Elsevier

NeuroImage

Volume 18, Issue 3, March 2003, Pages 675-684
NeuroImage

Regular article
Emotional valence modulates activity in the posterior fusiform gyrus and inferior medial prefrontal cortex in social perception

https://doi.org/10.1016/S1053-8119(02)00038-1Get rights and content

Abstract

Previous studies have shown that during the presentation of emotionally loaded visual stimuli, activity increases in the visual and limbic cortices. This study focuses on empathic reactions induced by presenting pictures of situations and facial expressions from a “third party” point of view only. We measured regional changes in blood flow (rCBF) in nine healthy subjects while they were looking at neutral, positive, or negative emotional pictures of low (facial expressions) and high (persons in real-life situations) social complexity. A significant rCBF increase occurred in the right posterior fusiform gyrus during presentation of emotional pictures of both low and high social complexity. We also observed an interaction between emotionality and social complexity in the left inferior occipital gyrus for situations, where emotionality produced a significantly larger rCBF increase for situations than faces. No significant rCBF changes were observed in the amygdala or other parts of the limbic system. A significant rCBF decrease was found in the right inferior medial prefrontal cortex during presentation of the emotional pictures. This is discussed with respect to the “default mode of the brain” theory. We suggest that there is a neural network in the posterior fusiform and inferior occipital gyrus specialized in identifying emotionally important visual clues. Messages from this and other areas converge to the medial prefrontal cortex, to be evaluated in terms of relevance for attention. We believe that this is a crucial part of a network used in normal empathic reactions and social interactions.

Introduction

Emotional social perception, here defined as the ability to assess the emotional valence of a social situation or the emotional state of a fellow human, is of obvious importance for an individual’s survival and well-being. If confronted with a horrible scene or faces expressing despair or anger, it is often appropriate to intervene or to escape. Rolls (1990) proposed the existence of primary reinforcers, universal unlearned rewards and punishers, to explain human emotion and motivation, using especially single-cell recordings of the inferior prefrontal cortex to support this theory. Primary reinforcers would be coupled to learned, often socially defined, secondary reinforcers by experience, in such a degree that the secondary reinforcers might end up being perceived as more rewarding or punishing than the primary. Especially for higher primates living in social groups is it important to keep track of the different reinforcers (Rolls, 2000a).

Based on findings from numerous neurophysiological studies on humans and animals, Lang and colleagues (1997) introduced the term “natural selective attention,” to describe the fact that any normal individual is more likely to attend to stimuli of evolutionary importance, than to others. When first exposed to a new picture, reaction time responses to probes are significantly slower for emotional than for neutral pictures (Bradley et al., 1992). This tendency to dwell on emotional pictures is also seen in a free-viewing paradigm. When normal subjects themselves can choose how long they want to see a certain picture, unpleasant or pleasant pictures are viewed longer than neutral (referring to findings by Hamm et al 1997, Lang et al 1998b. From an evolutionary point of view, one could postulate the existence of dedicated brain areas for the assignment of emotional valence and attention to social situations.

Neuroimaging studies indeed have shown that numerous brain regions are involved in emotional social perception. However, the exact areas that are activated depend on the type of emotion examined. For instance, fearful visual stimuli typically activate the amygdala (Adolphs, 1995), whereas sexually arousing pictures (Rauch et al., 1999), or beautiful (Aharon et al., 2001) or happy faces (Whalen et al., 1998) activate the basal ganglia. The results also depend on whether a cognitive demand is imposed on the subject while they are looking at the emotional stimuli. For instance, the insular region seems to be recruited only when subjects perform a cognitively demanding task in conjunction with emotional perception (Phan et al., 2002).

The main objective of this study was to investigate the cerebral response pattern to emotionally loaded social perception. We focused on empathic reactions to social situations and facial expressions from a “third-party” point of view. Therefore, no pictures showing aggression directed toward the observer, sexual activities, or angry or fearful facial expressions were presented. Since none of the pictures represented a direct threat or reward for the observer, the induced emotional state should derive from an assessment of how the depicted persons felt. The second objective was to study whether emotionality in pictures of low social complexity (operationalized as pictures displaying mainly emotional facial expressions) activate different areas compared to emotionality in pictures of high social complexity (operationalized as pictures of emotionally loaded social situations where facial expressions are absent or had little relevance for assessment of the situation).

Our regions of interest were the inferior medial prefrontal cortex, the anterior cingulate cortex, the inferior temporal cortex, especially the fusiform gyrus, and the amygdala. All regions have been shown to be activated in emotional activation paradigms (see Phan et al., 2002, for a recent review).

Section snippets

Subjects

Nine male subjects (mean age: 43 years, SD: 11.5 years) participated in the study. The study was approved by the local ethics committee and subjects gave written informed consent. All subjects were unmedicated and without known psychiatric or neurological illnesses. The PET data of one subject were excluded from the group analysis because of major anatomical differences between the subject’s brain anatomy and the average brain template. Manual identification of the anatomical regions of

Behavioral tests

There was a complete agreement on the general grouping and valence of each of the 12 EPS picture series shown during the PET study. The individual rating of each picture after the PET study also showed a high agreement in terms of grouping (Table 1). The average agreement of all pictures was 97.2 ± 2.8% (range 91–100%). The highest agreement was found for the emotional (pleasant and unpleasant) facial pictures. The unpleasant situational pictures were rated more unpleasant than the unpleasant

Discussion

This study investigated the effect of emotional valence on neural activation during visual processing of social stimuli. As predicted, we found that activity in the fusiform gyrus was modulated by the emotional valence, regardless of whether the images showed facial expressions or complex social interactions.

Our methodology differs in three important aspects from the majority of previous studies on emotional processing. First, we made a strict distinction between simple (faces) and complex

Methodological remarks

PET studies often imply the use of a block design. This may engender mental sets and may pose the problems of habituation and anticipation. These problems can be circumvented by using event-related fMRI designs. Notwithstanding these potential pitfalls, fMRI studies have not shown substantially different results for the areas that showed significant rCBF changes in this study. A possible exception concerns the amygdala (see above). However, future studies aimed at directly comparing activations

Conclusion

Our data suggest that the posterior fusiform area may be involved in a broader identification of emotionally important clues in social perception. Although this is mainly a right-hemispheric phenomenon, the left fusiform gyrus also becomes activated as social complexity increases. Messages from these areas and others converge on the right inferior medial prefrontal cortex, to be evaluated in terms of relevance for attention. We believe that this network is crucial to normal empathic reactions

Acknowledgements

We thank Chris Frith (FIL, London) and Richard Lane (Arizona) for helpful comments on an earlier version of the manuscript. We thank the technical staff for skillful assistance during PET scanning. We also thank Peter Neelin (McConnell Brain Imaging Centre, Montreal) and Flemming Andersen (PET Centre, Aarhus) for invaluable help with statistical analysis. Finally, we thank “Nordfoto,” “Jyllands-posten,” and Alan Rowoth for kindly letting us use their photo material in the EPS.

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