Elsevier

NeuroImage

Volume 54, Issue 1, 1 January 2011, Pages 689-696
NeuroImage

Functioning of neural systems supporting emotion regulation in anxiety-prone individuals

https://doi.org/10.1016/j.neuroimage.2010.07.041Get rights and content

Abstract

Previous neuroimaging studies suggest that prefrontal cortex (PFC) modulation of the amygdala and related limbic structures is an underlying neural substrate of effortful emotion regulation. Anxiety-prone individuals experience excessive negative emotions, signaling potential dysfunction of systems supporting down-regulation of negative emotions. We examined the hypothesis that anxious individuals require increased recruitment of lateral and medial PFC to decrease negative emotions. An emotion regulation task that involved viewing moderately negative images was presented during functional magnetic resonance imaging (fMRI). Participants with elevated trait anxiety scores (n = 13) and normal trait anxiety scores (n = 13) were trained to reduce negative emotions using cognitive reappraisal. Blood oxygenation level-dependent (BOLD) changes were contrasted for periods when participants were reducing emotions versus when they were maintaining emotions. Compared to healthy controls, anxious participants showed greater activation of brain regions implicated in effortful (lateral PFC) and automatic (subgenual anterior cingulate cortex) control of emotions during down-regulation of negative emotions. Left ventrolateral PFC activity was associated with greater self-reported reduction of distress in anxious participants, but not in healthy controls. These findings provide evidence of altered functioning of neural substrates of emotion regulation in anxiety-prone individuals. Anxious participants required greater engagement of lateral and medial PFC in order to successfully reduce negative emotions.

Research Highlights

►Following training in cognitive reappraisal (an effective emotion regulation skill), anxious and control subjects were equally adept at decreasing subjective negative emotions. ►However, anxious subjects required greater engagement of lateral and medial PFC in order to successfully reduce negative emotions. ►Regions of increased activation in anxious subjects included left dorsolateral PFC, bilateral ventrolateral PFC, dorsomedial PFC and subgenual ACC.

Introduction

Emotion regulation refers to a diverse set of processes that influence the occurrence, intensity, duration, and expression of emotion (Gross and Thompson, 2007). Effortful regulation of negative emotions constitutes one subtype of emotion regulation, in which individuals attempt to reduce negative emotions using deliberate strategies (e.g., distraction, re-interpretation). Empirical investigation has largely focused on this subtype of emotion regulation, given its relevance to emotional disorders and the potential that findings will translate to clinical intervention (Campbell-Sills & Barlow, 2007, Mennin et al., 2005).

Neuroimaging research has revealed neural substrates that contribute to effortful regulation of negative emotions (Ochsner et al., 2002, Ochsner et al., 2004, Levesque et al., 2003, Levesque et al., 2004 Kalisch et al., 2005, Phan et al., 2005, Beauregard et al., 2006, Johnstone et al., 2007, Goldin et al., 2008, Goldin et al., 2009a, Goldin et al., 2009b, New et al., 2009, Koenigsberg et al., 2009, Koenigsberg et al., 2010). Many studies have focused on cognitive reappraisal, an effective strategy (Gross, 1998, Gross & John, 2003) that entails reinterpreting the meaning of a stimulus in such a way that its emotional impact is diminished. Converging evidence suggests that lateral and medial regions of the prefrontal cortex (PFC) [e.g., dorsolateral prefrontal cortex (DLPFC); dorsal anterior cingulate cortex (dACC)] down-regulate neural substrates that are primary emotion processing areas (e.g., amygdala) during cognitive reappraisal (Ochsner et al., 2002, Ochsner et al., 2004, Levesque et al., 2003, Kalisch et al., 2005, Phan et al., 2005, Goldin et al., 2008, Koenigsberg et al., 2010).

With the literature broadly supporting this model of cognitive reappraisal, investigation has recently shifted toward exploring individual differences in the functioning of neural circuitry that supports this strategy. Studies have now examined the functional differences between healthy individuals and patients suffering from major depressive disorder (MDD; Beauregard et al., 2006, Johnstone et al., 2007) social anxiety disorder (SAD; Goldin et al., 2009a, Goldin et al., 2009b), posttraumatic stress disorder (PTSD; New et al., 2009), and borderline personality disorder (Koenigsberg et al., 2009). Although sufficient converging evidence is not yet available to support neural systems models of emotion regulation deficits associated with these disorders, several interesting findings have emerged. Studies of subjects with MDD have provided evidence of hyperactivity of “cognitive control” regions such as ventrolateral PFC (VLPFC; Johnstone et al., 2007) and dorsal anterior cingulate cortex (dACC; Beauregard et al., 2006) during down-regulation of negative emotions. A study of subjects with SAD also showed increased engagement of right DLPFC during regulation of responses to “physical threat” stimuli; however, during regulation of responses to “social threat” stimuli (which are most relevant to their disorder), socially anxious subjects engaged cognitive control regions (e.g., DLPFC, dACC) to a lesser degree than controls (Goldin et al., 2009a). Another study also showed decreased PFC recruitment in patients with PTSD versus controls during down-regulation of emotional responses to negative pictures (New et al., 2009).

The current study aimed to add to the emerging literature on individual differences in the functioning of neural systems supporting emotion regulation, by characterizing differences between subjects with high and normal levels of trait anxiety. The current sample differs from previous samples of patients with specific anxiety and mood disorders: the subjects recruited for the current study, while endorsing high levels of trait anxiety, have no history of treatment for anxiety or other emotional problems. Additionally, they do not self-identify as having a particular disorder (although the majority meet criteria for anxiety disorders upon examination). This sample therefore represents a different segment of the anxiety severity spectrum than previous studies of specific patient groups, and offers an opportunity to observe differences associated with anxiety status that are not confounded by general illness factors such as treatment history.

Subjects scoring in the high and normal ranges on a measure of trait anxiety were trained in cognitive reappraisal, after which they performed an emotion regulation task while undergoing functional magnetic resonance imaging (fMRI). We hypothesized that anxious participants would be able to learn and apply reappraisal, but would require greater top-down control to accomplish down-regulation of negative emotions. Thus, we expected to observe PFC hyperactivity in anxious participants during attempts to reduce negative emotions. We also predicted less attenuation of amygdala response in anxious participants during down-regulation of emotion (i.e., decreased efficacy of reappraisal).

Section snippets

Participants

The institutional review boards of University of California San Diego and San Diego State University approved this study. All participants provided written informed consent.

Participants were drawn from a pool of undergraduates (N = 950) who completed questionnaires for course credit that included the State Trait Anxiety Inventory (STAI; Spielberger et al., 1983). Subjects scoring high in trait anxiety (upper 15th percentile of the STAI distribution) and in the normal range (40th–60th percentile)

Group Differences in Self-Reported Distress

Bonferroni t tests (α = .0125 to account for 4 comparisons based on the distress ratings) were used to examine the effect of group (HA vs. NA) on distress ratings during Baseline, Reduce, and Maintain periods (see Fig. 2). HA subjects reported higher levels of distress during Baseline periods, t (24) = 3.04, p < .01. The HA and NA groups did not differ significantly on levels of distress reported during Reduce, t (24) = 0.83, ns, or Maintain periods, t (24) = 2.29, p = .03 (non-significant with Bonferroni

Discussion

The current investigation highlights functional differences in neural systems supporting emotion regulation in individuals with high and normal levels of trait anxiety. During efforts to reduce emotions, anxious participants showed greater activity in brain regions integral to effortful emotional control (e.g., DLPFC, VLPFC; Ochsner & Gross, 2005, Philips et al., 2008) and automatic regulation of emotional processing (e.g., sgACC; Pezawas et al., 2005).

These results are consistent with our

Acknowledgments

Dr. Campbell-Sills was supported by NIH grant T32 MH 18399-19 while conducting this study. The project was also supported by NIH grants MH65413 and MH64122. The NIH had no further role in study design; in the collection, analysis, and interpretation of the data; in the writing of the report; and in the decision to submit the paper for publication. The authors have no conflicts of interest to report in relation to this study.

The authors wish to thank Carla Hitchcock and Timothy McQueeny who

References (33)

  • K.N. Ochsner et al.

    The cognitive control of emotion

    Trends Cogn. Sci.

    (2005)
  • K.N. Ochsner et al.

    For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion

    Neuroimage

    (2004)
  • K.L. Phan et al.

    Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study

    Biol. Psychiatry

    (2005)
  • A.R. Aron

    The neural basis of inhibition in cognitive control

    Neuroscientist

    (2007)
  • Y. Bar-Haim et al.

    Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study

    Psychol. Bull.

    (2007)
  • M. Beauregard et al.

    Dysfunction in the neural circuitry of emotional self-regulation in major depressive disorder

    NeuroReport

    (2006)
  • Cited by (0)

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