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Abnormal anterior cingulate cortical activity during emotional n-back task performance distinguishes bipolar from unipolar depressed females

Published online by Cambridge University Press:  21 November 2011

M. A. Bertocci ,
G. M. Bebko ,
B. C. Mullin ,
S. A. Langenecker ,
C. D. Ladouceur ,
J. R. C. Almeida  and
M. L. Phillips
M. A. Bertocci*
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
G. M. Bebko
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
B. C. Mullin
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
S. A. Langenecker
Affiliation:
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA
C. D. Ladouceur
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
J. R. C. Almeida
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
M. L. Phillips
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA Department of Psychological Medicine, Cardiff University, Cardiff, UK
*
*Address for correspondence: M. A. Bertocci, Ph.D., Western Psychiatric Institute and Clinic, Loeffler Building, room 205, 121 Meyran Avenue, Pittsburgh, PA 15213, USA. (Email: [email protected])
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Abstract

Background

Depression in the context of bipolar disorder (BDd) is often misdiagnosed as unipolar disorder depression (UDd) leading to poor clinical outcomes for many bipolar sufferers. We examined neural circuitry supporting emotion regulation in females with either BDd or UDd as a first stage toward identifying biomarkers that may differentiate BDd from UDd.

Method

Fifty-seven females aged 18–45 years participated in this study: 23 with UDd, 18 with bipolar disorder type I depression (BDId) and 16 healthy females. During 3-T functional magnetic resonance imaging (fMRI), the participants performed an emotional face n-back (EFNBACK) task, that is an n-back task with high (2-back) and low (0-back) memory load conditions flanked by two positive, negative or neutral face distracters. This paradigm examines executive control with emotional distracters–emotion regulation.

Results

High memory load with neutral face distracters elicited greater bilateral and left dorsal anterior midcingulate cortex (dAMCC) activity in UDd than in healthy and BDId females respectively, and greater bilateral putamen activity in both depressed groups versus healthy females. High memory load with happy face distracters elicited greater left putamen activity in UDd than in healthy females. Psychotropic medication was associated with greater putamen activity to these contrasts in UDd females.

Conclusions

During high memory load with neutral face distracters, elevated dAMCC activity in UDd suggests abnormal recruitment of attentional control circuitry to maintain task performance, whereas elevated putamen activity unrelated to psychotropic medication in BDId females may suggest an attentional bias toward ambiguous neutral face distracters. Differential patterns of functional abnormalities in neural circuitry supporting attentional control during emotion regulation, especially in the dAMCC, is a promising neuroimaging measure to distinguish UDd from BDId in females.

Keywords

Bipolar disorderdepressionemotion regulationemotional n-backunipolar disorder
Type
Original Articles
Information
Psychological Medicine , Volume 42 , Issue 7 , July 2012 , pp. 1417 - 1428
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
Anand, A, Li, Y, Wang, Y, Gardner, K, Lowe, M (2007). Reciprocal effects of antidepressant treatment on activity and connectivity of the mood regulating circuit: an fMRI study. Journal of Neuropsychiatry Clinical Neuroscience 19, 274–282.CrossRefGoogle ScholarPubMed
Annett, M (1970). A classification of hand preference by association analysis. British Journal of Psychology 61, 303–321.CrossRefGoogle ScholarPubMed
Blair, K, Spreen, O (1989). Predicting premorbid IQ: a revision of the National Adult Reading Test. Clinical Neuropsychologist 3, 129–136.CrossRefGoogle Scholar
Bush, G, Shin, LM (2006). The Multi-Source Interference Task: an fMRI task that reliably activates the cingulo-frontal-parietal cognitive/attention network. Nature Protocols 1, 308–313.CrossRefGoogle ScholarPubMed
Chen, C, Lenox, B, Jacob, R, Calder, A, Lupson, V, Bisbrown-Chippendale, R, Suckling, J, Bullmore, E (2006). Explicit and implicit facial affect recognition in manic and depressed states of bipolar disorder: a functional magnetic resonance imaging study. Biological Psychiatry 59, 31–39.CrossRefGoogle ScholarPubMed
Dannlowski, U, Ohrmann, P, Bauer, J, Kugel, H, Arolt, V, heindel, W, Kersting, A, Baune, B, Suslow, T (2007). Amygdala reactivity to masked negative faces is associated with automatic judgmental bias in major depression: a 3T fMRI study. Journal of Psychiatry and Neuroscience 32, 423–429.Google Scholar
Deckersbach, T, Rauch, S, Buhlman, U, Ostacher, M, Beucke, J, Nierenberg, A, Sachs, G, Dougherty, DD (2008). An fMRI investigation of working memory and sadness in females with bipolar disorder: a brief report. Bipolar Disorders 10, 928–942.CrossRefGoogle ScholarPubMed
Drevets, WC (2003). Neuroimaging abnormalities in the amygdala in mood disorders. Annals of the New York Academy of Sciences 985, 420–444.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
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
Fales, C, Barch, D, Rundle, M, Mintun, M, Snyder, A, Cohen, J, Mathews, J, Sheline, Y (2008). Altered emotional interference processing in affective and cognitive-control brain circuitry in major depression. Biological Psychiatry 63, 377–384.CrossRefGoogle ScholarPubMed
First, M, Spitzer, R, Gibbon, M, Williams, J (1995). Structured Clinical Interview for DSM-IV Axis I Disorders, Version 2.0. Biometric Research Department, New York State Psychiatric Institute: New York.Google Scholar
Folstein, M, Folstein, S, McHugh, P (1975). ‘Mini-Mental State’. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 12, 189–198.CrossRefGoogle Scholar
Fu, CHY, Williams, SCR, 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
Grimm, S, Beck, J, Schuepbach, D, Hell, D, Boesinger, P, Permpohl, F, Niehaus, l, Boeker, H, Northoff, G (2008). Imbalance between left and right dorsolateral prefrontal cortex in major depression is linked to negative emotional judgment: an fMRI study in severe major depressive disorder. Biological Psychiatry 63, 369–376.CrossRefGoogle ScholarPubMed
Gruber, SA, Rogowska, J, Yurgelun-Todd, DA (2004). Decreased activation of the anterior cingulate in bipolar patients: an fMRI study. Journal of Affective Disorders 82, 191–201.CrossRefGoogle ScholarPubMed
Haber, SN, Kim, K-S, Mailly, P, Calzavara, R (2006). Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. Journal of Neuroscience 26, 8368–8376.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Hirschfeld, RM, Lewis, L, Vornik, LA (2003). Perceptions and impact of bipolar disorder: how far have we really come? Results of the National Depressive and Manic-Depressive Association 2000 survey of individuals with bipolar disorder. Journal of Clinical Psychiatry 64, 161–174.CrossRefGoogle ScholarPubMed
Johnstone, T, van Reekum, C, Urry, H, Kalin, N, Davidson, R (2007). Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. Journal of Neuroscience 27, 8877–8884.CrossRefGoogle ScholarPubMed
Koch, K, Pauly, K, Kellermann, T, Seiferth, NY, Reske, M, Backes, V, Stöcker, T, Shah, NJ, Amunts, K, Kircher, T, Schneider, F, Habel, U (2007). Gender differences in the cognitive control of emotion: an fMRI study. Neuropsychologia 45, 2744–2754.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
Langenecker, S, Bieliauskas, L, Rapport, L, Zubieta, J, Wilde, E, Berent, S (2005). Face emotion perception and executive functioning deficitis in depression. Journal of Clinical and Experimental Neuropsychology 27, 320–333.CrossRefGoogle Scholar
Langenecker, SA, Kennedy, S, Guidotti, L, Briceno, E, Own, L, Hooven, T, Young, E, Akil, H, Noll, DC, Zubieta, J (2007). Frontal and limbic activation during inhibitory control predicts treatment response in major depressive disorder. Biological Psychiatry 62, 1272–1280.CrossRefGoogle ScholarPubMed
Langenecker, SA, Saunders, E, Kade, A, Ransom, M, McInnis, M (2010). Intermediate cognitive phenotypes in bipolar disorder. Journal of Affective Disorders 122, 285–293.CrossRefGoogle ScholarPubMed
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
Lorenzetti, V, Allen, NB, Fornito, A, Yücel, M (2009). Structural brain abnormalities in major depressive disorder: a selective review of recent MRI studies. Journal of Affective Disorders 117, 1–17.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Malhi, G, Lagopoulos, J, Ward, P, Kumari, V, Mitchell, P, Parker, GB, Ivanovski, B, Schdev, P (2004). Cognitive generation of affect in bipolar depression: an fMRI study. European Journal of Neuroscience 19, 741–754.CrossRefGoogle ScholarPubMed
McRae, K, Ochsner, KN, Mauss, IB, Gabrieli, JJD, Gross, JJ (2008). Gender differences in emotion regulation: an fMRI study of cognitive reappraisal. Group Processes and Intergroup Relations 11, 143–162.CrossRefGoogle ScholarPubMed
Mitterschiffthaler, MT, Williams, SCR, Walsh, ND, Cleare, AJ, Donaldson, C, Scott, J, Fu, CHY (2008). Neural basis of the emotional Stroop interference effect in major depression. Psychological Medicine 38, 247–256.CrossRefGoogle ScholarPubMed
Ochsner, KN, Gross, JJ (2005). The cognitive control of emotion. Trends in Cognitive Sciences 9, 242–249.CrossRefGoogle ScholarPubMed
Pavuluri, MN, Oconnor, MM, Harral, E, Sweeney, JA (2007). Affective neural circuitry during facial emotion processing in pediatric bipolar disorder. Biological Psychiatry 62, 158–167.CrossRefGoogle ScholarPubMed
Phillips, M, Ladouceur, C, Drevets, W (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
Phillips, ML (2003). Understanding the neurobiology of emotion perception: implications for psychiatry. British Journal of Psychiatry 182, 190–192.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
Rich, BA, Vinton, DT, Roberson-Nay, R, Hommer, RE, Berghorst, LH, McClure, EB, Fromm, SJ, Pine, DS, Leibenluft, E (2006). Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder. Proceedings of the National Academy of Sciences USA 103, 8900–8905.CrossRefGoogle ScholarPubMed
Schienle, A, Schäfer, A, Stark, R, Walter, B, Vaitl, D (2005). Gender differences in the processing of disgust- and fear-inducing pictures: an fMRI study. Neuroreport 16, 277–280.CrossRefGoogle ScholarPubMed
Siegle, GJ, Steinhauer, SR, Thase, ME, Stenger, AV, 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
Strakowski, SM, Adler, CM, DelBello, MP (2002). Volumetric MRI studies of mood disorders: do they distinguish unipolar and bipolar disorder? Bipolar Disorders 4, 80–88.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
Surguladze, SA, Brammer, MJ, Young, AW, Andrew, C, Travis, MJ, Williams, SCR, Phillips, ML (2003). A preferential increase in the extrastriate response to signals of danger. NeuroImage 19, 1317–1328.CrossRefGoogle ScholarPubMed
Tottenhan, N, Tanaka, J, Leon, A, McCarry, T, Nurse, M, Hare, T (2009). The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Research 168, 242–249.CrossRefGoogle Scholar
Ward, B (2002). AlphaSim. National Institute of Mental Health: Bethesda, MD.Google Scholar
Weissman, MM, Bland, RC, Canino, GJ, Faravelli, C, Greenwald, S, Hwu, H-G, Joyce, PR, Karam, EG, Lee, C-K, Lellouch, J, Lépine, J-P, Newman, SC, Rubio-Stipec, M, Wells, JE, Wickramaratne, PJ, Wittchen, H-U, Yeh, E-K (1996). Cross-national epidemiology of major depression and bipolar disorder. Journal of the American Medical Association 276, 293–299.CrossRefGoogle ScholarPubMed
Young, AW, Rowland, D, Calder, AJ, Etcoff, NL, Seth, A, Perrett, DI (1997). Facial expression megamix: tests of dimensional and category accounts of emotion recognition. Cognition 63, 271–313.CrossRefGoogle ScholarPubMed
Young, R, Biggs, J, Ziegler, V, Meyer, D (1978). A rating scale for mania: reliability, validity, and sensitivity. British Journal of Psychiatry 133, 429–435.CrossRefGoogle ScholarPubMed
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