emotions also can vary along a sociality dimension, varying between either nonsocial or social.

The sociality dimension may reflect the differences between basic biological drives (nonsocial) and complex social interaction (social), where the main difference relies on the presence of human forms interacting in cognitively complex ways involving language, meaning and social intentionality to activate the emotion. In the nonsocial domain, emotions often promote individual survival by directing immediate physiological and behavioral responses to biologically significant stimuli (Darwin, 1998) such as approach behavior to food or sexual stimuli and aversive/avoidance behavior including fighting or fleeing (Frijda, 1988). On the other hand, in the social domain, emotions are motivated to direct long-term social goals and are embedded in semantic and thematic meaning. Thus, nonsocial emotions (e.g., appetite/food desire and disgust) are often elicited by incentive or aversive stimuli that have direct physiological relevance, while social emotions (e.g., joy/humor and sadness) emerge in social interactions with other individuals and are typically embedded in structures of social relationship, intentionality, and meaning. Experimentally, stimuli aimed to trigger emotions in the social domain might rely on the presence or absence of human forms and figures, or depict social scenes to elicit emotions. Using a newly developed behavioral paradigm, we differentiated nonsocial and social emotions, as well as positive and negative emotions, based on subjective and psychophysiological responses. Four distinct response profiles for appetite, disgust, joy/amusement, and sadness indicated sociality influences emotional responses, even to emotions of the same valence (Britton et al., in press). In this study, we asked whether sociality versus valence dimensions of emotion can be distinguished with neuroanatomical specificity?

Sociality includes processing human faces, understanding body language, and making inferences about the intentions of others; thus, it is not surprising that sociality may be processed by a dedicated network of brain regions including fusiform gyrus, superior temporal gyrus, medial prefrontal cortex, amygdala, and posterior cingulate. Face processing has been associated with fusiform and superior temporal gyrus activation. Fusiform gyrus is involved in the perception and recognition of faces (Kanwisher et al., 1997) and processing emotional pictures with human forms and social interactions (Geday et al., 2003). Superior temporal gyrus is involved in understanding complex social signals in eye gaze, mouth movements, and body language (Grossman and Blake, 2002, Pelphrey et al., 2005, Puce et al., 2003). In addition, regions such as medial prefrontal cortex, amygdala, and posterior cingulate have been implicated in self-reflection and assessing others intentions. The medial prefrontal cortex has been implicated in representing states of self versus others, theory of mind, and empathy (Frith and Frith, 2003, Kelley et al., 2002, Phan et al., 2004, Shamay-Tsoory et al., 2004). The amygdala has been associated with processing general salience or meaningfulness of emotional stimuli (Liberzon et al., 2003) and, in particular, social salience evidenced by the deficits in recognizing social emotions and making trustworthiness judgments associated with amygdalar lesions (Adolphs et al., 1998, Adolphs et al., 2002). Posterior cingulate responded to self-reflection and judgments about others (Johnson et al., 2002, Ochsner et al., 2004). Even though these regions may process social features of stimuli, do these regions respond to a social dimension of emotional stimuli, independent of valence?

Neuroimaging studies have identified key brain structures involved in processing appetite, disgust, joy, and sadness. For example, appetite ratings during food presentation have been reported to correlate with blood flow in the right posterior orbitofrontal cortex, suggesting that reward processes are involved (Morris and Dolan, 2001). Humorous film clips have activated the nucleus accumbens (Mobbs et al., 2003, Moran et al., 2004). In addition, amygdala, commonly associated with fear processing (LeDoux, 1998), has been also implicated in processing of happy faces and positive stimuli (Breiter et al., 1996, Liberzon et al., 2003, Somerville et al., 2004). Disgust perception typically activates insular regions (Phillips et al., 1997, Sprengelmeyer et al., 1998), which are also associated with visceral functions, or so-called “gut reactions” (Critchley et al., 2000). Sadness has been associated with subcallosal cingulate (BA25) activation (Phan et al., 2002), and subcallosal cingulate hypometabolism has been reported in depressed patients (Drevets et al., 1997, Mayberg et al., 2000, Mayberg et al., 1999). Although the research on neuroanatomy of emotions (appetite, joy, disgust, and sadness) has been growing, only few studies have compared these emotions across valence (Lane et al., 1997a, Lane et al., 1997b), and in particular, the sociality dimension has been relatively neglected.

To examine whether sociality modulates brain coding of valenced emotions, we used a novel behavioral paradigm, combining film to induce particular emotions and static picture stimuli to maintain those emotions under appropriate conditions for neuroimaging studies (Britton et al., in press). In the current fMRI study, we aimed to (1) identify regions that are involved in processing the sociality dimension of emotions (i.e., regions responsive to social emotions versus nonsocial emotions), (2) identify regions processing emotional valence (i.e., regions responsive to positive emotions versus negative emotions). We used a paradigm that aimed to manipulate sociality (nonsocial, social) and valence (positive, neutral, negative) as independent factors. Nonsocial conditions used images of physical stimuli, such as an appetizing pizza to elicit a nonsocial positively valenced emotion (appetite) and amputation procedures to elicit a nonsocial negatively valenced emotion (disgust). Social conditions had human actors in scripted situations featuring direct interpersonal engagement, using either humor to elicit a positively valenced social emotion (joy/amusement) or social bereavement to elicit a negatively valenced social emotion (sadness). We examined BOLD activation patterns for both main effects of sociality and valence and interactions effects between these two independent factors (sociality × valence). We hypothesized that regions would be more responsive to the social dimension (nonsocial: insula and hypothalamus, social: amygdala, superior temporal gyrus, fusiform, and ventromedial prefrontal cortex); whereas another set of regions may be more responsive to the valence dimension (positive: orbitofrontal cortex, positive/negative: nucleus accumbens, and negative: subgenual anterior cingulate). In addition, some regions may respond to the interaction between social and valence dimensions (e.g., nonsocial negative, disgust: insula).

Section snippets

Participants

Twelve healthy volunteers (6 male, 6 female; age range 19–29 years, mean age 23.6 ± 0.96 years) were recruited from advertisements placed at local universities. All participants were right-handed, English speaking and had normal or corrected-to-normal visual acuity and normal hearing. Participants did not have a history of head injury, learning disability, psychiatric illness, or substance abuse/dependence (>6 months) assessed by Mini-SCID (Sheehan et al., 1998). After explanation of the

On-task performance

Using reaction time as a measure, participants were on-task during the experiment. Participant's responded via button press to 96.5% of the images, missing an equal number of responses to pictures and blanks [t(11) = 1.603, P > 0.137].

The reaction times showed differences among conditions (Table 1). The reaction time to pictures (577.7 ± 24.6 ms) was greater than the reaction time to control images (451.6 ± 11.6 ms) [modality effect: F[1,11] = 4.695, P < 0.052]. The reaction time to social

Discussion

In the current study, four emotions (appetite, disgust, joy, and sadness) induced by film–picture pairs elicited neural activation patterns associated with both sociality and valence dimensions. Nonsocial emotions, appetite and disgust, activated regions involved in visceral response: insula and visual cortex. Nonsocial appetizing pizza also activated anterior cingulate cortex, and nonsocial disgusting wounds also activated amygdala. Social emotions, joy and sadness, activated

Acknowledgment

We thank Keith Newnham for his help with this project.

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