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Neural basis of the emotional Stroop interference effect in major depression

Published online by Cambridge University Press:  10 September 2007

M. T. Mitterschiffthaler*
Affiliation:
Institute of Psychiatry, King's College London, UK
S. C. R. Williams
Affiliation:
Institute of Psychiatry, King's College London, UK
N. D. Walsh
Affiliation:
University of Pittsburgh, School of Medicine, Department of Psychiatry, Pittsburgh, PA, USA
A. J. Cleare
Affiliation:
Institute of Psychiatry, King's College London, UK
C. Donaldson
Affiliation:
Institute of Psychiatry, King's College London, UK
J. Scott
Affiliation:
Institute of Psychiatry, King's College London, UK University Department of Psychiatry, Royal Victoria Infirmary, Newcastle upon Tyne, UK
C. H. Y. Fu
Affiliation:
Institute of Psychiatry, King's College London, UK
*
*Address for correspondence: M. Mitterschiffthaler, Ph.D., Neuroimaging Research Group, Clinical Neuroscience, PO Box 89; Institute of Psychiatry, De Crespigny Park, LondonSE5 8AF, UK. (Email: [email protected])

Abstract

Background

A mood-congruent sensitivity towards negative stimuli has been associated with development and maintenance of major depressive disorder (MDD). The emotional Stroop task assesses interference effects arising from the conflict of emotional expressions consistent with disorder-specific self-schemata and cognitive colour-naming instructions. Functional neuroimaging studies of the emotional Stroop effect advocate a critical involvement of the anterior cingulate cortex (ACC) during these processes.

Method

Subjects were 17 medication-free individuals with unipolar MDD in an acute depressive episode (mean age 39 years), and 17 age-, gender- and IQ-matched healthy volunteers. In an emotional Stroop task, sad and neutral words were presented in various colours, and subjects were required to name the colour of words whilst undergoing functional magnetic resonance imaging (fMRI). Overt verbal responses were acquired with a clustered fMRI acquisition sequence.

Results

Individuals with depression showed greater increases in response time from neutral to sad words relative to controls. fMRI data showed a significant engagement of left rostral ACC (BA 32) and right precuneus during sad words in patients relative to controls. Additionally, rostral ACC activation was positively correlated with latencies of negative words in MDD patients. Healthy controls did not have any regions of increased activation compared to MDD patients.

Conclusions

These findings provide evidence for a behavioural and neural emotional Stroop effect in MDD and highlight the importance of the ACC during monitoring of conflicting cognitive processes and mood-congruent processing in depression.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2007

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References

Banich, MT, Milham, MP, Atchley, R, Cohen, NJ, Webb, A, Wszalek, T, Kramer, AF, Liang, ZP, Wright, A, Shenker, J, Magin, R (2000). fMRI studies of Stroop tasks reveal unique roles of anterior and posterior brain systems in attentional selection. Journal of Cognitive Neuroscience 12, 9881000.CrossRefGoogle ScholarPubMed
Banich, MT, Milham, MP, Jacobson, BL, Webb, A, Wszalek, T, Cohen, NJ, Kramer, AF (2001). Attentional selection and the processing of task-irrelevant information: insights from fMRI examinations of the Stroop task. Progress in Brain Research 134, 459470.CrossRefGoogle ScholarPubMed
Beck, AT, Rush, AJ, Shaw, BF, Emery, Y (1979). Cognitive Therapy of Depression. Guilford Press: New York.Google Scholar
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561571.CrossRefGoogle ScholarPubMed
Bench, CJ, Frith, CD, Grasby, PM, Friston, KJ, Paulesu, E, Frackowiak, RS, Dolan, RJ (1993). Investigations of the functional anatomy of attention using the Stroop test. Neuropsychologia 31, 907922.CrossRefGoogle ScholarPubMed
Botvinick, M, Nystrom, LE, Fissell, K, Carter, CS, Cohen, JD (1999). Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402, 179181.CrossRefGoogle ScholarPubMed
Bower, GH (1981). Mood and memory. American Psychologist 36, 129148.CrossRefGoogle ScholarPubMed
Bradley, BP, Mogg, K, Millar, N (1996). Implicit memory bias in clinical and non-clinical depression. Behaviour Research and Therapy 34, 865879.CrossRefGoogle ScholarPubMed
Bradley, MM, Lang, PJ (1999). Affective Norms for English Words (ANEW). The NIMH Center for the Study of Emotion and Attention, University of Florida: Gainesville, FL.Google Scholar
Bush, G, Whalen, PJ, Rosen, BR, Jenike, MA, McInerney, SC, Rauch, SL (1998). The counting Stroop: an interference task specialized for functional neuroimaging – validation study with functional MRI. Human Brain Mapping 6, 270282.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Cabeza, R, Nyberg, L (2000). Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience 12, 147.CrossRefGoogle Scholar
Caligiuri, MP, Ellwanger, J (2000). Motor and cognitive aspects of motor retardation in depression. Journal of Affective Disorders 57, 8393.CrossRefGoogle ScholarPubMed
Carter, CS, Macdonald, AM, Botvinick, M, Ross, LL, Stenger, VA, Noll, D, Cohen, JD (2000). Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. Proceedings of the National Academy of Sciences USA 97, 19441948.CrossRefGoogle ScholarPubMed
Carter, CS, Mintun, M, Cohen, JD (1995). Interference and facilitation effects during selective attention: an H215O PET study of Stroop task performance. NeuroImage 2, 264272.CrossRefGoogle ScholarPubMed
Clark, DM, Teasdale, JD (1982). Diurnal variation in clinical depression and accessibility of memories of positive and negative experiences. Journal of Abnormal Psychology 91, 8795.CrossRefGoogle ScholarPubMed
Critchley, HD, Wiens, S, Rotshtein, P, Ohman, A, Dolan, RJ (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience 7, 189195.CrossRefGoogle ScholarPubMed
Dudley, R, O'Brien, J, Barnett, N, McGuckin, L, Britton, P (2002). Distinguishing depression from dementia in later life: a pilot study employing the Emotional Stroop task. International Journal of Geriatric Psychiatry 17, 4853.CrossRefGoogle ScholarPubMed
Elliott, R, Dolan, RJ (1998). Activation of different anterior cingulate foci in association with hypothesis testing and response selection. NeuroImage 8, 1729.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, 597604.CrossRefGoogle ScholarPubMed
Ellis, HC, Ashbrook, PW (1988). Resource allocation model of the effects of depressed mood states on memory. In Affect, Cognition and Social Behaviour (ed. Fiedler, K. and Forgas, J. P.), pp. 2543. Hogrefe: Goettingen.Google Scholar
Erickson, K, Drevets, WC, Clark, L, Cannon, DM, Bain, EE, Zarate, CA Jr., Charney, DS, Sahakian, BJ (2005). Mood-congruent bias in affective go/no-go performance of unmedicated patients with major depressive disorder. American Journal of Psychiatry 162, 21712173.CrossRefGoogle ScholarPubMed
Etkin, A, Egner, T, Peraza, DM, Kandel, ER, Hirsch, J (2006). resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 51, 871882.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1997). Structured Clinical Interview for DSM-IV Axis I Disorders, Patient Edition (SCID-P). Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Francis, WN, Kucera, H (1982). Frequency Analysis of English Usage. Houghton Mifflin: Boston, MA.Google Scholar
Fu, CH, Vythelingum, GN, Brammer, MJ, Williams, SC, Amaro, E Jr., Andrew, CM, Yaguez, L, van Haren, NE, Matsumoto, K, McGuire, PK (2006). An fMRI study of verbal self-monitoring: neural correlates of auditory verbal feedback. Cerebral Cortex 16, 969977.CrossRefGoogle ScholarPubMed
George, MS, Ketter, TA, Parekh, PI, Rosinsky, N, Ring, HA, Casey, BJ (1994). Regional brain activity when selecting a response despite interference: An H215O PET study of the Stroop and the emotional Stroop. Human Brain Mapping 1, 194209.CrossRefGoogle Scholar
George, MS, Ketter, TA, Parekh, PI, Rosinsky, N, Ring, HA, Pazzaglia, PJ, Marangell, LB, Callahan, AM, Post, RM (1997). Blunted left cingulate activation in mood disorder subjects during a response interference task (the Stroop). Journal of Neuropsychiatry and Clinical Neuroscience 9, 5563.Google ScholarPubMed
Goldman-Rakic, PS (1988). Topography of cognition: parallel distributed networks in primate association cortex. Annual Review of Neuroscience 11, 137156.CrossRefGoogle ScholarPubMed
Gotlib, IH, Cane, DB (1987). Construct accessibility and clinical depression: a longitudinal investigation. Journal of Abnormal Psychology 96, 199204.CrossRefGoogle ScholarPubMed
Gotlib, IH, McCann, CD (1984). Construct accessibility and depression: an examination of cognitive and affective factors. Journal of Personality and Social Psychology 47, 427439.CrossRefGoogle ScholarPubMed
Gruber, SA, Rogowska, J, Holcomb, P, Soraci, S, Yurgelun-Todd, D (2002). Stroop performance in normal control subjects: an fMRI study. NeuroImage 16, 349360.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 5662.CrossRefGoogle ScholarPubMed
John, CH (1988). Emotionality ratings and free-association norms of 240 emotional and non-emotional words. Cognition & Emotion 2, 4970.CrossRefGoogle Scholar
Kerns, JG, Cohen, JD, MacDonald, III AW, Cho, RY, Stenger, VA, Carter, CS (2004). Anterior cingulate conflict monitoring and adjustments in control. Science 303, 10231026.CrossRefGoogle ScholarPubMed
Kerr, N, Scott, J, Phillips, ML (2005). Patterns of attentional deficits and emotional bias in bipolar and major depressive disorder. British Journal of Clinical Psychology 44, 343356.CrossRefGoogle ScholarPubMed
Koster, EH, De, RR, Goeleven, E, Franck, E, Crombez, G (2005). Mood-congruent attentional bias in dysphoria: maintained attention to and impaired disengagement from negative information. Emotion 5, 446455.CrossRefGoogle ScholarPubMed
Krause, BJ, Schmidt, D, Mottaghy, FM, Taylor, J, Halsband, U, Herzog, H, Tellmann, L, Muller-Gartner, HW (1999). Episodic retrieval activates the precuneus irrespective of the imagery content of word pair associates. A PET study. Brain 122, 255263.CrossRefGoogle ScholarPubMed
LaBar, KS, Gitelman, DR, Parrish, TB, Mesulam, M (1999). Neuroanatomic overlap of working memory and spatial attention networks: a functional MRI comparison within subjects. NeuroImage 10, 695704.CrossRefGoogle ScholarPubMed
Langenecker, SA, Nielson, KA, Rao, SM (2004). fMRI of healthy older adults during Stroop interference. NeuroImage 21, 192200.CrossRefGoogle ScholarPubMed
Lloyd, GG, Lishman, WA (1975). Effect of depression on the speed of recall of pleasant and unpleasant experiences. Psychological Medicine 5, 173180.CrossRefGoogle ScholarPubMed
MacLeod, CM (1991). Half a century of research on the Stroop effect: an integrative review. Psychololgical Bulletin 109, 163203.CrossRefGoogle ScholarPubMed
Malhi, GS, Lagopoulos, J, Sachdev, PS, Ivanovski, B, Shnier, R (2005). An emotional Stroop functional MRI study of euthymic bipolar disorder. Bipolar Disorder 7 (Suppl. 5), 5869.CrossRefGoogle ScholarPubMed
Mayberg, HS (1997). Limbic-cortical dysregulation: a proposed model of depression. Journal of Neuropsychiatry and Clinical Neuroscience 9, 471481.Google ScholarPubMed
Mead, LA, Mayer, AR, Bobholz, JA, Woodley, SJ, Cunningham, JM, Hammeke, TA, Rao, SM (2002). Neural basis of the Stroop interference task: response competition or selective attention? Journal of the International Neuropsychological Society 8, 735742.CrossRefGoogle ScholarPubMed
Murphy, FC, Sahakian, BJ, Rubinsztein, JS, Michael, A, Rogers, RD, Robbins, TW, Paykel, ES (1999). Emotional bias and inhibitory control processes in mania and depression. Psychological Medicine 29, 13071321.CrossRefGoogle ScholarPubMed
Neshat-Doost, HT, Taghavi, MR, Moradi, AR, Yule, W, Dalgleish, T (1998). Memory for emotional trait adjectives in clinically depressed youth. Journal of Abnormal Psychology 107, 642650.CrossRefGoogle ScholarPubMed
Nyberg, L, Persson, J, Habib, R, Tulving, E, McIntosh, AR, Cabeza, R, Houle, S (2000). Large scale neurocognitive networks underlying episodic memory. Journal of Cognitive Neuroscience 12, 163173.CrossRefGoogle ScholarPubMed
Pardo, JV, Pardo, PJ, Janer, KW, Raichle, ME (1990). The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. Proceedings of the National Academy of Sciences USA 87, 256259.CrossRefGoogle ScholarPubMed
Paus, T (2001). Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nature Review Neuroscience 2, 417424.CrossRefGoogle ScholarPubMed
Peterson, BS, Skudlarski, P, Gatenby, JC, Zhang, H, Anderson, AW, Gore, JC (1999). An fMRI study of Stroop word-color interference: evidence for cingulate subregions subserving multiple distributed attentional systems. Biological Psychiatry 45, 12371258.CrossRefGoogle ScholarPubMed
Pinel, P, Dehaene, S, Riviere, D, LeBihan, D (2001). Modulation of parietal activation by semantic distance in a number comparison task. NeuroImage 14, 10131026.CrossRefGoogle Scholar
Posner, MI (1980). Attention and Consciousness. Lawrence Erlbaum Associates: Mahwah, NJ.Google Scholar
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, 111.CrossRefGoogle ScholarPubMed
Segal, ZV, Gemar, M, Truchon, C, Guirguis, M, Horowitz, LM (1995). A priming methodology for studying self-representation in major depressive disorder. Journal of Abnormal Psychology 104, 205213.CrossRefGoogle ScholarPubMed
Talairach, J, Tournoux, P (1988). Co-planar Sterotaxic Atlas of the Human Brain. Thieme Medical Publishers Inc.: New York.Google Scholar
Taylor, JL, John, CH (2004). Attentional and memory bias in persecutory delusions and depression. Psychopathology 37, 233241.CrossRefGoogle ScholarPubMed
Taylor, SF, Kornblum, S, Lauber, EJ, Minoshima, S, Koeppe, RA (1997). Isolation of specific interference processing in the Stroop task: PET activation studies. NeuroImage 6, 8192.CrossRefGoogle ScholarPubMed
Taylor, SF, Kornblum, S, Minoshima, S, Oliver, LM, Koeppe, RA (1994). Changes in medial cortical blood flow with a stimulus-response compatibility task. Neuropsychologia 32, 249255.CrossRefGoogle ScholarPubMed
Teasdale, JD, Fogarty, SJ (1979). Differential effects of induced mood on retrieval of pleasant and unpleasant events from episodic memory. Journal of Abnormal Psychology 88, 248257.CrossRefGoogle ScholarPubMed
Teasdale, JD, Russell, ML (1983). Differential effects of induced mood on the recall of positive, negative and neutral words. British Journal of Clinical Psychology 22, 163171.CrossRefGoogle ScholarPubMed
Tsourtos, G, Thompson, JC, Stough, C (2002). Evidence of an early information processing speed deficit in unipolar major depression. Psychological Medicine 32, 259265.CrossRefGoogle ScholarPubMed
van den Heuvel, OA, Veltman, DJ, Groenewegen, HJ, Witter, MP, Merkelbach, J, Cath, DC, van Balkom, AJ, van Oppen, P, van Dyck, R (2005). Disorder-specific neuroanatomical correlates of attentional bias in obsessive-compulsive disorder, panic disorder, and hypochondriasis. Archives of General Psychiatry 62, 922933.CrossRefGoogle ScholarPubMed
Wagner, G, Sinsel, E, Sobanski, T, Kohler, S, Marinou, V, Mentzel, HJ, Sauer, H, Schlosser, RGM (2006). Cortical inefficiency in patients with unipolar depression: an event-related fMRI study with the Stroop task. Biological Psychiatry 59 958965.CrossRefGoogle ScholarPubMed
Watkins, PC, Vache, K, Verney, SP, Muller, S, Mathews, A (1996). Unconscious mood-congruent memory bias in depression. Journal of Abnormal Psychology 105, 3441.CrossRefGoogle ScholarPubMed
Wechsler, D (1999). Wechsler Abbreviated Scale of Intelligence (WASI). Psychological Corporation Harcourt Brace & Co.: San Antonio, TX.Google Scholar
Whalen, PJ, Bush, G, McNally, RJ, Wilhelm, S, McInerney, SC, Jenike, MA, Rauch, SL (1998). The emotional counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division. Biological Psychiatry 44, 12191228.CrossRefGoogle ScholarPubMed
Williams, JM, Broadbent, K (1986). Distraction by emotional stimuli: use of a Stroop task with suicide attempters. British Journal of Clinical Psychology 25, 101110.CrossRefGoogle ScholarPubMed