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Neural correlates of perception of emotional facial expressions in out-patients with mild-to-moderate depression and anxiety. A multicenter fMRI study

Published online by Cambridge University Press:  06 May 2011

L. R. Demenescu ,
R. Renken ,
R. Kortekaas ,
M.-J. van Tol ,
J. B. C. Marsman ,
M. A. van Buchem ,
N. J. A. van der Wee ,
D. J. Veltman ,
J. A. den Boer  and
A. Aleman
L. R. Demenescu
Affiliation:
Neuroimaging Center, Department of Neuroscience, University Medical Center Groningen, University of Groningen, The Netherlands Department of Psychiatry and Psychotherapy, RWTH Aachen University, Germany
R. Renken
Affiliation:
Neuroimaging Center, Department of Neuroscience, University Medical Center Groningen, University of Groningen, The Netherlands
R. Kortekaas
Affiliation:
Neuroimaging Center, Department of Neuroscience, University Medical Center Groningen, University of Groningen, The Netherlands
M.-J. van Tol
Affiliation:
Department of Psychiatry and Leiden Institute for Brain and Cognition, Leiden University Medical Center, The Netherlands
J. B. C. Marsman
Affiliation:
Laboratory of Experimental Ophthalmology and BCN Neuroimaging Center, University Medical Center Groningen, The Netherlands
M. A. van Buchem
Affiliation:
Department of Radiology and Leiden Institute for Brain and Cognition, Leiden University Medical Center, The Netherlands
N. J. A. van der Wee
Affiliation:
Department of Psychiatry and Leiden Institute for Brain and Cognition, Leiden University Medical Center, The Netherlands
D. J. Veltman
Affiliation:
Department of Psychiatry, VU University Medical Center Amsterdam and Academic Medical Center Amsterdam, The Netherlands
J. A. den Boer
Affiliation:
Department of Psychiatry, University Medical Center Groningen, The Netherlands
A. Aleman*
Affiliation:
Neuroimaging Center, Department of Neuroscience, University Medical Center Groningen, University of Groningen, The Netherlands Department of Psychology, University of Groningen, The Netherlands
*
*Address for correspondence: Prof. Dr. A. Aleman, BCN Neuroimaging Center, University Medical Center Groningen, A. Deusinglaan 2, 9713 AW, Groningen, The Netherlands. (Email: [email protected])
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Abstract

Background

Depression has been associated with limbic hyperactivation and frontal hypoactivation in response to negative facial stimuli. Anxiety disorders have also been associated with increased activation of emotional structures such as the amygdala and insula. This study examined to what extent activation of brain regions involved in perception of emotional faces is specific to depression and anxiety disorders in a large community-based sample of out-patients.

Method

An event-related functional magnetic resonance imaging (fMRI) paradigm was used including angry, fearful, sad, happy and neutral facial expressions. One hundred and eighty-two out-patients (59 depressed, 57 anxiety and 66 co-morbid depression-anxiety) and 56 healthy controls selected from the Netherlands Study of Depression and Anxiety (NESDA) were included in the present study. Whole-brain analyses were conducted. The temporal profile of amygdala activation was also investigated.

Results

Facial expressions activated the amygdala and fusiform gyrus in depressed patients with or without anxiety and in healthy controls, relative to scrambled faces, but this was less evident in patients with anxiety disorders. The response shape of the amygdala did not differ between groups. Depressed patients showed dorsolateral prefrontal cortex (PFC) hyperactivation in response to happy faces compared to healthy controls.

Conclusions

We suggest that stronger frontal activation to happy faces in depressed patients may reflect increased demands on effortful emotion regulation processes triggered by mood-incongruent stimuli. The lack of strong differences in neural activation to negative emotional faces, relative to healthy controls, may be characteristic of the mild-to-moderate severity of illness in this sample and may be indicative of a certain cognitive-emotional processing reserve.

Keywords

Anxiety disorderemotionfacial expressionfMRImajor depression
Type
Original Articles
Information
Psychological Medicine , Volume 41 , Issue 11 , November 2011 , pp. 2253 - 2264
Copyright
Copyright © Cambridge University Press 2011

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References

Almeida, JR, Versace, A, Hassel, S, Kupfer, DJ, Phillips, ML (2009). Elevated amygdala activity to sad facial expressions: a state marker of bipolar but not unipolar depression. Biological Psychiatry 67, 414–421.CrossRefGoogle Scholar
Anand, A, Li, Y, Wang, Y, Wu, J, Gao, S, Bukhari, L, Mathews, VP, Kalnin, A, Lowe, MJ (2005). Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biological Psychiatry 57, 1079–1088.CrossRefGoogle ScholarPubMed
Andrews, G, Peters, L (1998). The psychometric properties of the composite international diagnostic interview. Social Psychiatry and Psychiatric Epidemiology 33, 80–88.CrossRefGoogle ScholarPubMed
APA (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Press: Washington, DC.Google Scholar
Beck, AT, Epstein, N, Brown, G, Steer, RA (1988). An inventory for measuring clinical anxiety: psychometric properties. Journal of Consulting and Clinical Psychology 56, 893–897.CrossRefGoogle ScholarPubMed
Birbaumer, N, Grodd, W, Diedrich, O, Klose, U, Erb, M, Lotze, M, Schneider, F, Weiss, U, Flor, H (1998). fMRI reveals amygdala activation to human faces in social phobics. Neuroreport 9, 1223–1226.CrossRefGoogle ScholarPubMed
Bishop, SJ (2007). Neurocognitive mechanisms of anxiety: an integrative account. Trends in Cognitive Sciences 11, 307–316.CrossRefGoogle ScholarPubMed
Brett, M, Anton, JL, Valabregue, R, Poline, JB (2002). Region of interest analysis using an SPM toolbox. NeuroImage 16, abstract 497 (available on CD-ROM).Google Scholar
Campbell, DW, Sareen, J, Paulus, MP, Goldin, PR, Stein, MB, Reiss, JP (2007). Time-varying amygdala response to emotional faces in generalized social phobia. Biological Psychiatry 62, 455–463.CrossRefGoogle ScholarPubMed
Cooney, RE, Atlas, LY, Joormann, J, Eugne, F, Gotlib, IH (2006). Amygdala activation in the processing of neutral faces in social anxiety disorder: is neutral really neutral? Psychiatry Research 148, 55–59.CrossRefGoogle ScholarPubMed
Davidson, RJ, Irwin, W, Anderle, MJ, Kalin, NH (2003 a). The neural substrates of affective processing in depressed patients treated with venlafaxine. American Journal of Psychiatry 160, 64–75.CrossRefGoogle ScholarPubMed
Davidson, RJ, Pizzagalli, D, Nitschke, JB, Kalin, NH (2003 b). Handbook of Affective Science, pp. 8–24. Oxford University Press: New York.Google Scholar
Diekhof, EK, Falkai, P, Gruber, O (2008). Functional neuroimaging of reward processing and decision-making: a review of aberrant motivational and affective processing in addiction and mood disorders. Brain Research Review 59, 164–184.CrossRefGoogle ScholarPubMed
Elliott, R, Friston, KJ, Dolan, RJ (2000). Dissociable neural responses in human reward systems. Journal of Neuroscience 20, 6159–6165.CrossRefGoogle ScholarPubMed
Elliott, R, Rubinsztein, JS, Sahakian, BJ, Dolan, RJ (2002). The neural basis of mood-congruent processing biases in depression. Archives of General Psychiatry 59, 597–604.CrossRefGoogle ScholarPubMed
Engel, K, Bandelow, B, Gruber, O, Wedekind, D (2009). Neuroimaging in anxiety disorders. Journal of Neural Transmission 116, 703–716.CrossRefGoogle ScholarPubMed
Epstein, J, Pan, H, Kocsis, JH, Yang, Y, Butler, T, Chusid, J, Hochberg, H, Murrough, J, Strohmayer, E, Stern, E, Silbersweig, DA (2006). Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. American Journal of Psychiatry 163, 1784–1790.CrossRefGoogle ScholarPubMed
Etkin, A, Wager, TD (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry 164, 1476–1488.CrossRefGoogle ScholarPubMed
Fales, CL, Barch, DM, Rundle, MM, Mintun, MA, Mathews, J, Snyder, AZ, Sheline, YI (2009). Antidepressant treatment normalizes hypoactivity in dorsolateral prefrontal cortex during emotional interference processing in major depression. Journal of Affective Disorders 112, 206–211.CrossRefGoogle ScholarPubMed
Fales, CL, Barch, DM, Rundle, MM, Mintun, MA, Snyder, AZ, Cohen, JD, Mathews, J, Sheline, YI (2008). Altered emotional interference processing in affective and cognitive-control brain circuitry in major depression. Biological Psychiatry 63, 377–384.CrossRefGoogle ScholarPubMed
Fitzgerald, PB, Laird, AR, Maller, J, Daskalakis, ZJ (2008). A meta-analytic study of changes in brain activation in depression. Human Brain Mapping 29, 736.CrossRefGoogle ScholarPubMed
Friston, KJ, Fletcher, P, Josephs, O, Holmes, A, Rugg, MD, Turner, R (1998). Event-related fMRI: characterizing differential responses. NeuroImage 7, 30–40.CrossRefGoogle ScholarPubMed
Frodl, T, Scheuerecker, J, Albrecht, J, Kleemann, AM, Müller-Schunk, S, Koutsouleris, N, Möller, HJ, Brückmann, H, Wiesmann, M, Meisenzahl, E (2009). Neuronal correlates of emotional processing in patients with major depression. World Journal of Biological Psychiatry 10, 202–208.CrossRefGoogle ScholarPubMed
Fu, CHY, Williams, SCR, Cleare, AJ, Brammer, MJ, Walsh, ND, Kim, J, Andrew, CM, Merlo Pich, E, Williams, PM, Reed, LJ, Mitterschiffthaler, MT, Suckling, J, Bullmore, ET (2004). Attenuation of the neural response to sad faces in major depression by antidepressant treatment: a prospective, event-related functional magnetic resonance imaging study. Archives of General Psychiatry 61, 877–889.CrossRefGoogle ScholarPubMed
Gorno-Tempini, ML, Pradelli, S, Serafini, M, Pagnoni, G, Baraldi, P, Porro, C, Nicoletti, R, Umit, C, Nichelli, P (2001). Explicit and incidental facial expression processing: an fMRI study. NeuroImage 14, 465–473.CrossRefGoogle ScholarPubMed
Gotlib, IH, Sivers, H, Gabrieli, JDE, Whitfield-Gabrieli, S, Goldin, P, Minor, KL, Canli, T (2005). Subgenual anterior cingulate activation to valenced emotional stimuli in major depression. Neuroreport 16, 1731–1734.CrossRefGoogle ScholarPubMed
Haxby, JV, Hoffman, EA, Gobbini, MI (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences 4, 223–233.CrossRefGoogle ScholarPubMed
Hirschfeld, RMA (2001). The comorbidity of major depression and anxiety disorders: recognition and management in primary care Journal of Clinical Psychiatry. Primary Care Companion 3, 244–254.Google Scholar
Lawrence, NS, Williams, AM, Surguladze, S, Giampietro, V, Brammer, MJ, Andrew, C, Frangou, S, Ecker, C, Phillips, ML (2004). Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biological Psychiatry 55, 578–587.CrossRefGoogle ScholarPubMed
Lee, BT, Seok, JH, Lee, BC, Cho, SW, Yoon, BJ, Lee, KU, Chae, JH, Choi, IG, Ham, BJ (2008). Neural correlates of affective processing in response to sad and angry facial stimuli in patients with major depressive disorder. Progress in Neuropsychopharmacology and Biological Psychiatry 32, 778–785.CrossRefGoogle ScholarPubMed
Lundqvist, D, Flykt, A, Ohmann, A (1998). The Karolinska Directed Emotional Faces (KDEF). Karolinska Institute: Stockholm.Google Scholar
Marks, IM, Mathews, AM (1979). Brief standard self-rating for phobic patients. Behaviour Research Therapy 17, 263–267.CrossRefGoogle ScholarPubMed
Mayberg, HS (1997). Limbic-cortical dysregulation: a proposed model of depression. Journal of Neuropsychiatry and Clinical Neurosciences 9, 471–481.Google ScholarPubMed
McRae, K, Reiman, EM, Fort, CL, Chen, K, Lane, RD (2008). Association between trait emotional awareness and dorsal anterior cingulate activity during emotion is arousal-dependent. NeuroImage 41, 648–655.CrossRefGoogle ScholarPubMed
Montgomery, SA, Asberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382–389.CrossRefGoogle ScholarPubMed
Müller, MJ, Szegedi, A, Wetzel, H, Benkert, O (2000). Moderated and severe depression. Gradations for the Montgomery-Asberg Depression Rating Scale. Journal of Affective Disorders 60, 137–140.CrossRefGoogle ScholarPubMed
Norbury, R, Selvaraj, S, Taylor, MJ, Harmer, C, Cowen, PJ (2009). Increased neural response to fear in patients recovered from depression: a 3T functional magnetic resonance imaging study. Psychological Medicine 40, 425–432.CrossRefGoogle ScholarPubMed
Ochsner, KN, Ray, RR, Hughes, B, McRae, K, Cooper, JC, Weber, J, Gabrieli, JD, Gross, JJ (2009). Bottom-up and top-down processes in emotion generation: common and distinct neural mechanisms. Psychological Science 20, 1322–1331.CrossRefGoogle ScholarPubMed
Palmen, SJMC, Durston, S, Nederveen, H, Van Engeland, H (2006). No evidence for preferential involvement of medial temporal lobe structures in high-functioning autism. Psychological Medicine 36, 827–834.CrossRefGoogle ScholarPubMed
Paulus, MP (2008). The role of neuroimaging for the diagnosis and treatment of anxiety disorders. Depression and Anxiety 25, 348–356.CrossRefGoogle ScholarPubMed
Penninx, BWJH, Beekman, ATF, Smit, JH, Zitman, FG, Nolen, WA, Spinhoven, P, Cuijpers, P, De Jong, PJ, Van Marwijk, HWJ, Assendelft, WJJ, Van Der Meer, K, Verhaak, P, Wensing, M, De Graaf, R, Hoogendijk, WJ, Ormel, J, Van Dyck, R; NESDA (2008). The Netherlands Study of Depression and Anxiety (NESDA): rationale, objectives and methods. International Journal of Methods in Psychiatric Research 17, 121–140.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
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biological Psychiatry 54, 515–528.CrossRefGoogle ScholarPubMed
Savitz, JB, Drevets, WC (2009). Imaging phenotypes of major depressive disorder: genetic correlates. Neuroscience 164, 300–330.CrossRefGoogle ScholarPubMed
Sheline, YI, Barch, DM, Donnelly, JM, Ollinger, JM, Snyder, AZ, Mintun, MA (2001). Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biological Psychiatry 50, 651–658.CrossRefGoogle ScholarPubMed
Siegle, GJ, Steinhauer, SR, Thase, ME, Stenger, VA, Carter, CS (2002). Can't shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals. Biological Psychiatry 51, 693–707.CrossRefGoogle ScholarPubMed
Stein, MB, Goldin, PR, Sareen, J, Zorrilla, ELT, Brown, GG (2002). Increased amygdala activation to angry and contemptuous faces in generalized social phobia. Archives of General Psychiatry 59, 1027–1034.CrossRefGoogle ScholarPubMed
Stein, MB, Tancer, ME, Gelernter, CS, Vittone, BJ, Uhde, TW (1990). Major depression in patients with social phobia. American Journal of Psychiatry 147, 637–639.Google ScholarPubMed
Straube, T, Kolassa, IT, Glauer, M, Mentzel, HJ, Miltner, WHR (2004). Effect of task conditions on brain responses to threatening faces in social phobics: an event-related functional magnetic resonance imaging study. Biological Psychiatry 56, 921–930.CrossRefGoogle ScholarPubMed
Straube, T, Mentzel, HJ, Miltner, WHR (2005). Common and distinct brain activation to threat and safety signals in social phobia. Neuropsychobiology 52, 163–168.CrossRefGoogle ScholarPubMed
Surguladze, S, Brammer, MJ, Keedwell, P, Giampietro, V, Young, AW, Travis, MJ, Williams, SCR, Phillips, ML (2005). A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biological Psychiatry 57, 201–209.CrossRefGoogle ScholarPubMed
Wolfensberger, SPA, Veltman, DJ, Hoogendijk, WJG, Boomsma, DI, de Geus, EJC (2008). Amygdala responses to emotional faces in twins discordant or concordant for the risk for anxiety and depression. NeuroImage 41, 544–552.CrossRefGoogle ScholarPubMed
Yoo, HK, Kim, MJ, Kim, SJ, Sung, YH, Sim, ME, Lee, YS, Song, SY, Kee, BS, Lyoo, IK (2005). Putaminal gray matter volume decrease in panic disorder: an optimized voxel-based morphometry study. European Journal of Neuroscience 22, 2089–2094.CrossRefGoogle ScholarPubMed
Zimmerman, M, Posternal, MA, Chelminski, I (2004). Derivation of a definition of remission on the Montgomery-Asberg depression rating scale corresponding to the definition of remission on the Hamilton rating scale for depression. Journal of Psychiatric Research 38, 577–582.CrossRefGoogle Scholar
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