Women with Major Depressive Disorder, Irrespective of Comorbid Anxiety Disorders, Show Blunted Bilateral Frontal Responses during Win and Loss Anticipation

Jennifer L. Stewart; Evan J. White; Rayus Kuplicki; Elisabeth Akeman; Jerzy Bodurka; Yoon Hee Cha; Justin S. Feinstein; Sahib S. Khalsa; Jonathan A. Savitz; Teresa A. Victor; Martin P. Paulus; Robin L. Aupperle

doi:10.1016/j.jad.2020.04.064

Women with Major Depressive Disorder, Irrespective of Comorbid Anxiety Disorders, Show Blunted Bilateral Frontal Responses during Win and Loss Anticipation

Jennifer L. Stewart, Evan J. White, Rayus Kuplicki, Elisabeth Akeman, Jerzy Bodurka, Yoon Hee Cha, Justin S. Feinstein, Sahib S. Khalsa, Jonathan A. Savitz, Teresa A. Victor, Martin P. Paulus, Robin L. Aupperle

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

Background: Electroencephalography (EEG) studies suggest that major depressive disorder (MDD) is associated with lower left than right frontal brain activity (asymmetry), a pattern appearing stronger in women than men, and when elicited during emotionally-relevant paradigms versus an uncontrolled resting state. However, it is unclear whether this asymmetry pattern generalizes to the common presentation of MDD with co-occurring anxiety. Moreover, asymmetry may differ for anxiety subtypes, wherein anxious apprehension (AnxApp: worry characteristic of generalized anxiety disorder) appears left-lateralized, but anxious arousal (AnxAro: panic characteristic of social anxiety, posttraumatic stress, and panic disorders) may be right-lateralized. Methods: This analysis attempted to replicate frontal EEG asymmetry patterns using functional magnetic resonance imaging (fMRI). Participants completed clinical interviews and a monetary incentive delay (MID) task during fMRI recording. We compared five groups of right-handed women from the Tulsa 1000 study, MDD (n=40), MDD-AnxApp (n=26), MDD-AnxAro (n=34), MDD-Both (with AnxApp and AnxAro; n=26), and healthy controls (CTL; n=24), as a function of MID anticipation condition (no win/loss, win, loss) and hemisphere on frontal blood oxygen-level-dependent (BOLD) signal. Results: CTL exhibited higher bilateral superior, middle, and inferior middle frontal gyrus BOLD signal than the four MDD groups for high arousal (win and loss) conditions. However, frontal attenuations were unrelated to current depression/anxiety symptoms, suggestive of a trait as opposed to a state marker. Limitations: This was a cross-sectional analysis restricted to women. Conclusions: Reduced prefrontal cortex recruitment during processing of both positively and negatively valenced stimuli is consistent with the emotion context insensitivity theory of MDD.

Original language	English (US)
Pages (from-to)	157-166
Number of pages	10
Journal	Journal of Affective Disorders
Volume	273
DOIs	https://doi.org/10.1016/j.jad.2020.04.064
State	Published - Aug 1 2020
Externally published	Yes

Bibliographical note

Funding Information:
This work has been supported in part by The William K. Warren Foundation, the National Institute of Mental Health (K23MH112949 (SSK), K23MH108707 (RLA)), and the National Institute of General Medical Sciences Center Grant, P20GM121312. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. JerzyBodurka Yoon-HeeCha Justin S.Feinstein Sahib S.Khalsa Jonathan A. Savitz Teresa A.Victor.

Funding Information:
This work has been supported in part by The William K. Warren Foundation, the National Institute of Mental Health (K23MH112949 (SSK), K23MH108707 (RLA)), and the National Institute of General Medical Sciences Center Grant, P20GM121312. The funding sources had no influence on study design, data analysis, manuscript preparation, or the decision to submit this manuscript for publication.

Funding Information:
This work has been supported in part by The William K. Warren Foundation, the National Institute of Mental Health (K23MH112949 (SSK), K23MH108707 (RLA)), and the National Institute of General Medical Sciences Center Grant, P20GM121312. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. JerzyBodurka Yoon-HeeCha Justin S.Feinstein Sahib S.Khalsa Jonathan A. Savitz Teresa A.Victor.

Publisher Copyright:
© 2020 Elsevier B.V.

Keywords

Anxious apprehension
Anxious arousal
Frontal brain asymmetry
Functional magnetic resonance imaging
Major depressive disorder

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Stewart, J. L., White, E. J., Kuplicki, R., Akeman, E., Bodurka, J., Cha, Y. H., Feinstein, J. S., Khalsa, S. S., Savitz, J. A., Victor, T. A., Paulus, M. P., & Aupperle, R. L. (2020). Women with Major Depressive Disorder, Irrespective of Comorbid Anxiety Disorders, Show Blunted Bilateral Frontal Responses during Win and Loss Anticipation. Journal of Affective Disorders, 273, 157-166. https://doi.org/10.1016/j.jad.2020.04.064

Stewart, JL, White, EJ, Kuplicki, R, Akeman, E, Bodurka, J, Cha, YH, Feinstein, JS, Khalsa, SS, Savitz, JA, Victor, TA, Paulus, MP & Aupperle, RL 2020, 'Women with Major Depressive Disorder, Irrespective of Comorbid Anxiety Disorders, Show Blunted Bilateral Frontal Responses during Win and Loss Anticipation', Journal of Affective Disorders, vol. 273, pp. 157-166. https://doi.org/10.1016/j.jad.2020.04.064

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title = "Women with Major Depressive Disorder, Irrespective of Comorbid Anxiety Disorders, Show Blunted Bilateral Frontal Responses during Win and Loss Anticipation",

abstract = "Background: Electroencephalography (EEG) studies suggest that major depressive disorder (MDD) is associated with lower left than right frontal brain activity (asymmetry), a pattern appearing stronger in women than men, and when elicited during emotionally-relevant paradigms versus an uncontrolled resting state. However, it is unclear whether this asymmetry pattern generalizes to the common presentation of MDD with co-occurring anxiety. Moreover, asymmetry may differ for anxiety subtypes, wherein anxious apprehension (AnxApp: worry characteristic of generalized anxiety disorder) appears left-lateralized, but anxious arousal (AnxAro: panic characteristic of social anxiety, posttraumatic stress, and panic disorders) may be right-lateralized. Methods: This analysis attempted to replicate frontal EEG asymmetry patterns using functional magnetic resonance imaging (fMRI). Participants completed clinical interviews and a monetary incentive delay (MID) task during fMRI recording. We compared five groups of right-handed women from the Tulsa 1000 study, MDD (n=40), MDD-AnxApp (n=26), MDD-AnxAro (n=34), MDD-Both (with AnxApp and AnxAro; n=26), and healthy controls (CTL; n=24), as a function of MID anticipation condition (no win/loss, win, loss) and hemisphere on frontal blood oxygen-level-dependent (BOLD) signal. Results: CTL exhibited higher bilateral superior, middle, and inferior middle frontal gyrus BOLD signal than the four MDD groups for high arousal (win and loss) conditions. However, frontal attenuations were unrelated to current depression/anxiety symptoms, suggestive of a trait as opposed to a state marker. Limitations: This was a cross-sectional analysis restricted to women. Conclusions: Reduced prefrontal cortex recruitment during processing of both positively and negatively valenced stimuli is consistent with the emotion context insensitivity theory of MDD.",

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author = "Stewart, {Jennifer L.} and White, {Evan J.} and Rayus Kuplicki and Elisabeth Akeman and Jerzy Bodurka and Cha, {Yoon Hee} and Feinstein, {Justin S.} and Khalsa, {Sahib S.} and Savitz, {Jonathan A.} and Victor, {Teresa A.} and Paulus, {Martin P.} and Aupperle, {Robin L.}",

note = "Funding Information: This work has been supported in part by The William K. Warren Foundation, the National Institute of Mental Health (K23MH112949 (SSK), K23MH108707 (RLA)), and the National Institute of General Medical Sciences Center Grant, P20GM121312. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. JerzyBodurka Yoon-HeeCha Justin S.Feinstein Sahib S.Khalsa Jonathan A. Savitz Teresa A.Victor. Funding Information: This work has been supported in part by The William K. Warren Foundation, the National Institute of Mental Health (K23MH112949 (SSK), K23MH108707 (RLA)), and the National Institute of General Medical Sciences Center Grant, P20GM121312. The funding sources had no influence on study design, data analysis, manuscript preparation, or the decision to submit this manuscript for publication. Funding Information: This work has been supported in part by The William K. Warren Foundation, the National Institute of Mental Health (K23MH112949 (SSK), K23MH108707 (RLA)), and the National Institute of General Medical Sciences Center Grant, P20GM121312. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. JerzyBodurka Yoon-HeeCha Justin S.Feinstein Sahib S.Khalsa Jonathan A. Savitz Teresa A.Victor. Publisher Copyright: {\textcopyright} 2020 Elsevier B.V.",

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doi = "10.1016/j.jad.2020.04.064",

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volume = "273",

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T1 - Women with Major Depressive Disorder, Irrespective of Comorbid Anxiety Disorders, Show Blunted Bilateral Frontal Responses during Win and Loss Anticipation

AU - Stewart, Jennifer L.

AU - White, Evan J.

AU - Kuplicki, Rayus

AU - Akeman, Elisabeth

AU - Bodurka, Jerzy

AU - Cha, Yoon Hee

AU - Feinstein, Justin S.

AU - Khalsa, Sahib S.

AU - Savitz, Jonathan A.

AU - Victor, Teresa A.

AU - Paulus, Martin P.

AU - Aupperle, Robin L.

N1 - Funding Information: This work has been supported in part by The William K. Warren Foundation, the National Institute of Mental Health (K23MH112949 (SSK), K23MH108707 (RLA)), and the National Institute of General Medical Sciences Center Grant, P20GM121312. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. JerzyBodurka Yoon-HeeCha Justin S.Feinstein Sahib S.Khalsa Jonathan A. Savitz Teresa A.Victor. Funding Information: This work has been supported in part by The William K. Warren Foundation, the National Institute of Mental Health (K23MH112949 (SSK), K23MH108707 (RLA)), and the National Institute of General Medical Sciences Center Grant, P20GM121312. The funding sources had no influence on study design, data analysis, manuscript preparation, or the decision to submit this manuscript for publication. Funding Information: This work has been supported in part by The William K. Warren Foundation, the National Institute of Mental Health (K23MH112949 (SSK), K23MH108707 (RLA)), and the National Institute of General Medical Sciences Center Grant, P20GM121312. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. JerzyBodurka Yoon-HeeCha Justin S.Feinstein Sahib S.Khalsa Jonathan A. Savitz Teresa A.Victor. Publisher Copyright: © 2020 Elsevier B.V.

PY - 2020/8/1

Y1 - 2020/8/1

N2 - Background: Electroencephalography (EEG) studies suggest that major depressive disorder (MDD) is associated with lower left than right frontal brain activity (asymmetry), a pattern appearing stronger in women than men, and when elicited during emotionally-relevant paradigms versus an uncontrolled resting state. However, it is unclear whether this asymmetry pattern generalizes to the common presentation of MDD with co-occurring anxiety. Moreover, asymmetry may differ for anxiety subtypes, wherein anxious apprehension (AnxApp: worry characteristic of generalized anxiety disorder) appears left-lateralized, but anxious arousal (AnxAro: panic characteristic of social anxiety, posttraumatic stress, and panic disorders) may be right-lateralized. Methods: This analysis attempted to replicate frontal EEG asymmetry patterns using functional magnetic resonance imaging (fMRI). Participants completed clinical interviews and a monetary incentive delay (MID) task during fMRI recording. We compared five groups of right-handed women from the Tulsa 1000 study, MDD (n=40), MDD-AnxApp (n=26), MDD-AnxAro (n=34), MDD-Both (with AnxApp and AnxAro; n=26), and healthy controls (CTL; n=24), as a function of MID anticipation condition (no win/loss, win, loss) and hemisphere on frontal blood oxygen-level-dependent (BOLD) signal. Results: CTL exhibited higher bilateral superior, middle, and inferior middle frontal gyrus BOLD signal than the four MDD groups for high arousal (win and loss) conditions. However, frontal attenuations were unrelated to current depression/anxiety symptoms, suggestive of a trait as opposed to a state marker. Limitations: This was a cross-sectional analysis restricted to women. Conclusions: Reduced prefrontal cortex recruitment during processing of both positively and negatively valenced stimuli is consistent with the emotion context insensitivity theory of MDD.

AB - Background: Electroencephalography (EEG) studies suggest that major depressive disorder (MDD) is associated with lower left than right frontal brain activity (asymmetry), a pattern appearing stronger in women than men, and when elicited during emotionally-relevant paradigms versus an uncontrolled resting state. However, it is unclear whether this asymmetry pattern generalizes to the common presentation of MDD with co-occurring anxiety. Moreover, asymmetry may differ for anxiety subtypes, wherein anxious apprehension (AnxApp: worry characteristic of generalized anxiety disorder) appears left-lateralized, but anxious arousal (AnxAro: panic characteristic of social anxiety, posttraumatic stress, and panic disorders) may be right-lateralized. Methods: This analysis attempted to replicate frontal EEG asymmetry patterns using functional magnetic resonance imaging (fMRI). Participants completed clinical interviews and a monetary incentive delay (MID) task during fMRI recording. We compared five groups of right-handed women from the Tulsa 1000 study, MDD (n=40), MDD-AnxApp (n=26), MDD-AnxAro (n=34), MDD-Both (with AnxApp and AnxAro; n=26), and healthy controls (CTL; n=24), as a function of MID anticipation condition (no win/loss, win, loss) and hemisphere on frontal blood oxygen-level-dependent (BOLD) signal. Results: CTL exhibited higher bilateral superior, middle, and inferior middle frontal gyrus BOLD signal than the four MDD groups for high arousal (win and loss) conditions. However, frontal attenuations were unrelated to current depression/anxiety symptoms, suggestive of a trait as opposed to a state marker. Limitations: This was a cross-sectional analysis restricted to women. Conclusions: Reduced prefrontal cortex recruitment during processing of both positively and negatively valenced stimuli is consistent with the emotion context insensitivity theory of MDD.

KW - Anxious apprehension

KW - Anxious arousal

KW - Frontal brain asymmetry

KW - Functional magnetic resonance imaging

KW - Major depressive disorder

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Women with Major Depressive Disorder, Irrespective of Comorbid Anxiety Disorders, Show Blunted Bilateral Frontal Responses during Win and Loss Anticipation

Abstract

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Keywords

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