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Attenuated responses to emotional expressions in women with generalized anxiety disorder

Published online by Cambridge University Press:  18 August 2010

M. E. Palm ,
R. Elliott ,
S. McKie ,
J. F. W. Deakin  and
I. M. Anderson
M. E. Palm*
Affiliation:
The University of Manchester, Neuroscience & Psychiatry Unit, Stopford Building, Manchester, UK
R. Elliott
Affiliation:
The University of Manchester, Neuroscience & Psychiatry Unit, Stopford Building, Manchester, UK
S. McKie
Affiliation:
The University of Manchester, Neuroscience & Psychiatry Unit, Stopford Building, Manchester, UK
J. F. W. Deakin
Affiliation:
The University of Manchester, Neuroscience & Psychiatry Unit, Stopford Building, Manchester, UK
I. M. Anderson
Affiliation:
The University of Manchester, Neuroscience & Psychiatry Unit, Stopford Building, Manchester, UK
*
*Address for correspondence: Dr M. E. Palm, Nowgen, A Centre for Genetics in Healthcare, NIHR Biomedical Research Centre, The University of Manchester, The Nowgen Centre, 29 Grafton Street, Manchester M13 9WU, UK. (Email: [email protected])
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Abstract

Background

Generalized anxiety disorder (GAD) is under-researched despite its high prevalence and large impact on the healthcare system. There is a paucity of functional magnetic resonance imaging (fMRI) studies that explore the neural correlates of emotional processing in GAD. The present study investigated the blood oxygen level dependent (BOLD) response to processing positive and negative facial emotions in patients with GAD.

Method

A total of 15 female GAD patients and 16 female controls undertook an implicit face emotion task during fMRI scanning. They also performed a face emotion recognition task outside the scanner.

Results

The only behavioural difference observed in GAD patients was less accurate detection of sad facial expressions compared with control participants. However, GAD patients showed an attenuated BOLD signal in the prefrontal cortex to fearful, sad, angry and happy facial expressions and an attenuated signal in the anterior cingulate cortex to happy and fearful facial expressions. No differences were found in amygdala response.

Conclusions

In contrast with previous research, this study found BOLD signal attenuation in the ventrolateral and medial prefrontal cortex and the anterior cingulate cortex during face emotion processing, consistent with a hypothesis of hypo-responsivity to external emotional stimuli in GAD. These decreases were in areas that have been implicated in emotion and cognition and may reflect an altered balance between internally and externally directed attentional processes.

Keywords

AnxietyemotionfMRIGAD
Type
Original Articles
Information
Psychological Medicine , Volume 41 , Issue 5 , May 2011 , pp. 1009 - 1018
Copyright
Copyright © Cambridge University Press 2010

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References

Adolphs, R, Tranel, D, Damasio, H, Damasio, AR (1995). Fear and the human amygdala. Journal of Neuroscience 15, 5879–5891.CrossRefGoogle ScholarPubMed
Ammons, RB, Ammons, CH (1962). The Quick Test (QT): provisional manual. Psychological Reports 11, 111–116.CrossRefGoogle Scholar
Argyropoulos, SV, Ploubidis, GB, Wright, TS, Palm, ME, Hood, SD, Nash, JR, Taylor, AC, Forshall, SW, Anderson, IM, Nutt, DJ, Potokar, JP (2007). Development and validation of the Generalized Anxiety Disorder Inventory (GADI). Journal of Psychopharmacology 21, 145–152.CrossRefGoogle ScholarPubMed
Beck, AT, Ward, C, Mendelson, M (1961). Beck Depression Inventory (BDI). Archives of General Psychiatry 4, 561–571.CrossRefGoogle Scholar
Blair, K, Shaywitz, J, Smith, BW, Rhodes, R, Geraci, M, Jones, M, McCaffrey, D, Vythilingam, M, Finger, E, Mondillo, K (2008). Response to emotional expressions in generalized social phobia and generalized anxiety disorder: evidence for separate disorders. American Journal of Psychiatry 165, 1193–1202.CrossRefGoogle ScholarPubMed
Bishop, SJ (2008). Neural mechanisms underlying selective attention to threat. Annals of the New York Academy of Sciences 1129, 141–152.CrossRefGoogle ScholarPubMed
Bishop, S, Duncan, J, Brett, M, Lawrence, AD (2004). Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli. Nature Neuroscience 7, 184–188.CrossRefGoogle ScholarPubMed
Borkovec, TD, Newman, MG (1998). Worry and generalized anxiety disorder. In Comprehensive Clinical Psychology: Vol. 6. Adults: Clinical Formulation and Treatment (ed. Salkovskis, P., Bellack, A. S. and Hersen, M.), pp. 439–459. Pergamon: New York.CrossRefGoogle Scholar
Borkovec, TD, Roemer, L (1995). Perceived functions of worry among generalized anxiety disorder subjects: distraction from more emotionally distressing topics? Journal of Behavior Therapy and Experimental Psychiatry 26, 25–30.CrossRefGoogle ScholarPubMed
Bremner, JD, Staib, LH, Kaloupek, D, Southwick, SM, Soufer, R, Charney, DS (1999). Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study. Biological Psychiatry 45, 806–816.CrossRefGoogle ScholarPubMed
Chua, P, Krams, M, Toni, I, Passingham, R, Dolan, R (1999). A functional anatomy of anticipatory anxiety. NeuroImage 9, 563–571.CrossRefGoogle ScholarPubMed
Critchley, HD, Mathias, CJ, Dolan, RJ (2001). Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 29, 537–545.CrossRefGoogle ScholarPubMed
Dugas, MJ, Anderson, KG, Deschenes, SS, Donegan, E (2010). Generalized anxiety disorders publications: Where do we stand a decade later? Journal of Anxiety Disorders Published online: 25 May 2010. doi:10.1016/j.janxdis.2010.05.012.CrossRefGoogle ScholarPubMed
Ekman, PF, Friesen, WV (1976). Pictures of Facial Affect. Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Etkin, A, Prater, KE, Hoeft, F, Menon, V, Schatzberg, AF (2010). Failure of anterior cingulate activation and connectivity with the amygdala during implicit regulation of emotional processing in generalized anxiety disorder. American Journal of Psychiatry 167, 545–554.CrossRefGoogle ScholarPubMed
Etkin, A, Prater, KE, Schatzberg, AF, Menon, V, Greicius, MD (2009). Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Archives of General Psychiatry 12, 1361–1372.CrossRefGoogle Scholar
Fischer, H, Andersson, JL, Furmark, T, Fredrikson, M (1998). Brain correlates of an unexpected panic attack: a human positron emission tomographic study. Neuroscience Letters 251, 137–140.CrossRefGoogle ScholarPubMed
Grant, BF, Hasin, DS, Stinson, FS, Dawson, DA, June Ruan, W, Goldstein, RB, Smith, SM, Saha, TD, Huang, B (2005). Prevalence, correlates, co-morbidity, and comparative disability of DSM-IV generalized anxiety disorder in the USA: results from the National Epidemiologic Survey on Alcohol and Related Conditions. Psychological Medicine 35, 1747–1759.CrossRefGoogle ScholarPubMed
Hamilton, M (1959). The assessment of anxiety states by rating. The British Journal of Medical Psychology 32, 50–55.CrossRefGoogle ScholarPubMed
Hariri, AR, Mattay, VS, Tessitore, A, Fera, F, Weinberger, DR (2003). Neocortical modulation of the amygdala response to fearful stimuli. Biological Psychiatry 53, 494–501.CrossRefGoogle ScholarPubMed
Harmer, CJ, Perrett, DI, Cowen, PJ, Goodwin, GM (2001). Administration of the beta-adrenoceptor blocker propranolol impairs the processing of facial expressions of sadness. Psychopharmacology 154, 383–389.CrossRefGoogle ScholarPubMed
Hofer, A, Siedentopf, CM, Ischebeck, A, Rettenbacher, MA, Verius, M, Felber, S, Fleischhacker, WW (2007). Sex differences in brain activation patterns during processing of positively and negatively valenced emotional words. Psychological Medicine 37, 109–119.CrossRefGoogle ScholarPubMed
Hoffman, DL, Dukes, EM, Wittchen, HU (2008). Human and economic burden of generalized anxiety disorder. Depression and Anxiety 25, 72–90.CrossRefGoogle ScholarPubMed
Kesler-West, ML, Andersen, AH, Smith, CD, Avison, MJ, Davis, CE, Kryscio, RJ, Blonder, LX (2001). Neural substrates of facial emotion processing using fMRI. Brain Research, Cognitive Brain Research 11, 213–226.CrossRefGoogle ScholarPubMed
Klein, S, Smolka, MN, Wrase, J, Gruesser, SM, Mann, K, Braus, DF, Heinz, A (2003). The influence of gender and emotional valence of visual cues on fMRI activation in humans. Pharmacopsychiatry 36, 191–194.Google ScholarPubMed
Lee, BT, Seok, JH, Lee, BC, Cho, SW, Yoon, BJ, Lee, KU, Chae, JH, Choi, IG, Ham, BJ (2008 a). Neural correlates of affective processing in response to sad and angry facial stimuli in patients with major depressive disorder. Progress in Neuro-psychopharmacology & Biological Psychiatry 32, 778–785.CrossRefGoogle ScholarPubMed
Lee, E, Kang, JI, Park, IH, Kim, JJ, An, SK (2008 b). Is a neutral face really evaluated as being emotionally neutral? Psychiatry Research 157, 77–85.CrossRefGoogle ScholarPubMed
Leppanen, JM (2006). Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Current Opinion in Psychiatry 19, 34–39.CrossRefGoogle ScholarPubMed
Phan, KL, Fitzgerald, DA, Nathan, PJ, Tancer, ME (2006). Association between amygdala hyperactivity to harsh faces and severity of social anxiety symptoms in generalized social phobia. Biological Psychiatry 59, 424–429.CrossRefGoogle ScholarPubMed
McClure, EB, Adler, A, Monk, CS, Cameron, J, Smith, S, Nelson, EE, Leibenluft, E, Ernst, M, Pine, DS (2007). fMRI predictors of treatment outcome in pediatric anxiety disorders. Psychopharmacology 191, 97–105.CrossRefGoogle ScholarPubMed
Maslowsky, J, Mogg, K, Bradley, BP, McClure-Tone, E, Ernst, M, Pine, DS, Monk, CS (2010). A preliminary investigation of neural correlates of treatment in adolescents with generalized anxiety disorder. Journal of Child and Adolescent Psychopharmacology 20, 105–111.CrossRefGoogle ScholarPubMed
Matthews, SC, Strigo, IA, Simmons, AN, Yang, TT, Paulus, MP (2008). Decreased functional coupling of the amygdala and supragenual cingulate is related to increased depression in unmedicated individuals with current major depressive disorder. Journal of Affective Disorders 111, 13–20.CrossRefGoogle ScholarPubMed
Mennin, DS, Heimberg, RG, Turk, CL, Fresco, DM (2002). Applying an emotion regulation framework to integrative approaches to generalized anxiety disorder. Clinical Psychology: Science and Practice 9, 85–90.Google Scholar
Mennin, DS, Heimberg, RG, Turk, CL, Fresco, DM (2005). Preliminary evidence for an emotion dysregulation model of generalized anxiety disorder. Behaviour Research and Therapy 43, 1281–1310.CrossRefGoogle ScholarPubMed
Meyer, TJ, Miller, ML, Metzger, RL, Borkovec, TD (1990). Development and validation of the Penn State Worry Questionnaire. Behaviour Research and Therapy 28, 487–495.CrossRefGoogle ScholarPubMed
Monk, CS, Nelson, EE, McClure, EB, Mogg, K, Bradley, BP, Leibenluft, E, Blair, RJR, Chen, G, Charney, DS, Ernst, M, Pine, DS (2006). Ventrolateral prefrontal cortex activation and attentional bias in response to angry faces in adolescents with generalized anxiety disorder. American Journal of Psychiatry 163, 1091–1097.CrossRefGoogle ScholarPubMed
Monk, CS, Telzer, EH, Mogg, K, Bradley, BP, Mai, X, Louro, HM, Chen, G, McClure-Tone, EB, Ernst, M, Pine, DS (2008). Amygdala and ventrolateral prefrontal cortex activation to masked angry faces in children and adolescents with generalized anxiety disorder. Archives of General Psychiatry 65, 568–576.CrossRefGoogle ScholarPubMed
Montagne, B, Schutters, S, Westenberg, HG, van Honk, J, Kessels, RP, de Haan, EH (2006). Reduced sensitivity in the recognition of anger and disgust in social anxiety disorder. Cognitive Neuropsychiatry 11, 389–401.CrossRefGoogle ScholarPubMed
Nitschke, JB, Sarinopoulos, I, Mackiewicz, KL, Schaefer, HS, Davidson, RJ (2006). Functional neuroanatomy of aversion and its anticipation. NeuroImage 29, 106–116.CrossRefGoogle ScholarPubMed
Nitschke, JB, Sarinopoulos, I, Oathes, DJ, Johnstone, T, Whalen, PJ, Davidson, RJ, Kalin, NH (2009). Anticipatory activation in the amygdala and anterior cingulate in generalized anxiety disorder and prediction of treatment response. American Journal of Psychiatry 166, 302–310.CrossRefGoogle ScholarPubMed
Ochsner, KN, Ray, RD, Cooper, JC, Robertson, ER, Chopra, S, Gabrieli, JD, Gross, JJ (2004). For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage 23, 483–499.CrossRefGoogle ScholarPubMed
Olatunji, BO, Moretz, MW, Zlomke, KR (2010). Linking cognitive avoidance and GAD symptoms: the mediating role of fear of emotion. Behaviour Research and Therapy 48, 435–441.CrossRefGoogle ScholarPubMed
Paulesu, E, Sambugaro, E, Torti, T, Danelli, L, Ferri, F, Scialfa, G, Sberna, M, Ruggiero, GM, Bottini, G, Sassaroli, S (2010). Neural correlates of worry in generalized anxiety disorder and in normal controls: a functional MRI study. Psychological Medicine 40, 117–124.CrossRefGoogle ScholarPubMed
Phan, KL, Wager, T, Taylor, SF, Liberzon, I (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 16, 331–348.CrossRefGoogle ScholarPubMed
Philippot, P, Douilliez, C (2005). Social phobics do not misinterpret facial expression of emotion. Behaviour Research and Therapy 43, 639–652.CrossRefGoogle Scholar
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biological Psychiatry 54, 504–514.CrossRefGoogle ScholarPubMed
Ray, RD, Ochsner, KN, Cooper, JC, Robertson, ER, Gabrieli, JD, Gross, JJ (2005). Individual differences in trait rumination and the neural systems supporting cognitive reappraisal. Cognitive, Affective & Behavioral Neuroscience 5, 156–168.CrossRefGoogle ScholarPubMed
Rogers, MA, Kasai, K, Koji, M, Fukuda, R, Iwanami, A, Nakagome, K, Fukuda, M, Kato, N (2004). Executive and prefrontal dysfunction in unipolar depression: a review of neuropsychological and imaging evidence. Neuroscience Research 50, 1–11.CrossRefGoogle ScholarPubMed
Scheuerecker, J, Frodl, T, Koutsouleris, N, Zetzsche, T, Wiesmann, M, Kleemann, A, Bruckmann, H, Schmitt, G, Moller, HJ, Meisenzahl, EM (2007). Cerebral differences in explicit and implicit emotional processing – an fMRI study. Neuropsychobiology 56, 32–39.CrossRefGoogle ScholarPubMed
Spielberger, CD (1983). Manual for the State-Trait Anxiety Inventory (STAI). Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Spitzer, RL, Williams, JBW, Gibbon, M, First, MB (1992). The Structured Clinical Interview for DSM-III-R (SCID): I. History, rationale, and description. Archives of General Psychiatry 49, 624–629.CrossRefGoogle ScholarPubMed
Turk, CL, Heimberg, RG, Luterek, JA, Mennin, DS, Fresco, DM (2005). Emotion dysregulation in generalized anxiety disorder: a comparison with social anxiety disorder. Cognitive Therapy and Research 29, 89–106.CrossRefGoogle Scholar
Whalen, PJ, Johnstone, T, Somerville, LH, Nitschke, JB, Polis, S, Alexander, AL, Davidson, RJ, Kalin, NH (2008). A functional magnetic resonance imaging predictor of treatment response to venlafaxine in generalized anxiety disorder. Biological Psychiatry 63, 858–863.CrossRefGoogle ScholarPubMed
Whalen, PJ, Shin, LM, McInerney, SC, Fischer, H, Wright, CI, Rauch, SL (2001). A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion (Washington, DC) 1, 70–83.CrossRefGoogle ScholarPubMed
Wittchen, H-U, Zhao, S, Kessler, RC, Eaton, WW (1994). DSM-III-R generalized anxiety disorder in the National Comorbidity Survey. Archives of General Psychiatry 51, 355–364.CrossRefGoogle ScholarPubMed