Elsevier

Biological Psychiatry

Volume 53, Issue 6, 15 March 2003, Pages 502-510
Biological Psychiatry

Neural circuitry underlying voluntary suppression of sadness

https://doi.org/10.1016/S0006-3223(02)01817-6Get rights and content

Abstract

Background

The ability to voluntarily self-regulate negative emotion is essential to a healthy psyche. Indeed, a chronic incapacity to suppress negative emotion might be a key factor in the genesis of depression and anxiety. Regarding the neural underpinnings of emotional self-regulation, a recent functional neuroimaging study carried out by our group has revealed that the dorsolateral prefrontal cortex (DLPFC) and anterior cingulate cortex are involved in voluntary suppression of sexual arousal. As few things are known, still, with respect to the neural substrate underlying volitional self-regulation of basic emotions, here we used functional magnetic resonance imaging to identify the neural circuitry associated with the voluntary suppression of sadness.

Methods

Twenty healthy female subjects were scanned during a Sad condition and a Suppression condition. In the Sad condition, subjects were instructed to react normally to sad film excerpts whereas, in the Suppression condition, they were asked to voluntarily suppress any emotional reaction in response to comparable stimuli.

Results

Transient sadness was associated with significant loci of activation in the anterior temporal pole and the midbrain, bilaterally, as well as in the left amygdala, left insula, and right ventrolateral prefrontal cortex (VLPFC) (Brodmann area [BA] 47). Correlational analyses carried out between self-report ratings of sadness and regional blood oxygen level dependent (BOLD) signal changes revealed the existence of positive correlations in the right VLPFC (BA 47), bilaterally, as well as in the left insula and the affective division of the left anterior cingulate gyrus (BA 24/32). In the Suppression condition, significant loci of activation were noted in the right DLPFC (BA 9) and the right orbitofrontal cortex (OFC) (BA 11), and positive correlations were found between the self-report ratings of sadness and BOLD signal changes in the right OFC (BA 11) and right DLPFC (BA 9).

Conclusions

These results confirm the key role played by the DLPFC in emotional self-regulation. They also indicate that the right DLPFC and right OFC are components of a neural circuit implicated in voluntary suppression of sadness.

Introduction

Emotional self-regulation has been defined as “the extrinsic and intrinsic processes responsible for monitoring, evaluating, and modifying emotional reaction, especially their intensive and temporal features, to accomplish one’s goal” (Thompson 1994). In a colloquial usage, emotional self-regulation often refers either to suppression, maintenance, or enhancement of the subjective emotional experience, but it also applies to the modulation of the behavioral and physiologic dimensions of emotion (Gross 1999). Rationalization and reappraisal are among some of the most prevalent cognitive strategies used to self-regulate emotion Gross 1999, Hariri et al 2000.

Conscious and voluntary self-regulation of emotion represents indisputably one of the most remarkable mental faculties having emerged throughout the course of human evolution. In our view, this metacognitive capacity constitutes one of the cornerstones on which human societal systems are built. Supportive of such a view, there is mounting evidence that a chronic incapacity to suppress negative emotion may be a key factor in the genesis of depression, anxiety, and aggressive or violent behaviors Davidson et al 2000, Jackson et al 2000. With respect to major depression, this dysregulation of negative affect may be related to the cognitive/executive inhibitory deficit that characterizes depressed patients. This impairment is manifested by increased choice reaction-time on a Stroop-Color-Word test and increased effect of interference on the Visuo-Spatial Interference Test, when compared with normal control subjects Lemelin et al 1996, Lemelin et al 1997.

Regarding the neural bases of such capacity, it was postulated several decades ago that a fronto–limbic network is involved in emotional suppression (Nauta 1971). More recently, evidence from lesion studies in animals, and clinical neuropsychological, psychophysiological, and functional neuroimaging studies in humans have led to the view that a neural circuit comprising several prefrontal cortex (PFC) regions (e.g., orbitofrontal, anterior cingulate) underlies emotional suppression (Davidson et al 2000). The results of a functional magnetic resonance imaging (fMRI) study recently carried out by our group to test the validity of this view (Beauregard et al 2001) demonstrated the involvement of the dorsolateral PFC (DLPFC) and anterior cingulate cortex in voluntary suppression of sexual arousal, a positive emotional state.

In the present study, we used whole-brain fMRI to delineate the neural circuitry associated with the voluntary suppression of sadness, a basic emotion with a negative valence (Plutchik 1994). We predicted a priori that various subdivisions of the PFC (DLPFC, orbitofrontal cortex [OFC], medial PFC, and anterior cingulate cortex) would be associated with voluntary suppression of sadness.

Section snippets

Subjects

Twenty healthy female volunteers (right-handed Caucasian university students) (age range: 20–30, mean age: 24.3 years) took part in the study. They had no history of psychiatric or neurologic disorder. These subjects all gave written, informed consent, and the study was approved by the ethics committee of Centre hospitalier de l’Université de Montréal, Hôpital Notre-Dame.

Behavioral procedures

Blood oxygen level dependent (BOLD) signal changes were measured during two experimental conditions: a Sad condition and a

Self-report data

Phenomenologically, the viewing of the sad film excerpts, in both the Sad and the Suppression conditions, induced a transient state of sadness in all subjects. As expected, the mean level of reported sadness was significantly higher in the Sad condition (mean = 5.15; SD = 1.30; range: 2–7) than in the Suppression condition (mean = 1.85; SD = 1.42; range: 0–4) (p < .0001). During both experimental conditions, the viewing of the sad film excerpts did not practically produce marked changes in the

Discussion

The main goal of the present study was to identify the neural substrate associated with voluntary suppression of sadness. This study comprised two experimental conditions, a Sad condition and a Suppression condition. In the Sad condition, significant loci of activation were noted, bilaterally, in the anterior temporal pole (BA 21 and 38) and the midbrain. Significant loci of activation were also seen in the right VLPFC (BA 47), left amygdala, and left insula. In the Suppression condition,

Acknowledgements

This work was supported by grants from National Sciences and Engineering Research Council of Canada and the National Alliance for Research in Schizophrenia and Depression to MB.

The authors thank the staff of the Département de radiologie, Centre Hospitalier de l’Université de Montréal, Hôpital Notre-Dame, for their skillful technical assistance.

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