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Neural alterations of fronto-striatal circuitry during reward anticipation in euthymic bipolar disorder

Published online by Cambridge University Press:  30 August 2016

S. Schreiter ,
S. Spengler ,
A. Willert ,
S. Mohnke ,
D. Herold ,
S. Erk ,
N. Romanczuk-Seiferth ,
E. Quinlivan ,
C. Hindi-Attar  and
C. Banzhaf
...Show all authors
S. Schreiter*
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
S. Spengler
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
A. Willert
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
S. Mohnke
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
D. Herold
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany Department of Psychiatry, Psychotherapy and Psychosomatic Medicine, Ruppiner Kliniken, Brandenburg Medical School, Neuruppin, Germany
S. Erk
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
N. Romanczuk-Seiferth
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
E. Quinlivan
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
C. Hindi-Attar
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
C. Banzhaf
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
C. Wackerhagen
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
L. Romund
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
M. Garbusow
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
T. Stamm
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
A. Heinz
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
H. Walter
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
F. Bermpohl
Affiliation:
Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Germany
*
*Address for correspondence: S. Schreiter, Department of Psychiatry and Psychotherapy, Charité – Universitätsmedizin Berlin, Campus Mitte, Charitéplatz 1, 10117 Berlin, Germany. (Email: [email protected])
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Abstract

Background

Bipolar disorder (BD), with the hallmark symptoms of elevated and depressed mood, is thought to be characterized by underlying alterations in reward-processing networks. However, to date the neural circuitry underlying abnormal responses during reward processing in BD remains largely unexplored. The aim of this study was to investigate whether euthymic BD is characterized by aberrant ventral striatal (VS) activation patterns and altered connectivity with the prefrontal cortex in response to monetary gains and losses.

Method

During functional magnetic resonance imaging 20 euthymic BD patients and 20 age-, gender- and intelligence quotient-matched healthy controls completed a monetary incentive delay paradigm, to examine neural processing of reward and loss anticipation. A priori defined regions of interest (ROIs) included the VS and the anterior prefrontal cortex (aPFC). Psychophysiological interactions (PPIs) between these ROIs were estimated and tested for group differences for reward and loss anticipation separately.

Results

BD participants, relative to healthy controls, displayed decreased activation selectively in the left and right VS during anticipation of reward, but not during loss anticipation. PPI analyses showed decreased functional connectivity between the left VS and aPFC in BD patients compared with healthy controls during reward anticipation.

Conclusions

This is the first study showing decreased VS activity and aberrant connectivity in the reward-processing circuitry in euthymic, medicated BD patients during reward anticipation. Our findings contrast with research supporting a reward hypersensitivity model of BD, and add to the body of literature suggesting that blunted activation of reward processing circuits may be a vulnerability factor for mood disorders.

Keywords

Bipolar disorderconnectivityfunctional magnetic resonance imagingrewardventral striatum
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 15 , November 2016 , pp. 3187 - 3198
Copyright
Copyright © Cambridge University Press 2016 

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References

Abler, B, Greenhouse, I, Ongur, D, Walter, H, Heckers, S (2008). Abnormal reward system activation in mania. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 33, 2217–2227.CrossRefGoogle ScholarPubMed
Adida, M, Jollant, F, Clark, L, Besnier, N, Guillaume, S, Kaladjian, A, Mazzola-Pomietto, P, Jeanningros, R, Goodwin, GM, Azorin, J-M, Courtet, P (2011). Trait-related decision-making impairment in the three phases of bipolar disorder. Biological Psychiatry 70, 357–365.CrossRefGoogle ScholarPubMed
Almeida, JRC, Versace, A, Hassel, S, Kupfer, D, 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
American Psychiatric Association (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Press: Washington, DC.Google Scholar
Andrews, MM, Meda, SA, Thomas, AD, Potenza, MN, Krystal, JH, Worhunsky, PD, Stevens, MC, O'Malley, S, Book, GA, Reynolds, B, Pearlson, GD (2011). Individuals family history positive for alcoholism show functional magnetic resonance imaging differences in reward sensitivity that are related to impulsivity factors. Biological Psychiatry 69, 675–683.CrossRefGoogle ScholarPubMed
Bermpohl, F, Dalanay, U, Kahnt, T, Sajonz, B, Heimann, H, Ricken, R, Stoy, M, Hägele, C, Schlagenhauf, F, Adli, M, Wrase, J, Ströhle, A, Heinz, A, Bauer, M (2009). A preliminary study of increased amygdala activation to positive affective stimuli in mania. Bipolar Disorders 11, 70–75.CrossRefGoogle ScholarPubMed
Bermpohl, F, Kahnt, T, Dalanay, U, Hägele, C, Sajonz, B, Wegner, T, Stoy, M, Adli, M, Krüger, S, Wrase, J, Ströhle, A, Bauer, M, Heinz, A (2010). Altered representation of expected value in the orbitofrontal cortex in mania. Human Brain Mapping 31, 958–969.CrossRefGoogle ScholarPubMed
Caseras, X, Lawrence, NS, Murphy, K, Wise, RG, Phillips, ML (2013). Ventral striatum activity in response to reward: differences between bipolar I and II disorders. American Journal of Psychiatry 170, 533–541.CrossRefGoogle ScholarPubMed
Chandler, RA, Wakeley, J, Goodwin, GM, Rogers, RD (2009). Altered risk-aversion and risk-seeking behavior in bipolar disorder. Biological Psychiatry 66, 840–846.CrossRefGoogle ScholarPubMed
Chase, H, Nusslock, R, Almeida, JRC, Forbes, EE, Labarbara, EJ, 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.CrossRefGoogle ScholarPubMed
Delgado, MR, Nystrom, LE, Fissell, C, Noll, DC, Fiez, JA (2000). Tracking the hemodynamic responses to reward and punishment in the striatum. Journal of Neurophysiology 84, 3072–3077.CrossRefGoogle ScholarPubMed
Diekhof, EK, Gruber, O (2010). When desire collides with reason: functional interactions between anteroventral prefrontal cortex and nucleus accumbens underlie the human ability to resist impulsive desires. Journal of Neuroscience: the Official Journal of the Society for Neuroscience 30, 1488–1493.CrossRefGoogle ScholarPubMed
Diekhof, EK, Keil, M, Obst, KU, Henseler, I, Dechent, P, Falkai, P, Gruber, O (2012 a). A functional neuroimaging study assessing gender differences in the neural mechanisms underlying the ability to resist impulsive desires. Brain Research 1473, 63–77.CrossRefGoogle ScholarPubMed
Diekhof, EK, Nerenberg, L, Falkai, P, Dechent, P, Baudewig, J, Gruber, O (2012 b). Impulsive personality and the ability to resist immediate reward: an fMRI study examining interindividual differences in the neural mechanisms underlying self-control. Human Brain Mapping 33, 2768–2784.CrossRefGoogle ScholarPubMed
Duncan, J, Owen, AM (2000). Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends in Neurosciences 23, 475–483.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1997). Structured Clinical Interview for DSM-IV Axis I Disorders, Clinician Version (SCID-CV). American Psychiatric Press, Inc.: Washington, DC.Google Scholar
Friedman, L, Glover, GH (2006). Report on a multicenter fMRI quality assurance protocol. Journal of Magnetic Resonance Imaging 23, 827–839.CrossRefGoogle ScholarPubMed
Gray, J (1994). Framework for a taxonomy of psychiatric disorder. In Emotions: Essays on Emotion Theory (ed. Van Goozen, H. M., Van De Poll, N. E. and Sergeant, J. A.), pp. 29–59. Lawrence Erlbaum Associates: Hillsdale, NJ.Google Scholar
Grimm, O, Heinz, A, Walter, H, Kirsch, P, Erk, S, Haddad, L, Plichta, MM, Romanczuk-Seiferth, N, Pöhland, L, Mohnke, S, Mühleisen, TW, Mattheisen, M, Witt, SH, Schäfer, A, Cichon, S, Nöthen, M, Rietschel, M, Tost, H, Meyer-Lindenberg, A (2014). Striatal response to reward anticipation. JAMA Psychiatry 71, 531–539.CrossRefGoogle ScholarPubMed
Guitart-Masip, M, Fuentemilla, L, Bach, DR, Huys, QJ, Dayan, P, Dolan, RJ, Duzel, E (2011). Action dominates valence in anticipatory representations in the human striatum and dopaminergic midbrain. Journal of Neuroscience 31, 7867–7875.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Hägele, C, Schlagenhauf, F, Rapp, M, Sterzer, P, Beck, A, Bermpohl, F, Stoy, M, Ströhle, A, Wittchen, HU, Dolan, RJ, Heinz, A (2015). Dimensional psychiatry: reward dysfunction and depressive mood across psychiatric disorders. Psychopharmacology 232, 331–341.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Heller, AS, Johnstone, T, Light, SN, Peterson, MJ, Kolden, GG, Kalin, NH, Davidson, RJ (2013). Relationships between changes in sustained fronto-striatal connectivity and positive affect in major depression resulting from antidepressant treatment. American Journal of Psychiatry 170, 197–206.CrossRefGoogle ScholarPubMed
Heller, AS, Johnstone, T, Shackman, AJ, Light, SN, Peterson, MJ, Kolden, GG, Kalin, NH, Davidson, RJ (2009). Reduced capacity to sustain positive emotion in major depression reflects diminished maintenance of fronto-striatal brain activation. Proceedings of the National Academy of Sciences of the USA 106, 22445–22450.CrossRefGoogle ScholarPubMed
Kaplan, H, Sadock, B (1997). Kaplan and Sadock's Synopsis of Psychiatry: Behavioral Sciences, Clinical Psychiatry. Lippincott Williams & Wilkins: Baltimore, MD.Google Scholar
Kirsch, P, Schienle, A, Stark, R, Sammer, G, Blecker, C, Walter, B, Ott, U, Burkart, J, Vaitl, D (2003). Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study. NeuroImage 20, 1086–1095.CrossRefGoogle Scholar
Knutson, B, Fong, GW, Adams, CM, Varner, JL, Hommer, D (2001). Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport 12, 3683–3687.CrossRefGoogle ScholarPubMed
Knutson, B, Greer, SM (2008). Anticipatory affect: neural correlates and consequences for choice. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 3771–3786.CrossRefGoogle ScholarPubMed
Kobiella, A, Ripke, S, Kroemer, NB, Vollmert, C, Vollstädt-Klein, S, Ulshöfer, DE, Smolka, MN (2014). Acute and chronic nicotine effects on behaviour and brain activation during intertemporal decision making. Addiction Biology 19, 918–930.CrossRefGoogle ScholarPubMed
Lehrl, S (2005). Mehrfachwahl-Wortschatz-Intelligenztest: MWT-B. Spitta: Balingen.Google Scholar
Lessov-Schlaggar, CN, Lepore, RL, Kristjansson, SD, Schlaggar, BL, Barnes, KA, Petersen, SE, Madden, PAF, Heath, AC, Barch, DM (2013). Functional neuroimaging study in identical twin pairs discordant for regular cigarette smoking. Addiction Biology 18, 98–108.CrossRefGoogle ScholarPubMed
Linke, J, King, AV, Rietschel, M, Strohmaier, J, Hennerici, M, Gass, A, Meyer-lindenberg, A (2012). Increased medial orbitofrontal and amygdala activation: evidence for a systems-level endophenotype of bipolar I disorder. American Journal of Psychiatry 169, 316–325.CrossRefGoogle ScholarPubMed
Luo, S, Ainslie, G, Giragosian, L, Monterosso, JR (2011). Striatal hyposensitivity to delayed rewards among cigarette smokers. Drug and Alcohol Dependence 116, 18–23.CrossRefGoogle ScholarPubMed
Martin-Soelch, C, Missimer, J, Leenders, KL, Schultz, W (2003). Neural activity related to the processing of increasing monetary reward in smokers and nonsmokers. European Journal of Neuroscience 18, 680–688.CrossRefGoogle Scholar
McClure, SM, York, MK, Montague, PR (2004). The neural substrates of reward processing in humans: the modern role of fMRI. Neuroscientist: a Review Journal Bringing Neurobiology, Neurology and Psychiatry 10, 260–268.CrossRefGoogle ScholarPubMed
McLaren, DG, Ries, ML, Xu, G, Johnson, SC (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. NeuroImage 61, 1277–1286.CrossRefGoogle ScholarPubMed
Miller, EK, Cohen, JD (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience 24, 167–202.CrossRefGoogle ScholarPubMed
Nusslock, R, Almeida, JRC, Forbes, EE, Versace, A, Frank, E, Labarbara, EJ, Klein, CR, 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.CrossRefGoogle ScholarPubMed
O'Doherty, JP (2004). Reward representations and reward-related learning in the human brain: insights from neuroimaging. Current Opinion in Neurobiology 14, 769–776.CrossRefGoogle ScholarPubMed
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9, 97–113.CrossRefGoogle ScholarPubMed
Phillips, ML, Travis, MJ, Fagiolini, A, Kupfer, DJ (2008). Medication effects in neuroimaging studies of bipolar disorder. American Journal of Psychiatry 165, 313–320.CrossRefGoogle ScholarPubMed
Sackeim, HA (2001). The definition and meaning of treatment-resistant depression. Journal of Clinical Psychiatry 62 (Suppl. 16), 10–17.Google ScholarPubMed
Satterthwaite, TD, Kable, JW, Vandekar, L, Katchmar, N, Bassett, DS, Baldassano, CF, Ruparel, K, Elliott, MA, Sheline, YI, Gur, RC, Gur, RE, Davatzikos, C, Leibenluft, E, Thase, ME, Wolf, DH (2015). Common and dissociable dysfunction of the reward system in bipolar and unipolar depression reward dysfunction in depression. Neuropsychopharmacology 40, 2258–2268.CrossRefGoogle ScholarPubMed
Strakowski, SM, Adler, CM, Almeida, JRC, 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
Trost, S, Diekhof, EK, Zvonik, K, Lewandowski, M, Usher, J, Keil, M, Zilles, D, Falkai, P, Dechent, P, Gruber, O (2014). Disturbed anterior prefrontal control of the mesolimbic reward system and increased impulsivity in bipolar disorder. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 39, 1–37.CrossRefGoogle ScholarPubMed
Urošević, S, Abramson, LY, Harmon-Jones, E, Alloy, LB (2008). Dysregulation of the behavioral approach system (BAS) in bipolar spectrum disorders: review of theory and evidence. Clinical Psychology Review 28, 1188–1205.CrossRefGoogle Scholar
Valentin, VV, O'Doherty, JP (2009). Overlapping prediction errors in dorsal striatum during instrumental learning with juice and money reward in the human brain. Journal of Neurophysiology 102, 3384–3391.CrossRefGoogle ScholarPubMed
Wittchen, H-U, Wunderlich, U, Gruschwitz, S, Zaudig, M (1997). SKID-I. Strukturiertes Klinisches Interview für DSM-IV. Hogrefe: Göttingen.Google Scholar
Yacubian, J, Sommer, T, Schroeder, K, Glascher, J, Braus, DF, Buchel, C (2007). Subregions of the ventral striatum show preferential coding of reward magnitude and probability. NeuroImage 38, 557–563.CrossRefGoogle ScholarPubMed
Yip, SW, Worhunsky, PD, Rogers, RD, 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.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
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