Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T06:41:29.224Z Has data issue: false hasContentIssue false
  • English
  • Français

Longitudinal changes in brain activation during anticipation of monetary loss in bipolar disorder

Published online by Cambridge University Press:  21 December 2018

Anna Manelis Open the ORCID record for Anna Manelis [Opens in a new window] ,
Richelle Stiffler ,
Jeanette C. Lockovich ,
Jorge R. C. Almeida Open the ORCID record for Jorge R. C. Almeida [Opens in a new window] ,
Haris A. Aslam  and
Mary L. Phillips
Anna Manelis*
Affiliation:
Department of Psychiatry, Western Psychiatric Institute and Clinic, University of Pittsburgh Medical Center, University of Pittsburgh, Pittsburgh, PA, USA
Richelle Stiffler
Affiliation:
Department of Psychiatry, Western Psychiatric Institute and Clinic, University of Pittsburgh Medical Center, University of Pittsburgh, Pittsburgh, PA, USA
Jeanette C. Lockovich
Affiliation:
Department of Psychiatry, Western Psychiatric Institute and Clinic, University of Pittsburgh Medical Center, University of Pittsburgh, Pittsburgh, PA, USA
Jorge R. C. Almeida
Affiliation:
Dell Medical School, The University of Texas at Austin, Austin, TX, USA
Haris A. Aslam
Affiliation:
Department of Psychiatry, Western Psychiatric Institute and Clinic, University of Pittsburgh Medical Center, University of Pittsburgh, Pittsburgh, PA, USA
Mary L. Phillips
Affiliation:
Department of Psychiatry, Western Psychiatric Institute and Clinic, University of Pittsburgh Medical Center, University of Pittsburgh, Pittsburgh, PA, USA
*
Author for correspondence: Anna Manelis, E-mail: anna.manelis@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Individuals with bipolar disorder (BD) show aberrant brain activation patterns during reward and loss anticipation. We examined for the first time longitudinal changes in brain activation during win and loss anticipation to identify trait markers of aberrant anticipatory processing in BD.

Methods

Thirty-four euthymic and depressed individuals with BD-I and 17 healthy controls (HC) were scanned using functional magnetic resonance imaging twice 6 months apart during a reward task.

Results

HC, but not individuals with BD, showed longitudinal reductions in the right lateral occipital cortex (RLOC) activation during processing of cues predicting possible money loss (p-corrected <0.05). This result was not affected by psychotropic medication, mood state or the changes in depression/mania severity between the two scans in BD. Elevated symptoms of subthreshold hypo/mania at baseline predicted more aberrant longitudinal patterns of RLOC activation explaining 12.5% of variance in individuals with BD.

Conclusions

Increased activation in occipital cortex during negative outcome anticipation may be related to elevated negative emotional arousal during anticipatory cue processing. One interpretation is that, unlike HC, individuals with BD were not able to learn at baseline that monetary losses were smaller than monetary gains and were not able to reduce emotional arousal for negative cues 6 months later. Future research in BD should examine how modulating occipital cortical activation affects learning from experience in individuals with BD.

Keywords

Bipolar disorderfMRIlongitudinalloss anticipationoccipital cortex
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 16 , December 2019 , pp. 2781 - 2788
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andersen, SM, Spielman, LA and Bargh, JA (1992) Future-event schemas and certainty about the future: automaticity in depressives’ future-event predictions. Journal of Personality and Social Psychology 63, 711–723.Google Scholar
Andersson, JLR, Jenkinson, M and Smith, S (2007) Non-Linear Registration Aka Spatial Normalisation (Technical Report FMRIB Technical Report TR07JA2). Oxford: FMRIB Centre.Google Scholar
Bertocci, MA, Bebko, G, Dwojak, A, Iyengar, S, Ladouceur, CD, Fournier, JC, Versace, A, Perlman, SB, Almeida, JRC, Travis, MJ, Gill, MK, Bonar, L, Schirda, C, Diwadkar, VA, Sunshine, JL, Holland, SK, Kowatch, RA, Birmaher, B, Axelson, D, Horwitz, SM, Frazier, T, Arnold, LE, Fristad, MA, Youngstrom, EA, Findling, RL and Phillips, ML (2017) Longitudinal relationships among activity in attention redirection neural circuitry and symptom severity in youth. Biological Psychiatry. Cognitive Neuroscience and Neuroimaging 2, 336–345.Google Scholar
Blair, J and Spreen, O (1989) Predicting premorbid IQ: a revision of the national adult reading test. The Clinical Neuropsychologist 3, 129–136.Google Scholar
Caseras, X, Lawrence, NS, Murphy, K, Wise, RG and Phillips, ML (2013) Ventral striatum activity in response to reward: differences between bipolar I and II disorders. The American Journal of Psychiatry 170, 533–541.Google Scholar
Cerullo, MA, Fleck, DE, Eliassen, JC, Smith, MS, DelBello, MP, Adler, CM and Strakowski, SM (2012) A longitudinal functional connectivity analysis of the amygdala in bipolar I disorder across mood states. Bipolar Disorders 14, 175–184.Google Scholar
Chase, HW, Nusslock, R, Almeida, JRC, Forbes, EE, LaBarbara, EJ and Phillips, ML (2013) Dissociable patterns of abnormal frontal cortical activation during anticipation of an uncertain reward or loss in bipolar versus major depression. Bipolar Disorders 15, 839–854.Google Scholar
Davidson, RJ (1995) Cerebral asymmetry, emotion, and affective style. In Davidson, RJ and Hughdahl, K (eds), Brain Asymmetry. Cambridge, MA: MIT Press, pp. 361–387.Google Scholar
Dell'Osso, L, Armani, A, Rucci, P, Frank, E, Fagiolini, A, Corretti, G, Shear, MD, Grochocinski, VJ, Maser, JD, Endicott, J and Cassano, G (2002) Measuring mood spectrum: comparison of interview (SCI MOODS) and self-report (MOODS-SR) instrument. Comprehensive Psychiatry 43, 69–73.Google Scholar
First, M, Spitzer, R, Gibbon, M and Williams, J (1995) Structured clinical interview for DSM-IV Axis I Disorders – Patient Edition (SCID-I/P, Version 2.0), Biometrics Research Department, New York State Psychiatric Institute, New York, NY.Google Scholar
Folstein, M, Folstein, S and 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.Google Scholar
Forbes, EE, Hariri, AR, Martin, SL, Silk, JS, Moyles, DL, Fisher, PM, Brown, SM, Ryan, ND, Birmaher, B, Axelson, DA and Dahl, RE (2009) Altered striatal activation predicting real-world positive affect in adolescent major depressive disorder. The American Journal of psychiatry 166, 64–73.Google Scholar
Ganis, G, Thompson, WL and Kosslyn, SM (2004) Brain areas underlying visual mental imagery and visual perception: an fMRI study. Brain research. Cognitive Brain Research 20, 226–241.Google Scholar
Grill-Spector, K, Kushnir, T, Edelman, S, Avidan, G, Itzchak, Y and Malach, R (1999) Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24, 187–203.Google Scholar
Hägele, C, Schlagenhauf, F, Rapp, M, Sterzer, P, Beck, A, Bermpohl, F, Stoy, M, Ströhle, A, Wittchen, H-U, Dolan, RJ and Heinz, A (2015) Dimensional psychiatry: reward dysfunction and depressive mood across psychiatric disorders. Psychopharmacology (Berl.) 232, 331–341.Google Scholar
Hamilton, M (1960) A rating scale for depression. Journal of Neurology Neurosurgery & Psychiatry 23, 56–62.Google Scholar
Hirschfeld, RMA, Lewis, L and 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. The Journal of Clinical Psychiatry 64, 161–174.Google Scholar
Jenkinson, M, Bannister, P, Brady, M and Smith, S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17, 825–841.Google Scholar
Johnson, SL, Eisner, LR and Carver, CS (2009) Elevated expectancies among persons diagnosed with bipolar disorder. The British Journal of Clinical Psychology 48, 217–222.Google Scholar
Judd, LL and Akiskal, HS (2003) Depressive episodes and symptoms dominate the longitudinal course of bipolar disorder. Current Psychiatry Reports 5, 417–418.Google Scholar
Kollmann, B, Scholz, V, Linke, J, Kirsch, P and Wessa, M (2017) Reward anticipation revisited – evidence from an fMRI study in euthymic bipolar I patients and healthy first-degree relatives. Journal of Affective Disorders 219, 178–186.Google Scholar
Kosslyn, SM, Shin, LM, Thompson, WL, McNally, RJ, Rauch, SL, Pitman, RK and Alpert, NM (1996) Neural effects of visualizing and perceiving aversive stimuli: a PET investigation. Neuroreport 7, 1569–1576.Google Scholar
Lang, PJ, Bradley, MM, Fitzsimmons, JR, Cuthbert, BN, Scott, JD, Moulder, B and Nangia, V (1998) Emotional arousal and activation of the visual cortex: an fMRI analysis. Psychophysiology 35, 199–210.Google Scholar
Maller, JJ, Anderson, R, Thomson, RH, Rosenfeld, JV, Daskalakis, ZJ and Fitzgerald, PB (2015) Occipital bending (Yakovlevian torque) in bipolar depression. Psychiatry Research 231, 8–14.Google Scholar
Manelis, A, Almeida, JRC, Stiffler, R, Lockovich, JC, Aslam, HA and Phillips, ML (2016) Anticipation-related brain connectivity in bipolar and unipolar depression: a graph theory approach. Brain 139, 2554–2566.Google Scholar
Marchand, WR, Lee, JN, Thatcher, J, Thatcher, GW, Jensen, C and Starr, J (2007) A preliminary longitudinal fMRI study of frontal-subcortical circuits in bipolar disorder using a paced motor activation paradigm. Journal of Affective Disorders 103, 237–241.Google Scholar
Mather, M, Mitchell, KJ, Raye, CL, Novak, DL, Greene, EJ and Johnson, MK (2006) Emotional arousal can impair feature binding in working memory. Journal of Cognitive Neuroscience 18, 614–625.Google Scholar
Nusslock, R, Almeida, JR, Forbes, EE, Versace, A, Frank, E, Labarbara, EJ, Klein, CR and Phillips, ML (2012) Waiting to win: elevated striatal and orbitofrontal cortical activity during reward anticipation in euthymic bipolar disorder adults. Bipolar Disorders 14, 249–260.Google Scholar
Phan, KL, Wager, T, Taylor, SF and Liberzon, I (2002) Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 16, 331–348.Google Scholar
Pruim, RHR, Menne, M, van Rooij, D, Llera, A, Buitelaa, JK and Beckmann, CF (2015) ICA-AROMA: a robust ICA-based strategy for removing motion artifacts from fMRI data. Neuroimage 112, 267–277.Google Scholar
Robinson, TE, Yager, LM, Cogan, ES and Saunders, BT (2014) On the motivational properties of reward cues: individual differences. Neuropharmacology 76, 450–459.Google Scholar
Schreiter, S, Spengler, S, Willert, A, Mohnke, S, Herold, D, Erk, S, Romanczuk-Seiferth, N, Quinlivan, E, Hindi-Attar, C, Banzhaf, C, Wackerhagen, C, Romund, L, Garbusow, M, Stamm, T, Heinz, A, Walter, H and Bermpohl, F (2016) Neural alterations of fronto-striatal circuitry during reward anticipation in euthymic bipolar disorder. Psychological Medicine 46, 3187–3198.Google Scholar
Shaffer, JJ, Johnson, CP, Fiedorowicz, JG, Christensen, GE, Wemmie, JA and Magnotta, VA (2018) Impaired sensory processing measured by functional MRI in bipolar disorder manic and depressed mood states. Brain Imaging and Behavior 12, 837–847.Google Scholar
Smith, SM (2002) Fast robust automated brain extraction. Human Brain Mapping 17, 143–155.Google Scholar
Strunk, DR, Lopez, H and DeRubeis, RJ (2006) Depressive symptoms are associated with unrealistic negative predictions of future life events. Behaviour Research and Therapy 44, 861–882.Google Scholar
Wise, T, Radua, J, Via, E, Cardoner, N, Abe, O, Adams, TM, Amico, F, Cheng, Y, Cole, JH, de Azevedo Marques Périco, C, Dickstein, DP, Farrow, TFD, Frodl, T, Wagner, G, Gotlib, IH, Gruber, O, Ham, BJ, Job, DE, Kempton, MJ, Kim, MJ, Koolschijn, PCMP, Malhi, GS, Mataix-Cols, D, McIntosh, AM, Nugent, AC, O'Brien, JT, Pezzoli, S, Phillips, ML, Sachdev, PS, Salvadore, G, Selvaraj, S, Stanfield, AC, Thomas, AJ, van Tol, MJ, van der Wee, NJA, Veltman, DJ, Young, AH, Fu, CH, Cleare, AJ and Arnone, D (2017) Common and distinct patterns of grey-matter volume alteration in major depression and bipolar disorder: evidence from voxel-based meta-analysis. Molecular Psychiatry 22, 1455–1463.Google Scholar
Worsley, K (2001) Statistical analysis of activation images. In Jezzard, P, Matthews, PM and Smith, SM (eds), Functional MRI: An Introduction to Methods. New York: Oxford University Press, pp. 251–270.Google Scholar
Yip, SW, Worhunsky, PD, Rogers, RD and Goodwin, GM (2015) Hypoactivation of the ventral and dorsal striatum during reward and loss anticipation in antipsychotic and mood stabilizer-naive bipolar disorder. Neuropsychopharmacology 40, 658–666.Google Scholar
Young, RC, Biggs, JT, Ziegler, VE and Meyer, DA (1978) A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429–435.Google Scholar
Supplementary material: File

Manelis et al. supplementary material

Manelis et al. supplementary material

Download Manelis et al. supplementary material(File)
File 227.7 KB