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Abnormal prefrontal activity subserving attentional control of emotion in remitted depressed patients during a working memory task with emotional distracters

Published online by Cambridge University Press:  07 July 2011

R. Kerestes ,
C. D. Ladouceur ,
S. Meda ,
P. J. Nathan ,
H. P. Blumberg ,
K. Maloney ,
B. Ruf ,
A. Saricicek ,
G. D. Pearlson  and
Z. Bhagwagar
...Show all authors
R. Kerestes*
Affiliation:
Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA School of Psychology and Psychiatry, Monash University Clayton Campus, Melbourne, Australia
C. D. Ladouceur
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
S. Meda
Affiliation:
Olin Neuropsychiatry Research Center, Hartford, CT, USA
P. J. Nathan
Affiliation:
School of Psychology and Psychiatry, Monash University Clayton Campus, Melbourne, Australia Brain Mapping Unit, Department of Psychiatry, University of Cambridge, UK
H. P. Blumberg
Affiliation:
Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA
K. Maloney
Affiliation:
Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA
B. Ruf
Affiliation:
Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA
A. Saricicek
Affiliation:
Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA
G. D. Pearlson
Affiliation:
Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA Olin Neuropsychiatry Research Center, Hartford, CT, USA
Z. Bhagwagar
Affiliation:
Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA Bristol Myers Squibb, Wallingford, CT, USA
M. L. Phillips
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA Department of Psychological Medicine, Cardiff University School of Medicine, Cardiff, UK
*
*Address for correspondence: Miss R. Kerestes, School of Psychology and Psychiatry, Monash University Clayton Campus, Wellington Road, Clayton, Melbourne Victoria, Australia. (Email:Rebecca.Kerestes@monash.edu)
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Abstract

Background

Patients with major depressive disorder (MDD) show deficits in processing of facial emotions that persist beyond recovery and cessation of treatment. Abnormalities in neural areas supporting attentional control and emotion processing in remitted depressed (rMDD) patients suggests that there may be enduring, trait-like abnormalities in key neural circuits at the interface of cognition and emotion, but this issue has not been studied systematically.

Method

Nineteen euthymic, medication-free rMDD patients (mean age 33.6 years; mean duration of illness 34 months) and 20 age- and gender-matched healthy controls (HC; mean age 35.8 years) performed the Emotional Face N-Back (EFNBACK) task, a working memory task with emotional distracter stimuli. We used blood oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI) to measure neural activity in the dorsolateral (DLPFC) and ventrolateral prefrontal cortex (VLPFC), orbitofrontal cortex (OFC), ventral striatum and amygdala, using a region of interest (ROI) approach in SPM2.

Results

rMDD patients exhibited significantly greater activity relative to HC in the left DLPFC [Brodmann area (BA) 9/46] in response to negative emotional distracters during high working memory load. By contrast, rMDD patients exhibited significantly lower activity in the right DLPFC and left VLPFC compared to HC in response to positive emotional distracters during high working memory load. These effects occurred during accurate task performance.

Conclusions

Remitted depressed patients may continue to exhibit attentional biases toward negative emotional information, reflected by greater recruitment of prefrontal regions implicated in attentional control in the context of negative emotional information.

Keywords

Depressionemotional processingfunctional magnetic resonance imagingprefrontal cortexworking memory
Type
Original Articles
Information
Psychological Medicine , Volume 42 , Issue 1 , January 2012 , pp. 29 - 40
Copyright
Copyright © Cambridge University Press 2011

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References

Almeida, JR, Versace, A, Hassel, S, Kupfer, DJ, Phillips, ML (2010). Elevated amygdala activity to sad facial expressions: a state marker of bipolar but not unipolar depression. Biological Psychiatry 67, 414–421.CrossRefGoogle Scholar
Almeida, JR, Versace, A, Mechelli, A, Hassel, S, Quevedo, K, Kupfer, DJ, Phillips, ML (2009). Abnormal amygdala-prefrontal effective connectivity to happy faces differentiates bipolar from major depression. Biological Psychiatry 66, 451–459.CrossRefGoogle ScholarPubMed
Anticevic, A, Repovs, G, Barch, DM (2010). Resisting emotional interference: brain regions facilitating working memory performance during negative distraction. Cognitive, Affective and Behavioral Neuroscience 10, 159–173.CrossRefGoogle ScholarPubMed
Barch, DM, Sheline, YI, Csernansky, JG, Snyder, AZ (2003). Working memory and prefrontal cortex dysfunction: specificity to schizophrenia compared with major depression. Biological Psychiatry 53, 376–384.CrossRefGoogle ScholarPubMed
Becerril, K, Barch, D (2010). Influence of emotional processing on working memory in schizophrenia. Schizophrenia Bulletin. Published online: 22 February 2010. doi:10.1093/schbul/sbq009.Google ScholarPubMed
Bhagwagar, Z, Cowen, PJ, Goodwin, GM, Harmer, CJ (2004). Normalization of enhanced fear recognition by acute SSRI treatment in subjects with a previous history of depression. American Journal of Psychiatry 161, 166–168.CrossRefGoogle ScholarPubMed
Blair, KS, Smith, BW, Mitchell, DG, Morton, J, Vythilingam, M, Pessoa, L, Fridberg, D, Zametkin, A, Sturman, D, Nelson, EE, Drevets, WC, Pine, DS, Martin, A, Blair, RJ (2007). Modulation of emotion by cognition and cognition by emotion. NeuroImage 35, 430–440.CrossRefGoogle ScholarPubMed
Carvajal-Rodriguez, A, de Una-Alvarez, J, Rolan-Alvarez, E (2009). A new multitest correction (SGoF) that increases its statistical power when increasing the number of tests. BMC Bioinformatics 10, 209.CrossRefGoogle ScholarPubMed
Clark, L, Sarna, A, Goodwin, GM (2005). Impairment of executive function but not memory in first-degree relatives of patients with bipolar I disorder and in euthymic patients with unipolar depression. American Journal of Psychiatry 162, 1980–1982.CrossRefGoogle Scholar
Cohen, JD, Forman, SD, Braver, TS, Casey, BJ (1994). Activation of the prefrontal cortex in a non-spatial working memory task with functional MRI. Human Brain Mapping 1, 293–304.CrossRefGoogle Scholar
Cremers, HR, Demenescu, LR, Aleman, A, Renken, R, van Tol, MJ, van der Wee, NJ, Veltman, DJ, Roelofs, K (2009). Neuroticism modulates amygdala-prefrontal connectivity in response to negative emotional facial expressions. NeuroImage 49, 963–970.CrossRefGoogle ScholarPubMed
Davidson, RJ (1992). Anterior cerebral asymmetry and the nature of emotion. Brain and Cognition 20, 125–151.CrossRefGoogle ScholarPubMed
Dolcos, F, Kragel, P, Wang, L, McCarthy, G (2006). Role of the inferior frontal cortex in coping with distracting emotions. Neuroreport 17, 1591–1594.CrossRefGoogle ScholarPubMed
Dolcos, F, McCarthy, G (2006). Brain systems mediating cognitive interference by emotional distraction. Journal of Neuroscience 26, 2072–2079.CrossRefGoogle ScholarPubMed
Drevets, WC, Videen, TO, Price, JL, Preskorn, SH, Carmichael, ST, Raichle, ME (1992). A functional anatomical study of unipolar depression. Journal of Neuroscience 12, 3628–3641.CrossRefGoogle ScholarPubMed
Elliott, R, Baker, SC, Rogers, RD, O'Leary, DA, Paykel, ES, Frith, CD, Dolan, RJ, Sahakian, BJ (1997). Prefrontal dysfunction in depressed patients performing a complex planning task: a study using positron emission tomography. Psychological Medicine 27, 931–942.CrossRefGoogle ScholarPubMed
Elliott, R, Zahn, R, Deakin, JF, Anderson, IM (2010). Affective cognition and its disruption in mood disorders. Neuropsychopharmacology 36, 153–182.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
Erk, S, Kleczar, A, Walter, H (2007). Valence-specific regulation effects in a working memory task with emotional context. NeuroImage 37, 623–632.CrossRefGoogle Scholar
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
Fedoroff, JP, Starkstein, SE, Forrester, AW, Geisler, FH, Jorge, RE, Arndt, SV, Robinson, RG (1992). Depression in patients with acute traumatic brain injury. American Journal of Psychiatry 149, 918–923.Google ScholarPubMed
First, MB (2002). The DSM series and experience with DSM-IV. Psychopathology 35, 67–71.CrossRefGoogle ScholarPubMed
Fitzgerald, PB, Srithiran, A, Benitez, J, Daskalakis, ZZ, Oxley, TJ, Kulkarni, J, Egan, GF (2008). An fMRI study of prefrontal brain activation during multiple tasks in patients with major depressive disorder. Human Brain Mapping 29, 490–501.CrossRefGoogle ScholarPubMed
Forman, SD, Cohen, JD, Fitzgerald, M, Eddy, WF, Mintun, MA, Noll, DC (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magnetic Resonance in Medicine 33, 636–647.CrossRefGoogle ScholarPubMed
Freire, L, Roche, A, Mangin, JF (2002). What is the best similarity measure for motion correction in fMRI time series? IEEE Transactions on Medical Imaging 21, 470–484.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Gilboa-Schechtman, E, Ben-Artzi, E, Jeczemien, P, Marom, S, Hermesh, H (2004). Depression impairs the ability to ignore the emotional aspects of facial expressions: evidence from the Garner task. Cognition and Emotion 18, 209–231.CrossRefGoogle ScholarPubMed
Gotlib, IH, Krasnoperova, E, Yue, DN, Joormann, J (2004). Attentional biases for negative interpersonal stimuli in clinical depression. Journal of Abnormal Psychology 113, 121–135.CrossRefGoogle ScholarPubMed
Grober, E, Sliwinski, M (1991). Development and validation of a model for estimating premorbid verbal intelligence in the elderly. Journal of Clinical and Experimental Neuropsychology 13, 933–949.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 ScholarPubMed
Gur, RC, Skolnick, BE, Gur, RE (1994). Effects of emotional discrimination tasks on cerebral blood flow: regional activation and its relation to performance. Brain and Cognition 25, 271–286.CrossRefGoogle ScholarPubMed
Hale, WW 3rd (1998). Judgment of facial expressions and depression persistence. Psychiatry Research 80, 265–274.CrossRefGoogle ScholarPubMed
Harvey, PO, Fossati, P, Pochon, JB, Levy, R, Lebastard, G, Lehericy, S, Allilaire, JF, Dubois, B (2005). Cognitive control and brain resources in major depression: an fMRI study using the n-back task. NeuroImage 26, 860–869.CrossRefGoogle ScholarPubMed
Hugdahl, K, Rund, BR, Lund, A, Asbjornsen, A, Egeland, J, Ersland, L, Landro, NI, Roness, A, Stordal, KI, Sundet, K, Thomsen, T (2004). Brain activation measured with fMRI during a mental arithmetic task in schizophrenia and major depression. American Journal of Psychiatry 161, 286–293.CrossRefGoogle ScholarPubMed
Johnstone, T, van Reekum, CM, Urry, HL, Kalin, NH, Davidson, RJ (2007). Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. Journal of Neuroscience 27, 8877–8884.CrossRefGoogle ScholarPubMed
Joormann, J, Gotlib, IH (2007). Selective attention to emotional faces following recovery from depression. Journal of Abnormal Psychology 116, 80–85.CrossRefGoogle ScholarPubMed
Jorge, RE, Robinson, RG, Arndt, SV, Starkstein, SE, Forrester, AW, Geisler, F (1993). Depression following traumatic brain injury: a 1 year longitudinal study. Journal of Affective Disorders 27, 233–243.CrossRefGoogle ScholarPubMed
Kaiser, S, Unger, J, Kiefer, M, Markela, J, Mundt, C, Weisbrod, M (2003). Executive control deficit in depression: event-related potentials in a Go/Nogo task. Psychiatry Research: Neuroimaging 122, 169–184.CrossRefGoogle Scholar
Kim, MA, Tura, E, Potkin, SG, Fallon, JH, Manoach, DS, Calhoun, VD, Turner, JA (2010). Working memory circuitry in schizophrenia shows widespread cortical inefficiency and compensation. Schizophrenia Research 117, 42–51.CrossRefGoogle ScholarPubMed
Ladouceur, CD, Silk, JS, Dahl, RE, Ostapenko, L, Kronhaus, DM, Phillips, ML (2009). Fearful faces influence attentional control processes in anxious youth and adults. Emotion 9, 855–864.CrossRefGoogle Scholar
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 ScholarPubMed
Leppanen, JM, Milders, M, Bell, JS, Terriere, E, Hietanen, JK (2004). Depression biases the recognition of emotionally neutral faces. Psychiatry Research 128, 123–133.CrossRefGoogle ScholarPubMed
Levens, SM, Gotlib, IH (2010). Updating positive and negative stimuli in working memory in depression. Journal of Experimental Psychology: General 139, 654–664.CrossRefGoogle ScholarPubMed
Matsuo, K, Glahn, DC, Peluso, MA, Hatch, JP, Monkul, ES, Najt, P, Sanches, M, Zamarripa, F, Li, J, Lancaster, JL, Fox, PT, Gao, JH, Soares, JC (2007). Prefrontal hyperactivation during working memory task in untreated individuals with major depressive disorder. Molecular Psychiatry 12, 158–166.CrossRefGoogle ScholarPubMed
Mayberg, HS, Liotti, M, Brannan, SK, McGinnis, S, Mahurin, RK, Jerabek, PA, Silva, JA, Tekell, JL, Martin, CC, Lancaster, JL, Fox, PT (1999). Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. American Journal of Psychiatry 156, 675–682.CrossRefGoogle ScholarPubMed
Neumeister, A, Drevets, WC, Belfer, I, Luckenbaugh, DA, Henry, S, Bonne, O, Herscovitch, P, Goldman, D, Charney, DS (2006). Effects of a alpha 2C-adrenoreceptor gene polymorphism on neural responses to facial expressions in depression. Neuropsychopharmacology 31, 1750–1756.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
Okada, G, Okamoto, Y, Morinobu, S, Yamawaki, S, Yokota, N (2003). Attenuated left prefrontal activation during a verbal fluency task in patients with depression. Neuropsychobiology 47, 21–26.CrossRefGoogle ScholarPubMed
Paelecke-Habermann, Y, Pohl, J, Leplow, B (2005). Attention and executive functions in remitted major depression patients. Journal of Affective Disorders 89, 125–135.CrossRefGoogle ScholarPubMed
Paradiso, S, Lamberty, GJ, Garvey, MJ, Robinson, RG (1997). Cognitive impairment in the euthymic phase of chronic unipolar depression. Journal of Nervous and Mental Disease 185, 748–754.CrossRefGoogle ScholarPubMed
Petrides, M (2000). Dissociable roles of mid-dorsolateral prefrontal and anterior inferotemporal cortex in visual working memory. Journal of Neuroscience 20, 7496–7503.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
Phillips, ML, Ladouceur, CD, Drevets, WC (2008). A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry 13, 833–857.CrossRefGoogle ScholarPubMed
Preiss, M, Kucerova, H, Lukavsky, J, Stepankova, H, Sos, P, Kawaciukova, R (2009). Cognitive deficits in the euthymic phase of unipolar depression. Psychiatry Research 169, 235–239.CrossRefGoogle ScholarPubMed
Schoning, S, Zwitserlood, P, Engelien, A, Behnken, A, Kugel, H, Schiffbauer, H, Lipina, K, Pachur, C, Kersting, A, Dannlowski, U, Baune, BT, Zwanzger, P, Reker, T, Heindel, W, Arolt, V, Konrad, C (2009). Working-memory fMRI reveals cingulate hyperactivation in euthymic major depression. Human Brain Mapping 30, 2746–2756.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
Siegle, GJ, Thompson, W, Carter, CS, Steinhauer, SR, Thase, ME (2007). Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biological Psychiatry 61, 198–209.CrossRefGoogle ScholarPubMed
Somerville, LH, Kim, H, Johnstone, T, Alexander, AL, Whalen, PJ (2004). Human amygdala responses during presentation of happy and neutral faces: correlations with state anxiety. Biological Psychiatry 55, 897–903.CrossRefGoogle ScholarPubMed
Spielberger, CD (1983). State-Trait Inventory (Form Y) Manual. Mind Garden: Redwood City, CA.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 ScholarPubMed
Surguladze, SA, Young, AW, Senior, C, Brebion, G, Travis, MJ, Phillips, ML (2004). Recognition accuracy and response bias to happy and sad facial expressions in patients with major depression. Neuropsychology 18, 212–218.CrossRefGoogle ScholarPubMed
Sweeney, JA, Kmiec, JA, Kupfer, DJ (2000). Neuropsychologic impairments in bipolar and unipolar mood disorders on the CANTAB neurocognitive battery. Biological Psychiatry 48, 674–684.CrossRefGoogle ScholarPubMed
Taylor Tavares, JV, Clark, L, Cannon, DM, Erickson, K, Drevets, WC, Sahakian, BJ (2007). Distinct profiles of neurocognitive function in unmedicated unipolar depression and bipolar II depression. Biological Psychiatry 62, 917–924.CrossRefGoogle ScholarPubMed
Tottenham, N, Tanaka, JW, Leon, AC, McCarry, T, Nurse, M, Hare, TA, Marcus, DJ, Westerlund, A, Casey, BJ, Nelson, C (2009). The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Research 168, 242–249.CrossRefGoogle ScholarPubMed
Victor, TA, Furey, ML, Fromm, SJ, Ohman, A, Drevets, WC (2010). Relationship between amygdala responses to masked faces and mood state and treatment in major depressive disorder. Archives of General Psychiatry 67, 1128–1138.CrossRefGoogle ScholarPubMed
Wagner, G, Koch, K, Schachtzabel, C, Reichenbach, JR, Sauer, H, Schlosser Md, RG (2008). Enhanced rostral anterior cingulate cortex activation during cognitive control is related to orbitofrontal volume reduction in unipolar depression. Journal of Psychiatry and Neuroscience 33, 199–208.Google ScholarPubMed
Wang, L, LaBar, KS, Smoski, M, Rosenthal, MZ, Dolcos, F, Lynch, TR, Krishnan, RR, McCarthy, G (2008). Prefrontal mechanisms for executive control over emotional distraction are altered in major depression. Psychiatry Research: Neuroimaging 163, 143–155.CrossRefGoogle ScholarPubMed
Ward, BD (2000). Simultaneous inference for fMRI data. AFNI AlphaSim documentation. Biophysics Research Institute, Medical College of Wisconsin: Milwaukee, WI.Google Scholar
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