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Fronto-limbic-striatal dysfunction in pediatric and adult patients with bipolar disorder: impact of face emotion and attentional demands

Published online by Cambridge University Press:  12 August 2013

M. A. Brotman ,
W.-L. Tseng ,
A. K. Olsavsky ,
S. J. Fromm ,
E. J. Muhrer ,
J. G. Rutenberg ,
C. M. Deveney ,
N. E. Adleman ,
C. A. Zarate Jr.  and
D. S. Pine
...Show all authors
M. A. Brotman*
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
W.-L. Tseng
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
A. K. Olsavsky
Affiliation:
Semel Institute for Neuroscience and Human Behavior at UCLA, Los Angeles, CA, USA
S. J. Fromm
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
E. J. Muhrer
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
J. G. Rutenberg
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
C. M. Deveney
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
N. E. Adleman
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
C. A. Zarate Jr.
Affiliation:
Experimental Therapeutics and Pathophysiology Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
D. S. Pine
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
E. Leibenluft
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
*
*Address for correspondence: M. A. Brotman, Ph.D., Building 10, Room B1D43C, 10 Center Drive, Bethesda, MD 20892, USA. (Email: [email protected])
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Abstract

Background

Research in bipolar disorder (BD) implicates fronto-limbic-striatal dysfunction during face emotion processing but it is unknown how such dysfunction varies by task demands, face emotion and patient age.

Method

During functional magnetic resonance imaging (fMRI), 181 participants, including 62 BD (36 children and 26 adults) and 119 healthy comparison (HC) subjects (57 children and 62 adults), engaged in constrained and unconstrained processing of emotional (angry, fearful, happy) and non-emotional (neutral) faces. During constrained processing, subjects answered questions focusing their attention on the face; this was processed either implicitly (nose width rating) or explicitly (hostility; subjective fear ratings). Unconstrained processing consisted of passive viewing.

Results

Pediatric BD rated neutral faces as more hostile than did other groups. In BD patients, family-wise error (FWE)-corrected region of interest (ROI) analyses revealed dysfunction in the amygdala, inferior frontal gyrus (IFG), anterior cingulate cortex (ACC) and putamen. Patients with BD showed amygdala hyperactivation during explicit processing (hostility ratings) of fearful faces and passive viewing of angry and neutral faces but IFG hypoactivation during implicit processing of neutral and happy faces. In the ACC and striatum, the direction of dysfunction varied by task demand: BD demonstrated hyperactivation during unconstrained processing of angry or neutral faces but hypoactivation during constrained processing (implicit or explicit) of angry, neutral or happy faces.

Conclusions

Findings suggest amygdala hyperactivation in BD while processing negatively valenced and neutral faces, regardless of attentional condition, and BD IFG hypoactivation during implicit processing. In the cognitive control circuit involving the ACC and putamen, BD neural dysfunction was sensitive to task demands.

Keywords

Attentionbipolar disorderface emotionfronto-limbic-striatal dysfunctionimagingpediatric
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 8 , June 2014 , pp. 1639 - 1651
Copyright
Copyright © Cambridge University Press 2013 

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References

Almeida, JR, Mechelli, A, Hassel, S, Versace, A, Kupfer, DJ, Phillips, ML (2009). Abnormally increased effective connectivity between parahippocampal gyrus and ventromedial prefrontal regions during emotion labeling in bipolar disorder. Psychiatry Research 174, 195–201.CrossRefGoogle ScholarPubMed
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.Google Scholar
Altshuler, L, Bookheimer, S, Townsend, J, Proenza, MA, Sabb, F, Mintz, J, Cohen, MS (2008). Regional brain changes in bipolar I depression: a functional magnetic resonance imaging study. Bipolar Disorders 10, 708–717.Google Scholar
Beesdo, K, Lau, JY, Guyer, AE, McClure-Tone, EB, Monk, CS, Nelson, EE, Fromm, SJ, Goldwin, MA, Wittchen, HU, Leibenluft, E, Ernst, M, Pine, DS (2009). Common and distinct amygdala-function perturbations in depressed vs anxious adolescents. Archives of General Psychiatry 66, 275–285.Google Scholar
Blond, BN, Fredericks, CA, Blumberg, HP (2012). Functional neuroanatomy of bipolar disorder: structure, function, and connectivity in an amygdala-anterior paralimbic neural system. Bipolar Disorders 14, 340–355.Google Scholar
Blumberg, HP, Donegan, NH, Sanislow, CA, Collins, S, Lacadie, C, Skudlarski, P, Gueorguieva, R, Fulbright, RK, McGlashan, TH, Gore, JC, Krystal, JH (2005). Preliminary evidence for medication effects on functional abnormalities in the amygdala and anterior cingulate in bipolar disorder. Psychopharmacology (Berlin) 183, 308–313.Google Scholar
Brotman, MA, Guyer, AE, Lawson, ES, Horsey, SE, Rich, BA, Dickstein, DP, Pine, DS, Leibenluft, E (2008). Facial emotion labeling deficits in children and adolescents at risk for bipolar disorder. American Journal of Psychiatry 165, 385–389.CrossRefGoogle ScholarPubMed
Brotman, MA, Rich, BA, Guyer, AE, Lunsford, JR, Horsey, SE, Reising, MM, Thomas, LA, Fromm, SJ, Towbin, K, Pine, DS, Leibenluft, E (2010). Amygdala activation during emotion processing of neutral faces in children with severe mood dysregulation versus ADHD or bipolar disorder. American Journal of Psychiatry 167, 61–69.Google Scholar
Bush, G, Luu, P, Posner, MI (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 4, 215–222.Google Scholar
Cabeza, R, Nyberg, L (2000). Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience 12, 1–47.Google Scholar
Chang, KD, Wagner, C, Garrett, A, Howe, M, Reiss, A (2008). A preliminary functional magnetic resonance imaging study of prefrontal-amygdalar activation changes in adolescents with bipolar depression treated with lamotrigine. Bipolar Disorders 10, 426–431.Google Scholar
Chen, CH, Lennox, 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.Google Scholar
Chen, CH, Suckling, J, Lennox, BR, Ooi, C, Bullmore, ET (2011). A quantitative meta-analysis of fMRI studies in bipolar disorder. Bipolar Disorders 13, 1–15.Google Scholar
Chen, CH, Suckling, J, Ooi, C, Jacob, R, Lupson, V, Bullmore, ET, Lennox, BR (2010). A longitudinal fMRI study of the manic and euthymic states of bipolar disorder. Bipolar Disorders 12, 344–347.Google Scholar
Costafreda, SG, Brammer, MJ, David, AS, Fu, CH (2008). Predictors of amygdala activation during the processing of emotional stimuli: a meta-analysis of 385 PET and fMRI studies. Brain Research Reviews 58, 57–70.CrossRefGoogle ScholarPubMed
Davis, M, Whalen, PJ (2001). The amygdala: vigilance and emotion. Molecular Psychiatry 6, 13–34.Google Scholar
Delvecchio, G, Fossati, P, Boyer, P, Brambilla, P, Falkai, P, Gruber, O, Hietala, J, Lawrie, SM, Martinot, JL, McIntosh, AM, Meisenzahl, E, Frangou, S (2012). Common and distinct neural correlates of emotional processing in bipolar disorder and major depressive disorder: a voxel-based meta-analysis of functional magnetic resonance imaging studies. European Neuropsychopharmacology 22, 100–113.Google Scholar
Devinsky, O, Morrell, MJ, Vogt, BA (1995). Contributions of anterior cingulate cortex to behaviour. Brain 118, 279–306.Google Scholar
Drevets, WC, Savitz, J, Trimble, M (2008). The subgenual anterior cingulate cortex in mood disorders. CNS Spectrums 13, 663–681.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (2002). Structured Clinical Interview for DSM-IV TR Axis I Disorders, Research Version, Patient Edition (SCID-I/P). Biometrics Research Department, New York State Psychiatric Institute: New York.Google Scholar
Fleck, DE, Shear, PK, Madore, M, Strakowski, SM (2008). Wisconsin Card Sorting Test performance in bipolar disorder: effects of mood state and early course. Bipolar Disorders 10, 539–545.Google Scholar
Foland-Ross, LC, Bookheimer, SY, Lieberman, MD, Sugar, CA, Townsend, JD, Fischer, J, Torrisi, S, Penfold, C, Madsen, SK, Thompson, PM, Altshuler, LL (2012). Normal amygdala activation but deficient ventrolateral prefrontal activation in adults with bipolar disorder during euthymia. NeuroImage 59, 738–744.Google Scholar
Foland, LC, Altshuler, LL, Bookheimer, SY, Eisenberger, N, Townsend, J, Thompson, PM (2008). Evidence for deficient modulation of amygdala response by prefrontal cortex in bipolar mania. Psychiatry Research 162, 27–37.Google Scholar
Garrett, AS, Reiss, AL, Howe, ME, Kelley, RG, Singh, MK, Adleman, NE, Karchemskiy, A, Chang, KD (2012). Abnormal amygdala and prefrontal cortex activation to facial expressions in pediatric bipolar disorder. Journal of the American Academy of Child and Adolescent Psychiatry 51, 821–831.Google Scholar
Guyer, AE, Monk, CS, McClure-Tone, EB, Nelson, EE, Roberson-Nay, R, Adler, AD, Fromm, SJ, Leibenluft, E, Pine, DS, Ernst, M (2008). A developmental examination of amygdala response to facial expressions. Journal of Cognitive Neuroscience 20, 1565–1582.Google Scholar
Hafeman, DM, Chang, KD, Garrett, AS, Sanders, EM, Phillips, ML (2012). Effects of medication on neuroimaging findings in bipolar disorder: an updated review. Bipolar Disorders 14, 375–410.Google Scholar
Hassel, S, Almeida, JR, Frank, E, Versace, A, Nau, SA, Klein, CR, Kupfer, DJ, Phillips, ML (2009). Prefrontal cortical and striatal activity to happy and fear faces in bipolar disorder is associated with comorbid substance abuse and eating disorder. Journal of Affective Disorders 118, 19–27.Google Scholar
Hassel, S, Almeida, JR, Kerr, N, Nau, S, Ladouceur, CD, Fissell, K, Kupfer, DJ, Phillips, ML (2008). Elevated striatal and decreased dorsolateral prefrontal cortical activity in response to emotional stimuli in euthymic bipolar disorder: no associations with psychotropic medication load. Bipolar Disorders 10, 916–927.Google Scholar
Houenou, J, Frommberger, J, Carde, S, Glasbrenner, M, Diener, C, Leboyer, M, Wessa, M (2011). Neuroimaging-based markers of bipolar disorder: evidence from two meta-analyses. Journal of Affective Disorders 132, 344–355.Google Scholar
Hulvershorn, LA, Karne, H, Gunn, AD, Hartwick, SL, Wang, Y, Hummer, TA, Anand, A (2012). Neural activation during facial emotion processing in unmedicated bipolar depression, euthymia, and mania. Biological Psychiatry 71, 603–610.Google Scholar
Jogia, J, Haldane, M, Cobb, A, Kumari, V, Frangou, S (2008). Pilot investigation of the changes in cortical activation during facial affect recognition with lamotrigine monotherapy in bipolar disorder. British Journal of Psychiatry 192, 197–201.Google Scholar
Kalmar, JH, Wang, F, Chepenik, LG, Womer, FY, Jones, MM, Pittman, B, Shah, MP, Martin, A, Constable, RT, Blumberg, HP (2009). Relation between amygdala structure and function in adolescents with bipolar disorder. Journal of the American Academy of Child and Adolescent Psychiatry 48, 636–642.Google Scholar
Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Williamson, D, Ryan, N (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry 36, 980–988.Google Scholar
Keener, MT, Fournier, JC, Mullin, BC, Kronhaus, D, Perlman, SB, LaBarbara, E, Almeida, JC, Phillips, ML (2012). Dissociable patterns of medial prefrontal and amygdala activity to face identity versus emotion in bipolar disorder. Psychological Medicine 42, 1913–1924.Google Scholar
Killgore, WD, Gruber, SA, Yurgelun-Todd, DA (2008). Abnormal corticostriatal activity during fear perception in bipolar disorder. Neuroreport 19, 1523–1527.Google Scholar
Kim, P, Arizpe, JM, Rosen, BH, Razdan, V, Haring, CT, Jenkins, SE, Deveney, CM, Brotman, MA, Blair, RJR, Pine, DS, Baker, CI, Leibenluft, E (in press). Impaired fixation to eyes during face emotion labeling in children with bipolar disorder or severe mood dysregulation. Journal of Psychiatry and Neuroscience.Google Scholar
Kim, P, Thomas, LA, Rosen, BH, Moscicki, AM, Brotman, MA, Zarate, CA Jr., Blair, RJR, Pine, DS, Leibenluft, E (2012). Differing amygdala responses to facial expressions in children vs. adults with bipolar disorder. American Journal of Psychiatry 169, 642–649.Google Scholar
Kohler, CG, Hoffman, LJ, Eastman, LB, Healey, K, Moberg, PJ (2011). Facial emotion perception in depression and bipolar disorder: a quantitative review. Psychiatry Research 188, 303–309.Google Scholar
Kupferschmidt, DA, Zakzanis, KK (2011). Toward a functional neuroanatomical signature of bipolar disorder: quantitative evidence from the neuroimaging literature. Psychiatry Research 193, 71–79.Google Scholar
Ladouceur, CD, Farchione, T, Diwadkar, V, Pruitt, P, Radwan, J, Axelson, DA, Birmaher, B, Phillips, ML (2011). Differential patterns of abnormal activity and connectivity in the amygdala-prefrontal circuitry in bipolar-I and bipolar-NOS youth. Journal of the American Academy of Child and Adolescent Psychiatry 50, 1275–1289.e2.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.Google Scholar
Lennox, BR, Jacob, R, Calder, AJ, Lupson, V, Bullmore, ET (2004). Behavioural and neurocognitive responses to sad facial affect are attenuated in patients with mania. Psychological Medicine 34, 795–802.Google Scholar
Lieberman, MD, Cunningham, WA (2009). Type I and Type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience 4, 423–428.Google Scholar
Liu, J, Blond, BN, van Dyck, LI, Spencer, L, Wang, F, Blumberg, HP (2012). Trait and state corticostriatal dysfunction in bipolar disorder during emotional face processing. Bipolar Disorders 14, 432–441.Google Scholar
Mourão-Miranda, J, Oliveira, L, Ladouceur, CD, Marquand, A, Brammer, M, Birmaher, B, Axelson, D, Phillips, ML (2012). Pattern recognition and functional neuroimaging help to discriminate healthy adolescents at risk for mood disorders from low risk adolescents. PLoS One 7, e29482.Google Scholar
Nurnberger, JI, Blehar, MC, Kaufmann, CA, York-Cooler, C, Simpson, SG, Harkavy-Friedman, J, Severe, JB, Malaspina, D, Reich, T (1994). Diagnostic interview for genetic studies. Rationale, unique features, and training. NIMH Genetics Initiative. Archives of General Psychiatry 51, 849–859.Google Scholar
Olsavsky, AK, Brotman, MA, Rutenberg, JG, Muhrer, EJ, Deveney, CM, Fromm, SJ, Towbin, K, Pine, DS, Leibenluft, E (2012). Amygdala hyperactivation during face emotion processing in unaffected youth at risk for bipolar disorder. Journal of the American Academy of Child and Adolescent Psychiatry 51, 294–303.Google Scholar
Passarotti, AM, Sweeney, JA, Pavuluri, MN (2010). Emotion processing influences working memory circuits in pediatric bipolar disorder and attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry 49, 1064–1080.Google Scholar
Passarotti, AM, Sweeney, JA, Pavuluri, MN (2011). Fronto-limbic dysfunction in mania pre-treatment and persistent amygdala over-activity post-treatment in pediatric bipolar disorder. Psychopharmacology (Berlin) 216, 485–499.Google Scholar
Pavuluri, MN, O'Connor, MM, Harral, E, Sweeney, JA (2007). Affective neural circuitry during facial emotion processing in pediatric bipolar disorder. Biological Psychiatry 62, 158–167.Google Scholar
Pavuluri, MN, Passarotti, A (2008). Neural bases of emotional processing in pediatric bipolar disorder. Expert Review of Neurotherapeutics 8, 1381–1387.Google Scholar
Pavuluri, MN, Passarotti, AM, Fitzgerald, JM, Wegbreit, E, Sweeney, JA (2012). Risperidone and divalproex differentially engage the fronto-striato-temporal circuitry in pediatric mania: a pharmacological functional magnetic resonance imaging study. Journal of the American Academy of Child and Adolescent Psychiatry 51, 157–170.e5.Google Scholar
Pavuluri, MN, Passarotti, AM, Harral, EM, Sweeney, JA (2009). An fMRI study of the neural correlates of incidental versus directed emotion processing in pediatric bipolar disorder. Journal of the American Academy of Child and Adolescent Psychiatry 48, 308–319.Google Scholar
Perlman, SB, Almeida, JR, Kronhaus, DM, Versace, A, Labarbara, EJ, Klein, CR, Phillips, ML (2012). Amygdala activity and prefrontal cortex-amygdala effective connectivity to emerging emotional faces distinguish remitted and depressed mood states in bipolar disorder. Bipolar Disorders 14, 162–174.Google Scholar
Pfeifer, JC, Welge, J, Strakowski, SM, Adler, CM, DelBello, MP (2008). Meta-analysis of amygdala volumes in children and adolescents with bipolar disorder. Journal of the American Academy of Child and Adolescent Psychiatry 47, 1289–1298.Google Scholar
Phillips, ML, Travis, MJ, Fagiolini, A, Kupfer, DJ (2008). Medication effects in neuroimaging studies of bipolar disorder. American Journal of Psychiatry 165, 313–320.Google Scholar
Pochon, JB, Riis, J, Sanfey, AG, Nystrom, LE, Cohen, JD (2008). Functional imaging of decision conflict. Journal of Neuroscience 28, 3468–3473.Google Scholar
Poznanski, EO, Grossman, JA, Buchsbaum, Y, Banegas, M, Freeman, L, Gibbons, R (1984). Preliminary studies of the reliability and validity of the Children's Depression Rating Scale. Journal of the American Academy of Child Psychiatry 23, 191–197.Google Scholar
Quirk, GJ, Beer, JS (2006). Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Current Opinion in Neurobiology 16, 723–727.Google Scholar
Rich, BA, Fromm, SJ, Berghorst, LH, Dickstein, DP, Brotman, MA, Pine, DS, Leibenluft, E (2008). Neural connectivity in children with bipolar disorder: impairment in the face emotion processing circuit. Journal of Child Psychology and Psychiatry 49, 88–96.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.Google Scholar
Robinson, JL, Monkul, ES, Tordesillas-Gutiérrez, D, Franklin, C, Bearden, CE, Fox, PT, Glahn, DC (2008). Fronto-limbic circuitry in euthymic bipolar disorder: evidence for prefrontal hyperactivation. Psychiatry Research 164, 106–113.Google Scholar
Schenkel, LS, Pavuluri, MN, Herbener, ES, Harral, EM, Sweeney, JA (2007). Facial emotion processing in acutely ill and euthymic patients with pediatric bipolar disorder. Journal of the American Academy of Child and Adolescent Psychiatry 46, 1070–1079.Google Scholar
Sergerie, K, Chochol, C, Armony, JL (2008). The role of the amygdala in emotional processing: a quantitative meta-analysis of functional neuroimaging studies. Neuroscience and Biobehavioral Reviews 32, 811–830.Google Scholar
Shah, MP, Wang, F, Kalmar, JH, Chepenik, LG, Tie, K, Pittman, B, Jones, MM, Constable, RT, Gelernter, J, Blumberg, HP (2009). Role of variation in the serotonin transporter protein gene (SLC6A4) in trait disturbances in the ventral anterior cingulate in bipolar disorder. Neuropsychopharmacology 34, 1301–1310.Google Scholar
Strakowski, SM, Adler, CM, Almeida, J, Altshuler, LL, Blumberg, HP, Chang, KD, Delbello, MP, Frangou, S, McIntosh, A, Phillips, ML, Sussman, JE, Townsend, JD (2012). The functional neuroanatomy of bipolar disorder: a consensus model. Bipolar Disorders 14, 313–325.CrossRefGoogle ScholarPubMed
Strakowski, SM, Adler, CM, Holland, SK, Mills, NP, DelBello, MP, Eliassen, JC (2005). Abnormal fMRI brain activation in euthymic bipolar disorder patients during a counting Stroop interference task. American Journal of Psychiatry 162, 1697–1705.Google Scholar
Surguladze, SA, Marshall, N, Schulze, K, Hall, MH, Walshe, M, Bramon, E, Phillips, ML, Murray, RM, McDonald, C (2010). Exaggerated neural response to emotional faces in patients with bipolar disorder and their first-degree relatives. NeuroImage 53, 58–64.Google Scholar
Thomas, LA, Brotman, MA, Muhrer, EJ, Rosen, BH, Bones, BL, Reynolds, RC, Deveney, CM, Pine, DS, Leibenluft, E (2012). Parametric modulation of neural activity by emotion in youth with bipolar disorder, youth with severe mood dysregulation, and healthy volunteers. Archives of General Psychiatry 69, 1257–1266.Google Scholar
Thomas, LA, Kim, P, Bones, BL, Hinton, KE, Milch, HS, Reynolds, RC, Adleman, NE, Marsh, AA, Blair, RJR, Pine, DS, Leibenluft, E (2013). Elevated amygdala responses to emotional faces in youths with chronic irritability or bipolar disorder. NeuroImage: Clinical 2, 637–645.CrossRefGoogle ScholarPubMed
Townsend, J, Altshuler, LL (2012). Emotion processing and regulation in bipolar disorder: a review. Bipolar Disorders 14, 326–339.Google Scholar
Versace, A, Thompson, WK, Zhou, D, Almeida, JR, Hassel, S, Klein, CR, Kupfer, DJ, Phillips, ML (2010). Abnormal left and right amygdala-orbitofrontal cortical functional connectivity to emotional faces: state versus trait vulnerability markers of depression in bipolar disorder. Biological Psychiatry 67, 422–431.Google Scholar
Vizueta, N, Rudie, JD, Townsend, JD, Torrisi, S, Moody, TD, Bookheimer, SY, Altshuler, LL (2012). Regional fMRI hypoactivation and altered functional connectivity during emotion processing in nonmedicated depressed patients with bipolar II disorder. American Journal of Psychiatry 169, 831–840.Google Scholar
Wessa, M, Houenou, J, Paillère-Martinot, ML, Berthoz, S, Artiges, E, Leboyer, M, Martinot, JL (2007). Fronto-striatal overactivation in euthymic bipolar patients during an emotional go/nogo task. American Journal of Psychiatry 164, 638–646.Google Scholar
Williams, JB (1988). A structured interview guide for the Hamilton Depression Rating Scale. Archives of General Psychiatry 45, 742–747.Google Scholar
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429–435.CrossRefGoogle ScholarPubMed
Yurgelun-Todd, DA, Gruber, SA, Kanayama, G, Killgore, WD, Baird, AA, Young, AD (2000). fMRI during affect discrimination in bipolar affective disorder. Bipolar Disorders 2, 237–248.Google Scholar
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