Elsevier

Biological Psychology

Volume 79, Issue 2, October 2008, Pages 165-170
Biological Psychology

Worry, generalized anxiety disorder, and emotion: Evidence from the EEG gamma band

https://doi.org/10.1016/j.biopsycho.2008.04.005Get rights and content

Abstract

The present study examined EEG gamma (35–70 Hz) spectral power distributions during worry inductions in participants suffering from generalized anxiety disorder (GAD) and in control participants without a history of psychiatric illness. As hypothesized, the EEG gamma band was useful for differentiating worry from baseline and relaxation. During worry induction, GAD patients showed higher levels of gamma activity than control participants in posterior electrode sites that have been previously associated with negative emotion. Gamma fluctuations in these electrode sites were correlated with subjective emotional experience ratings lending additional support to interpretations of negative affect. Following 14 weeks of psychotherapy, the GAD group reported less negative affect with worry inductions and the corresponding gamma sites that previously differentiated the clinical from control groups changed for the GAD patients in the direction of control participants. These findings suggest converging evidence that patients suffering from GAD experience more negative emotion during worry and that the EEG gamma band is useful for monitoring fluctuations in pathological worry expected to follow successful treatment.

Introduction

The gamma rhythm (30–100 Hz) is widespread in the central nervous system including in areas associated with emotional processing such as the amygdala and perirhinal cortex (Collins et al., 2001). Recent research continues to suggest connections between EEG gamma activity and emotion with special emphasis on negative emotional processing (e.g. Luo et al., 2007, Matsumoto et al., 2006). Intracranial field potentials recorded from the amygdala confirm that gamma power is highest for aversive stimulus presentations as compared with neutral or pleasant stimuli (Oya et al., 2002).

Spectral power in the gamma band has been associated with emotional processing when both EEG alpha frequency and beta frequency activity have not shown sensitivity to emotional stimulus variations (Müller et al., 1999). Another attribute of gamma as opposed to other indexes of emotional perception is that gamma induced by emotional stimuli is typically not phase-locked to the onset of visual stimulus presentations (Oya et al., 2002). Instead, induced gamma is usually measured over periods of several seconds as with successive presentations of visual stimuli (Müller et al., 1999). This suggests that induced gamma reflects a more integrative or reflective aspect of processing emotional material.

Consistent with the idea that induced gamma fluctuates with extended periods of emotional processing; experimental tasks thought to induce emotional experience have been shown to increase gamma activity. When asked to imagine a phobic object, individuals suffering from a specific phobia show increases in gamma band activation as well as increases in heart rate and respiration (Gemignani et al., 2000). Also, gamma has been shown to decrease during periods of relaxation and to increase during periods of imagining negative emotional material (Sebastiani et al., 2003). Thus, the present study records periods of several minutes during which emotional experiences were thought to be induced.

Distributions of gamma activation recorded from the scalp surface may be important for discovering links between specific emotional experiences and physiological recordings. For example, relatively more gamma power in the right temporal area is associated with positively valenced stimulus presentations and relatively more gamma in the left temporal area is associated with negative stimulus presentations (Müller et al., 1999). The present study sought to contribute to a growing literature linking distributions of induced EEG gamma spectral power to pathological and non-pathological experiences of emotion. We utilized EEG spectral power as well as ratings of subjective experience to assess differences between GAD and non-psychiatric control groups; between baseline, relaxation and worry tasks; and between pre- and post-treatment assessments in our GAD group. Based on a literature linking GAD and worry to negative emotion, we expected gamma during worry to differentiate our patients from controls and to be sensitive to changes in the GAD group expected to follow treatment.

The present study focused on worry as a central negative emotional experience for chronic worriers suffering from GAD. Generalized anxiety disorder (GAD) is characterized by excessive anxiety and uncontrollable worry about a variety of topics (DSM-IV-TR; American Psychiatric Association, 2000). The process of worry in itself is a negative emotional experience whether or not the worrier suffers from GAD (Borkovec and Inz, 1990, Andrews and Borkovec, 1998). Though worry increases reports of negative affect and anxiety, particular physiological systems may not register emotional arousal during worry. When asked to worry, research participants report increases in anxiety while cardiovascular measures do not consistently reflect the change (Borkovec and Hu, 1990, Borkovec et al., 1993). Also, chronic worry does not increase fear-potentiated startle eyeblink EMG amplitudes to emotional stimuli (Nitschke et al., 2002) or muscle activity recorded using EMG (Oathes et al., in press; though see that paper for evidence of worry influences on motor preparation). Thus, it is important to identify a psychophysiological measure which not only characterizes worry experiences but also differentiates individuals suffering from pathological anxiety (GAD) from non-anxious individuals. The present study suggests that the EEG gamma band might function as such an index.

Our initial manipulation check to test the hypothesis that gamma might be sensitive to experimentally induced emotional intensity was based on a prediction that gamma spectral power would be increasingly present in the order from least to greatest beginning with our relaxation task followed by baseline recordings and that worry would facilitate the most gamma activity across our two groups. The relaxation task served as a comparison to worry in that relaxation was also a cognitive induction (which may influence gamma activity; cf. Jensen et al., 2007) but was expected to differ from worry according to the degree of negative affect induced by the experimental instructions. Based on relationships between subjective experiences of negative emotion and GAD (e.g. Borkovec and Inz, 1990, Borkovec and Ruscio, 2001) and between negative emotion and a particular distribution of scalp recorded induced EEG gamma activity (Müller et al., 1999), we expected greater left posterior gamma activity for the GAD group compared to control participants. It was expected that this difference would be especially pronounced during the worry task, as this was the task thought to be most relevant to the GAD diagnosis and its associated negative emotionality. Worry is especially relevant to studying GAD in that chronic uncontrollable worry is the essential feature common to all individuals diagnosed with GAD. Though the Penn State Worry Questionnaire or another measure of trait anxiety might be relevant to chronic worry and GAD, the present study sought to examine a less often assessed aspect of worry: negative affect. To support interpretations related to negative emotionality for group differences in EEG gamma during worry, we assessed ratings of subjective emotional experience during our physiological recording sessions that we expected to correlate with EEG gamma activity.

Section snippets

Participants

Anxious participants were drawn from newspaper advertisements or from outside agency referrals. Advertisements also invited control participants with a request for individuals between 18 and 65 years of age “without current or past anxiety or depression difficulties”. Fifteen clients and 15 control participants were used from the first wave recruited for a therapy outcome study (see Newman et al., 2004 for details). The study was approved by the Office for Research Protections (IRB) at the

Worry and EEG gamma

In the gamma frequency band (35–70 Hz), there was a main effect for task, F(2, 56) = 20.25, ɛ = 0.74, p < .005 (see Fig. 1; though also see worry specific results below and Fig. 2). A main effect of group status (GAD vs. control) across all tasks was not substantiated F(1, 28) = 3.13, p < .90. There was no group by task interaction. Post-hoc analysis of task differences indicated less gamma power during the relaxation task (M = −0.991, S.E. = 0.020) compared to the worry task (M = −0.858, S.E. = 0.026, p < .001),

Discussion

Consistent with predictions based on EEG gamma ties to emotionality (e.g. Sebastiani et al., 2003, Müller et al., 1999), gamma differentiated the worry task from both a relaxation induction period and the resting baseline period (marginal effect). Worry induced a particular pattern of gamma activation which was highly similar for GAD and control participants (no group by electrode site interaction). Instead, the amount of gamma in the relevant sites distinguished our anxious from non-anxious

Acknowledgements

The authors wish to thank Andreas Keil for helpful comments as well as Alison Staples for editing assistance.

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