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Neural basis of emotion recognition deficits in first-episode major depression

Published online by Cambridge University Press:  08 November 2010

G. A. van Wingen ,
P. van Eijndhoven ,
I. Tendolkar ,
J. Buitelaar ,
R. J. Verkes  and
G. Fernández
G. A. van Wingen*
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands Department of Psychiatry, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands Department of Neurology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
P. van Eijndhoven
Affiliation:
Department of Psychiatry, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
I. Tendolkar
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands Department of Psychiatry, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
J. Buitelaar
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands Department of Psychiatry, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
R. J. Verkes
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands Department of Psychiatry, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
G. Fernández
Affiliation:
Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands Department for Cognitive Neuroscience, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
*
*Address for correspondence: G. van Wingen, Ph.D., Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University Nijmegen Medical Centre, PO Box 9101, 6500 HB Nijmegen, The Netherlands. (Email: [email protected])
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Abstract

Background

Depressed individuals demonstrate a poorer ability to recognize the emotions of others, which could contribute to difficulties in interpersonal behaviour. This emotion recognition deficit appears related to the depressive state and is particularly pronounced when emotions are labelled semantically. Here, we investigated its neural basis by comparing emotion recognition processing between depressed, recovered and healthy individuals.

Method

Medication-naive patients with a first major depressive episode, medication-free patients who had recovered from a first episode, and a group of matched healthy individuals participated. They were requested to identify the emotion of angry and fearful face stimuli, either by matching them to other emotional faces on a perceptual basis or by matching them to a semantic label, while their brain activity was measured with functional magnetic resonance imaging.

Results

The depressed individuals performed worse than recovered and healthy individuals on the emotion-labelling but not the emotion-matching task. The labelling deficit was related to increased recruitment of the right amygdala, left inferior frontal gyrus and anterior cingulate cortex.

Conclusions

Deficits in semantic labelling of negative emotions are related to increased activation in specific brain regions and these abnormalities are mood state-dependent. These results indicate that accessing semantic knowledge about negative information triggers increased amygdala and left inferior frontal gyrus processing, which subsequently impairs task-relevant behaviour. We propose that this may reflect the activation of negative schemas.

Keywords

AmygdalaemotionfMRIMDDrecognition
Type
Original Articles
Information
Psychological Medicine , Volume 41 , Issue 7 , July 2011 , pp. 1397 - 1405
Copyright
Copyright © Cambridge University Press 2010

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References

Adolphs, R (2002). Neural systems for recognizing emotion. Current Opinion in Neurobiology 12, 169–177.CrossRefGoogle Scholar
Beck, AT, Clark, DA (1988). Anxiety and depression: an information processing perspective. Anxiety, Stress and Coping 1, 23–36.Google Scholar
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561–571.CrossRefGoogle ScholarPubMed
Botvinick, MM, Cohen, JD, Carter, CS (2004). Conflict monitoring and anterior cingulate cortex: an update. Trends in Cognitive Sciences 8, 539–546.CrossRefGoogle Scholar
Bouma, A, Mulder, J, Lindeboom, J (1998). Neuropsychologische Diagnostiek: Handboek [Neuropsychological Assessment: Manual]. Swets & Zeitlinger: Lisse, The Netherlands.Google Scholar
Davidson, RJ, Pizzagalli, D, Nitschke, JB, Putnam, K (2002). Depression: perspectives from affective neuroscience. Annual Review of Psychology 53, 545–574.CrossRefGoogle ScholarPubMed
Feinberg, TE, Rifkin, A, Schaffer, C, Walker, E (1986). Facial discrimination and emotional recognition in schizophrenia and affective disorders. Archives of General Psychiatry 43, 276–279.CrossRefGoogle Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1996). Structured Clinical Interview for DSM-IV Axis-I Disorders, Clinician Version (SCID-CV). American Psychiatric Press: Washington, DC.Google Scholar
Frank, E, Prien, RF, Jarrett, RB, Keller, MB, Kupfer, DJ, Lavori, PW, Rush, AJ, Weissman, MM (1991). Conceptualization and rationale for consensus definitions of terms in major depressive disorder: remission, recovery, relapse, and recurrence. Archives of General Psychiatry 48, 851–855.CrossRefGoogle Scholar
Friston, KJ, Worsley, KJ, Frackowiak, RSJ, Mazziotta, JC, Evans, AC (1994). Assessing the significance of focal activations using their spatial extent. Human Brain Mapping 1, 210–220.CrossRefGoogle Scholar
Fu, CH, Williams, SC, Cleare, AJ, Brammer, MJ, Walsh, ND, Kim, J, Andrew, CM, Pich, EM, 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 Scholar
Gur, RC, Erwin, RJ, Gur, RE, Zwil, AS, Heimberg, C, Kraemer, HC (1992). Facial emotion discrimination: II. Behavioral findings in depression. Psychiatry Research 42, 241–251.CrossRefGoogle Scholar
Hagoort, P (2005). On Broca, brain, and binding: a new framework. Trends in Cognitive Sciences 9, 416–423.CrossRefGoogle Scholar
Hariri, AR, Bookheimer, SY, Mazziotta, JC (2000). Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport 11, 43–48.CrossRefGoogle ScholarPubMed
Heaton, RK, Chelune, RK, Talley, JL, Kay, GG, Curtiss, G (1993). Wisconsin Card Sorting Test Manual: Revised and Expanded. Psychological Assessment Resources: Odessa, FL.Google Scholar
Hinchliffe, MK, Lancashire, M, Roberts, FJ (1971). Study of eye-contact changes in depressed and recovered psychiatric patients. British Journal of Psychiatry 119, 213–215.CrossRefGoogle Scholar
Ingram, RE (1984). Toward an information-processing analysis of depression. Cognitive Therapy and Research 8, 443–477.CrossRefGoogle Scholar
Lauer, CJ, Bronisch, T, Kainz, M, Schreiber, W, Holsboer, F, Krieg, JC (1997). Pre-morbid psychometric profile of subjects at high familial risk for affective disorder. Psychological Medicine 27, 355–362.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 Neuro-Psychopharmacology and Biological Psychiatry 32, 778–785.CrossRefGoogle Scholar
Lezak, MD (1995). Neuropsychological Assessment, 3rd edn. Oxford University Press: New York.Google Scholar
Libet, JM, Lewinsohn, PM (1973). Concept of social skill with special reference to behavior of depressed persons. Journal of Consulting and Clinical Psychology 40, 304–312.CrossRefGoogle Scholar
MacQueen, GM, Campbell, S, McEwen, BS, Macdonald, K, Amano, S, Joffe, RT, Nahmias, C, Young, LT (2003). Course of illness, hippocampal function, and hippocampal volume in major depression. Proceedings of the National Academy of Sciences USA 100, 1387–1392.CrossRefGoogle Scholar
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 1233–1239.CrossRefGoogle Scholar
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
Mikhailova, ES, Vladimirova, TV, Iznak, AF, Tsusulkovskaya, EJ, Sushko, NV (1996). Abnormal recognition of facial expression of emotions in depressed patients with major depression disorder and schizotypal personality disorder. Biological Psychiatry 40, 697–705.CrossRefGoogle ScholarPubMed
Murphy, SE, Norbury, R, O'Sullivan, U, Cowen, PJ, Harmer, CJ (2009). Effect of a single dose of citalopram on amygdala response to emotional faces. British Journal of Psychiatry 194, 535–540.CrossRefGoogle ScholarPubMed
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113.CrossRefGoogle Scholar
Ormel, J, Oldehinkel, AJ, Vollebergh, W (2004). Vulnerability before, during, and after a major depressive episode: a 3-wave population-based study. Archives of General Psychiatry 61, 990–996.CrossRefGoogle Scholar
Osterrieth, PA (1944). Test of copying a complex figure: contribution to the study of perception and memory [in French]. Archives de Psychologie 30, 306–356.Google Scholar
Peluso, MA, Glahn, DC, Matsuo, K, Monkul, ES, Najt, P, Zamarripa, F, Li, J, Lancaster, JL, Fox, PT, Gao, JH, Soares, JC (2009). Amygdala hyperactivation in untreated depressed individuals. Psychiatry Research: Neuroimaging 173, 158–161.CrossRefGoogle ScholarPubMed
Persad, SM, Polivy, J (1993). Differences between depressed and nondepressed individuals in the recognition of and response to facial emotional cues. Journal of Abnormal Psychology 102, 358–368.CrossRefGoogle Scholar
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 Scholar
Ray, RD, Ochsner, KN, Cooper, JC, Robertson, ER, Gabrieli, JDE, Gross, JJ (2005). Individual differences in trait rumination and the neural systems supporting cognitive reappraisal. Cognitive, Affective, and Behavioral Neuroscience 5, 156–168.CrossRefGoogle ScholarPubMed
Rubinow, DR, Post, RM (1992). Impaired recognition of affect in facial expression in depressed patients. Biological Psychiatry 31, 947–953.CrossRefGoogle Scholar
Saan, RJ, Deelman, BG (1986). De 15-Woorden Tests A en B: Een Voorlopige Handleiding [The 15-Word Tests A and B: A Provisional Manual]. University Medical Center Groningen, Department of Neuropsychology: Groningen.Google Scholar
Schmand, B, Lindeboom, J, van Harskamp, F (1992). Nederlandse Leestest voor Volwassenen: handleiding [Dutch Adult Reading Test: Manual]. Swets & Zeitlinger: Lisse, The Netherlands.Google Scholar
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R, Dunbar, GC (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59, 22–33.Google Scholar
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 Scholar
Smith, A (1982). Symbol Digit Modalities Test (SDMT): Manual (revised). Western Psychological Services: Los Angeles.Google Scholar
Spielberger, CD, Gorsuch, RL, Lushene, RE (1970). STAI Manual for the State Trait Anxiety Inventory. Consulting Psychologists Press: Palo Alto.Google Scholar
Surguladze, S, Brammer, MJ, Keedwell, P, Giampietro, V, Young, AW, Travis, MJ, Williams, SC, 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 Scholar
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273–289.CrossRefGoogle ScholarPubMed
van Wingen, GA, Van Eijndhoven, P, Cremers, HR, Tendolkar, I, Verkes, RJ, Buitelaar, JK, Fernández, G (2010). Neural state and trait bases of mood-incongruent memory formation and retrieval in first-episode major depression. Journal of Psychiatric Research 44, 527–534.CrossRefGoogle Scholar
Willems, RM, Ozyurek, A, Hagoort, P (2007). When language meets action: the neural integration of gesture and speech. Cerebral Cortex 17, 2322–2333.CrossRefGoogle Scholar
Worsley, KJ, Marrett, S, Neelin, P, Vandal, AC, Friston, KJ, Evans, AC (1996). A unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapping 4, 58–73.3.0.CO;2-O>CrossRefGoogle Scholar
Youngren, MA, Lewinsohn, PM (1980). The functional relation between depression and problematic interpersonal-behavior. Journal of Abnormal Psychology 89, 333–341.CrossRefGoogle ScholarPubMed