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Dissociable patterns of medial prefrontal and amygdala activity to face identity versus emotion in bipolar disorder

Published online by Cambridge University Press:  25 January 2012

M. T. Keener ,
J. C. Fournier ,
B. C. Mullin ,
D. Kronhaus ,
S. B. Perlman ,
E. LaBarbara ,
J. C. Almeida  and
M. L. Phillips
M. T. Keener*
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
J. C. Fournier
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
D. Kronhaus
Affiliation:
Institute for Adaptive and Neural Computation, School of Informatics, The University of Edinburgh, Edinburgh, UK Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge, UK
S. B. Perlman
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
E. LaBarbara
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
J. 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. T. Keener, M.D., Western Psychiatric Institute and Clinic, University of Pittsburgh School of Medicine, Loeffler Building Room 202, 121 Meyran Avenue, Pittsburgh, PA 15213, USA. (Email: keenermt@upmc.edu)
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Abstract

Background

Individuals with bipolar disorder demonstrate abnormal social function. Neuroimaging studies in bipolar disorder have shown functional abnormalities in neural circuitry supporting face emotion processing, but have not examined face identity processing, a key component of social function. We aimed to elucidate functional abnormalities in neural circuitry supporting face emotion and face identity processing in bipolar disorder.

Method

Twenty-seven individuals with bipolar disorder I currently euthymic and 27 healthy controls participated in an implicit face processing, block-design paradigm. Participants labeled color flashes that were superimposed on dynamically changing background faces comprising morphs either from neutral to prototypical emotion (happy, sad, angry and fearful) or from one identity to another identity depicting a neutral face. Whole-brain and amygdala region-of-interest (ROI) activities were compared between groups.

Results

There was no significant between-group difference looking across both emerging face emotion and identity. During processing of all emerging emotions, euthymic individuals with bipolar disorder showed significantly greater amygdala activity. During facial identity and also happy face processing, euthymic individuals with bipolar disorder showed significantly greater amygdala and medial prefrontal cortical activity compared with controls.

Conclusions

This is the first study to examine neural circuitry supporting face identity and face emotion processing in bipolar disorder. Our findings of abnormally elevated activity in amygdala and medial prefrontal cortex (mPFC) during face identity and happy face emotion processing suggest functional abnormalities in key regions previously implicated in social processing. This may be of future importance toward examining the abnormal self-related processing, grandiosity and social dysfunction seen in bipolar disorder.

Keywords

Affective disordersamygdalabipolar disorderface processingfunctional magnetic resonance imagingidentity processingmedial prefrontal cortexmorphself-processingsocial processing
Type
Original Articles
Information
Psychological Medicine , Volume 42 , Issue 9 , September 2012 , pp. 1913 - 1924
Copyright
Copyright © Cambridge University Press 2012

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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
Altshuler, L, Bookheimer, S, Proenza, MA, Townsend, J, Sabb, F, Firestine, A, Bartzokis, G, Mintz, J, Mazziotta, J, Cohen, MS (2005). Increased amygdala activation during mania: a functional magnetic resonance imaging study. American Journal of Psychiatry 162, 1211–1213.CrossRefGoogle Scholar
Amodio, DM, Frith, CD (2006). Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience 7, 268–277.CrossRefGoogle ScholarPubMed
Angst, J, Gamma, A, Lewinsohn, P (2002). The evolving epidemiology of bipolar disorder. World Psychiatry 1, 146–148.Google ScholarPubMed
Bechara, A, Tranel, D, Damasio, H, Adolphs, R, Rockland, C, Damasio, AR (1995). Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269, 1115–1118.CrossRefGoogle 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 183, 308–313.CrossRefGoogle ScholarPubMed
Blumberg, HP, Stern, E, Ricketts, S, Martinez, D, De Asis, J, White, T, Epstein, J, Isenberg, N, McBride, PA, Kemperman, I, Emmerich, S, Dhawan, V, Eidelber, GD, Kocsis, JH, Silbersweig, DA (1999). Rostral and orbital prefrontal cortex dysfunction in the manic state of bipolar disorder. American Journal of Psychiatry 156, 1986–1988.CrossRefGoogle ScholarPubMed
Bora, E, Vahip, S, Gonul, AS, Akdeniz, F, Alkan, M, Ogut, M, Eryavuz, A (2005). Evidence for theory of mind deficits in euthymic patients with bipolar disorder. Acta Psychiatrica Scandinavica 112, 110–116.CrossRefGoogle ScholarPubMed
Bruce, V, Young, A (1986). Understanding face recognition. British Journal of Psychology 77, 305–327.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Dannlowski, U, Ohrmann, P, Konrad, C, Bauer, J, Kugel, H, Schoning, S, Kersting, A, Baune, BT, Arolt, V, Heindel, W, Zwitserlood, P, Suslow, T (2007). Reduced amygdala-prefrontal connectivity is associated with symptom severity in major depression. Pharmacopsychiatry 40, A004.CrossRefGoogle Scholar
Farah, MJ (1996). Is face recognition ‘special’? Evidence from neuropsychology. Behavioral Brain Research 76, 181–189.CrossRefGoogle ScholarPubMed
Feinberg, TE (2011). The nested neural hierarchy and the self. Consciousness and Cognition 20, 4–15.CrossRefGoogle ScholarPubMed
First, MB, Frances, A, Pincus, HA (1995 a). DSM-IV Handbook of Differential Diagnosis. American Psychiatric Press: Washington, DC.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Willians, JBW (1995 b). Structured Clinical Interview for DSM-IV Axis I Disorders (SCID version 2.0). Biometric Research Department, New York State Psychiatric Institute: New York.Google Scholar
Fossati, P, Hevenor, SJ, Graham, SJ, Grady, C, Keightley, ML, Craik, F, Mayberg, H (2003). In search of the emotional self: an FMRI study using positive and negative emotional words. American Journal of Psychiatry 160, 1938–1945.CrossRefGoogle ScholarPubMed
Gallagher, M, McMahan, RW, Schoenbaum, G (1999). Orbitofrontal cortex and representation of incentive value in associative learning. Journal of Neuroscience 19, 6610–6614.CrossRefGoogle ScholarPubMed
Getz, GE, Shear, PK, Strakowski, SM (2003). Facial affect recognition deficits in bipolar disorder. Journal of the International Neuropsychological Society 9, 623–632.CrossRefGoogle ScholarPubMed
Goswami, U, Sharma, A, Khastigir, U, Ferrier, IN, Young, AH, Gallagher, P, Thompson, JM, Moore, PB (2006). Neuropsychological dysfunction, soft neurological signs and social disability in euthymic patients with bipolar disorder. British Journal of Psychiatry 188, 366–373.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Hariri, AR, Tessitore, A, Mattay, VS, Fera, F, Weinberger, DR (2002). The amygdala response to emotional stimuli: a comparison of faces and scenes. NeuroImage 17, 317–323.CrossRefGoogle ScholarPubMed
Hassel, S, Almeida, J, Kerr, N, Nau, S, Ladouceur, C, Fissell, K, Kupfer, D, Phillips, M (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.CrossRefGoogle ScholarPubMed
Haxby, JV, Hoffman, EA, Gobbini, MI (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences 4, 223–233.CrossRefGoogle ScholarPubMed
Haxby, JV, Hoffman, EA, Gobbini, MI (2002). Human neural systems for face recognition and social communication. Biological Psychiatry 51, 59–67.CrossRefGoogle ScholarPubMed
Haxby, JV, Horwitz, B, Ungerleider, LG, Maisog, JM, Pietrini, P, Grady, CL (1994). The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations. Journal of Neuroscience 14, 6336–6353.CrossRefGoogle ScholarPubMed
Hoffman, EA, Haxby, JV (2000). Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nature Neuroscience 3, 80–84.CrossRefGoogle ScholarPubMed
Inder, ML, Crowe, MT, Moor, S, Luty, SE, Carter, JD, Joyce, PR (2008). ‘I actually don't know who I am’: the impact of bipolar disorder on the development of self. Psychiatry 71, 123–133.CrossRefGoogle ScholarPubMed
Insel, T (2010). From Discovery to Cure. Report of the National Advisory Mental Health Council's Workgroup (http://www.nimh.nih.gov/about/advisory-boards-and-groups/namhc/reports/fromdiscoverytocure.pdf). National Institutes of Health, National Institute of Mental Health, National Advisory Mental Health Council, August 2010.Google Scholar
Insel, T, Cuthbert, B, Garvey, M, Heinssen, R, Pine, DS, Quinn, K, Sanislow, C, Wang, P (2010). Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. American Journal of Psychiatry 167, 748–751.CrossRefGoogle Scholar
Jamison, KR (1995). Manic-depressive illness and creativity. Scientific American 272, 62–67.CrossRefGoogle ScholarPubMed
Kanwisher, N, McDermott, J, Chun, MM (1997). The fusiform face area: a module in human extrastriate cortex specialized for face perception. Journal of Neuroscience 17, 4302–4311.CrossRefGoogle ScholarPubMed
Keener, MT, Phillips, ML (2007). Neuroimaging in bipolar disorder: a critical review of current findings. Current Psychiatry Reports 9, 512–520.CrossRefGoogle ScholarPubMed
Kruger, S, Seminowicz, D, Goldapple, K, Kennedy, SH, Mayberg, HS (2003). State and trait influences on mood regulation in bipolar disorder: blood flow differences with an acute mood challenge. Biological Psychiatry 54, 1274–1283.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
Lieberman, MD (2007). Social cognitive neuroscience: a review of core processes. Annual Review of Psychology 58, 259–289.CrossRefGoogle ScholarPubMed
Lyon, HM, Startup, M, Bentall, RP (1999). Social cognition and the manic defense: attributions, selective attention, and self-schema in bipolar affective disorder. Journal of Abnormal Psychology 108, 273–282.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, GS, Lagopoulos, J, Das, P, Moss, K, Berk, M, Coulston, CM (2008). A functional MRI study of Theory of Mind in euthymic bipolar disorder patients. Bipolar Disorders 10, 943–956.CrossRefGoogle ScholarPubMed
Malhi, GS, Lagopoulos, J, Owen, AM, Ivanovski, B, Shnier, R, Sachdev, P (2007). Reduced activation to implicit affect induction in euthymic bipolar patients: an fMRI study. Journal of Affective Disorders 97, 109–122.CrossRefGoogle ScholarPubMed
Malhi, GS, Lagopoulos, J, Sachdev, P, Mitchell, PB, Ivanovski, B, Parker, GB (2004). Cognitive generation of affect in hypomania: an fMRI study. Bipolar Disorders 6, 271–285.CrossRefGoogle ScholarPubMed
McClure-Tone, E (2009). Socioemotional functioning in bipolar disorder versus typical development: behavioral and neural differences. Clinical Psychology: Science and Practice 16, 98–113.Google Scholar
Murray, CJ, Lopez, AD (1996). Evidence-based health policy – lessons from the Global Burden of Disease Study. Science 274, 740–743.CrossRefGoogle ScholarPubMed
Pelphrey, KA, Morris, JP, McCarthy, G, Labar, KS (2007). Perception of dynamic changes in facial affect and identity in autism. Social Cognitive and Affective Neuroscience 2, 140–149.CrossRefGoogle ScholarPubMed
Phillips, M (2007). The emerging role of neuroimaging in psychiatry: characterizing treatment-relevant endophenotypes. American Journal of Psychiatry 164, 697–699.CrossRefGoogle ScholarPubMed
Phillips, M, Ladouceur, C, Drevets, W (2008 a). 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, Travis, MJ, Fagiolini, A, Kupfer, DJ (2008 b). Medication effects in neuroimaging studies of bipolar disorder. American Journal of Psychiatry 165, 313–320.CrossRefGoogle ScholarPubMed
Spielberger, CD, Vagg, PR (1984). Psychometric properties of the STAI: a reply to Ramanaiah, Franzen, and Schill. Journal of Personality Assesment 48, 95–97.CrossRefGoogle Scholar
Tottenham, N, Tanaka, J, Leon, A, Mccarry, T, Nurse, M, Hare, T, Marcus, D, 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
Vuilleumier, P, Pourtois, G (2007). Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 45, 174–194.CrossRefGoogle ScholarPubMed
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