Lithium modulates striatal reward anticipation and prediction error coding in healthy volunteers.
Journal
Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
ISSN: 1740-634X
Titre abrégé: Neuropsychopharmacology
Pays: England
ID NLM: 8904907
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
09
03
2020
accepted:
13
10
2020
revised:
12
10
2020
pubmed:
1
11
2020
medline:
24
6
2021
entrez:
31
10
2020
Statut:
ppublish
Résumé
Lithium is one of the most effective mood-stabilizing medications in bipolar disorder. This study was designed to test whether lithium administration may stabilize mood via effects on reward processing. It was hypothesized that lithium administration would modulate reward processing in the striatum and affect both anticipation and outcome computations. Thirty-seven healthy human participants (18 males, 33 with suitable fMRI data) received 11 (±1) days of lithium carbonate or placebo intervention (double-blind), after which they completed the monetary incentive delay task while fMRI data were collected. The monetary incentive delay task is a robust task with excellent test-retest reliability and is well suited to investigate different phases of reward processing within the caudate and nucleus accumbens. To test for correlations with prediction error signals a Rescorla-Wagner reinforcement-learning model was applied. Lithium administration enhanced activity in the caudate during reward anticipation compared to placebo. In contrast, lithium administration reduced caudate and nucleus accumbens activity during reward outcome. This latter effect seems related to learning as reward prediction errors showed a positive correlation with caudate and nucleus accumbens activity during placebo, which was absent after lithium administration. Lithium differentially modulates the anticipation relative to the learning of rewards. This suggests that lithium might reverse dampened reward anticipation while reducing overactive reward updating in patients with bipolar disorder. This specific effect of lithium suggests that a targeted modulation of reward learning may be a viable approach for novel interventions in bipolar disorder.
Identifiants
pubmed: 33127993
doi: 10.1038/s41386-020-00895-2
pii: 10.1038/s41386-020-00895-2
pmc: PMC7853118
doi:
Substances chimiques
Lithium
9FN79X2M3F
Types de publication
Journal Article
Randomized Controlled Trial
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
386-393Subventions
Organisme : Medical Research Council
ID : MR/S003037/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N008103/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/K022202/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : WT100973AIA
Pays : United Kingdom
Organisme : Department of Health
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 203139/Z/16/Z
Pays : United Kingdom
Références
Kessing LV, Bauer M, Nolen WA, Severus E, Goodwin GM, Geddes J. Effectiveness of maintenance therapy of lithium vs other mood stabilizers in monotherapy and in combinations: a systematic review of evidence from observational studies. Bipolar Disord. 2018;20:419–31.
doi: 10.1111/bdi.12623
Malhi GS, Tanious M, Das P, Coulston CM, Berk M. Potential mechanisms of action of lithium in bipolar disorder. CNS Drugs. 2013;27:135–53.
pubmed: 23371914
doi: 10.1007/s40263-013-0039-0
pmcid: 23371914
Nusslock R, Young CB, Damme KSF. Elevated reward-related neural activation as a unique biological marker of bipolar disorder: assessment and treatment implications. Behav Res Ther. 2014;62:74–87.
pubmed: 25241675
pmcid: 6727647
doi: 10.1016/j.brat.2014.08.011
Alloy LB, Abramson LY. The role of the behavioral approach system (BAS) in bipolar spectrum disorders. Curr Dir Psychol Sci. 2010. https://doi.org/10.1177/0963721410370292 .
Hommer DW, Bjork JM, Gilman JM. Imaging brain response to reward in addictive disorders. Ann N Y Acad Sci. 2011. https://doi.org/10.1111/j.1749-6632.2010.05898.x .
Oldham S, Murawski C, Fornito A, Youssef G, Yücel M, Lorenzetti V. The anticipation and outcome phases of reward and loss processing: a neuroimaging meta-analysis of the monetary incentive delay task. Hum Brain Mapp. 2018;39:1–21.
doi: 10.1002/hbm.24184
Cao Z, Bennett M, Orr C, Icke I, Banaschewski T, Barker GJ, et al. Mapping adolescent reward anticipation, receipt, and prediction error during the monetary incentive delay task. Hum Brain Mapp. 2019;40:262–83.
pubmed: 30240509
doi: 10.1002/hbm.24370
pmcid: 30240509
Schultz W. Behavioral dopamine signals. Trends Neurosci. 2007;30:203–10.
pubmed: 17400301
doi: 10.1016/j.tins.2007.03.007
pmcid: 17400301
Stringaris A, Belil PVR, Artiges E, Lemaitre H, Gollier-Briant F, Wolke S, et al. The brain s response to reward anticipation and depression in adolescence: dimensionality, specificity, and longitudinal predictions in a community-based sample. Am J Psychiatry. 2015. https://doi.org/10.1176/appi.ajp.2015.14101298 .
Ng TH, Alloy LB, Smith DV. Meta-analysis of reward processing in major depressive disorder reveals distinct abnormalities within the reward circuit. Transl Psychiatry. 2019. https://doi.org/10.1038/s41398-019-0644-x .
Berghorst LH, Kumar P, Greve DN, Deckersbach T, Ongur D, Dutra SJ, et al. Stress and reward processing in bipolar disorder: a functional magnetic resonance imaging study. Bipolar Disord. 2016;18:602–11.
pubmed: 27870507
pmcid: 5234857
doi: 10.1111/bdi.12444
Nusslock R, Almeida JRC, Forbes EE, Versace A, Frank E, Labarbara EJ, et al. Waiting to win: elevated striatal and orbitofrontal cortical activity during reward anticipation in euthymic bipolar disorder adults. Bipolar Disord. 2012;14:249–60.
pubmed: 22548898
doi: 10.1111/j.1399-5618.2012.01012.x
pmcid: 22548898
Mason L, O’Sullivan N, Montaldi D, Bentall RP, El-Deredy W. Decision-making and trait impulsivity in bipolar disorder are associated with reduced prefrontal regulation of striatal reward valuation. Brain. 2014;137:2346–55.
pubmed: 25009169
pmcid: 4107743
doi: 10.1093/brain/awu152
Abler B, Greenhouse I, Ongur D, Walter H, Heckers S. Abnormal reward system activation in mania. Neuropsychopharmacology. 2008;33:2217–27.
pubmed: 17987058
doi: 10.1038/sj.npp.1301620
pmcid: 17987058
Caseras X, Lawrence NS, Murphy K, Wise RG, Phillips ML. Ventral striatum activity in response to reward: Differences between bipolar i and II disorders. Am J Psychiatry. 2013;170:533–41.
pubmed: 23558337
pmcid: 3640293
doi: 10.1176/appi.ajp.2012.12020169
Yip SW, Worhunsky PD, Rogers RD, Goodwin GM. Hypoactivation of the ventral and dorsal striatum during reward and loss anticipation in antipsychotic and mood stabilizer-naive bipolar disorder. Neuropsychopharmacology. 2015;40:658–66.
pubmed: 25139065
doi: 10.1038/npp.2014.215
pmcid: 25139065
Hafeman DM, Chang KD, Garrett AS, Sanders EM, Phillips ML. Effects of medication on neuroimaging findings in bipolar disorder: an updated review. Bipolar Disord. 2012;14:375–410.
pubmed: 22631621
doi: 10.1111/j.1399-5618.2012.01023.x
pmcid: 22631621
Yip SW, Doherty J, Wakeley J, Saunders K, Tzagarakis C, De Wit H, et al. Reduced subjective response to acute ethanol administration among young men with a broad bipolar phenotype. Neuropsychopharmacology. 2012. https://doi.org/10.1038/npp.2012.45 .
Knutson B, Fong GW, Adams CM, Varner JL, Hommer D. Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport. 2001. https://doi.org/10.1097/00001756-200112040-00016 .
Monkul ES, Matsuo K, Nicoletti MA, Dierschke N, Hatch JP, Dalwani M, et al. Prefrontal gray matter increases in healthy individuals after lithium treatment: a voxel-based morphometry study. Neurosci Lett. 2007;429:7–11.
pubmed: 17996370
pmcid: 2693231
doi: 10.1016/j.neulet.2007.09.074
Kohno T, Shiga T, Toyomaki A, Kusumi I, Matsuyama T, Inoue T, et al. Effects of lithium on brain glucose metabolism in healthy men. J Clin Psychopharmacol. 2007. https://doi.org/10.1097/jcp.0b013e31815a23c2 .
Beck A, Wart C, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry. 1961;4:561–71.
pubmed: 13688369
pmcid: 13688369
doi: 10.1001/archpsyc.1961.01710120031004
Spielberger C, Gorsuch R, Lushene R. STAI manual. Palo Alto, CA: Consulting Psychologists Press; 1970.
Hirschfeld RMA, Williams JBW, Spitzer RL, Calabrese JR, Flynn L, Keck J, et al. Development and validation of a screening instrument for bipolar spectrum disorder: the mood disorder questionnaire. Am J Psychiatry. 2000. https://doi.org/10.1176/appi.ajp.157.11.1873 .
Price J, Cole V, Doll H, Goodwin GM. The Oxford Questionnaire on the emotional side-effects of antidepressants (OQuESA): development, validity, reliability and sensitivity to change. J Affect Disord. 2012. https://doi.org/10.1016/j.jad.2012.01.030 .
Nelson H, Willison J. The revised national adult reading test–test manual. Windsor, UK: NFER-Nelson; 1991.
Eysenck H, Eysenck S. Manual of the Eysenck personality questionnaire (junior and adult). Sevenoaks: Hodder and Stoughton; 1975.
von Zerssen D, Strian F, Schwarz D. Evaluation of depressive states, especially in longitudinal studies. In: Pichot P, Olivier-Martin R, editors. Psychological measurements in psychopharmacology. 7th ed. Basel, Karger; 1974. p. 189–202.
Watson D, Clark LA, Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS Scales. J Personal Soc Psychol. 1988. https://doi.org/10.1037/0022-3514.54.6.1063 .
Bond A, Lader M. The use of analogue scales in rating subjective feelings. Br J Med Psychol. 1974;47:211–8.
doi: 10.1111/j.2044-8341.1974.tb02285.x
Murphy SE, Norbury R, O’Sullivan U, Cowen PJ, Harmer CJ. Effect of a single dose of citalopram on amygdala response to emotional faces. Br J Psychiatry. 2009;194:535–40.
pubmed: 19478294
pmcid: 2802527
doi: 10.1192/bjp.bp.108.056093
Deichmann R, Gottfried JA, Hutton C, Turner R. Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage. 2003. https://doi.org/10.1016/S1053-8119(03)00073-9 .
Gläscher JP, O’Doherty JP. Model-based approaches to neuroimaging: combining reinforcement learning theory with fMRI data. Wiley Interdiscip Rev Cognit Sci. 2010;1:501–10.
doi: 10.1002/wcs.57
Rescorla R, Wagner AA. Theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Classical conditioning II current research and theory, Vol. 2. New York: Appleton-Century-Crofts, Meredith Corporation; 1972.
Zhang Y, Brady M, Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging. 2001;20:45–57.
pubmed: 11293691
doi: 10.1109/42.906424
pmcid: 11293691
Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17:143–55.
pubmed: 12391568
pmcid: 6871816
doi: 10.1002/hbm.10062
Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17:825–41.
pubmed: 12377157
doi: 10.1006/nimg.2002.1132
pmcid: 12377157
Beckmann CF, Smith SM. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging. 2004;23:137–52.
pubmed: 14964560
doi: 10.1109/TMI.2003.822821
pmcid: 14964560
Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Med Image Anal. 2001;5:143–56.
pubmed: 11516708
doi: 10.1016/S1361-8415(01)00036-6
pmcid: 11516708
Andersson JLR, Jenkinson M, Smith S. Non-linear registration, aka spatial normalisation. FMRIB Tech Rep TR07JA2. 2010.
Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL, et al. The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage. 2013;80:105–24.
pubmed: 23668970
pmcid: 3720813
doi: 10.1016/j.neuroimage.2013.04.127
Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage. 2012;62:782–90.
pubmed: 21979382
doi: 10.1016/j.neuroimage.2011.09.015
pmcid: 21979382
Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, et al. Bayesian analysis of neuroimaging data in FSL. Neuroimage. 2009;45:S173–86.
pubmed: 19059349
doi: 10.1016/j.neuroimage.2008.10.055
pmcid: 19059349
Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE. Permutation inference for the general linear model. Neuroimage. 2014;92:381–97.
pubmed: 24530839
pmcid: 4010955
doi: 10.1016/j.neuroimage.2014.01.060
Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2009;44:83–98.
pubmed: 18501637
doi: 10.1016/j.neuroimage.2008.03.061
pmcid: 18501637
Lenhard W, Lenhard A. Calculation of effect sizes; Retrieved from: https://www.psychometrica.de/effect_size.html . Dettelbach (Germany): Psychometrica. 2016. https://doi.org/10.13140/RG.2.2.17823.92329 .
Mai JK, Majtanik M, Paxinos G. Atlas of the human brain, 4th ed. Cambridge: Academic Press; 2015.
Seger CA, Cincotta CM. The roles of the caudate nucleus in human classification learning. J Neurosci. 2005;25:2941–51.
pubmed: 15772354
pmcid: 6725143
doi: 10.1523/JNEUROSCI.3401-04.2005
Scholl J, Kolling N, Nelissen N, Browning M, Rushworth MFS, Harmer CJ. Beyond negative valence: 2-week administration of a serotonergic antidepressant enhances both reward and effort learning signals. PLoS Biol. 2017;15:e2000756.
pubmed: 28207733
pmcid: 5331946
doi: 10.1371/journal.pbio.2000756
Srinivasan R, Fornari E, Knyazeva MG, Meuli R, Maeder P. fMRI responses in medial frontal cortex that depend on the temporal frequency of visual input. Exp Brain Res. 2007;180:677–91.
pubmed: 17297549
pmcid: 2084393
doi: 10.1007/s00221-007-0886-3
Knutson B, Heinz A. Probing psychiatric symptoms with the monetary incentive delay task. Biol Psychiatry. 2015;77:418–20.
pubmed: 25645271
doi: 10.1016/j.biopsych.2014.12.022
pmcid: 25645271
Wilson RP, Colizzi M, Bossong MG, Allen P, Kempton M, Abe N, et al. The neural substrate of reward anticipation in health: a meta-analysis of fMRI findings in the monetary incentive delay task. Neuropsychol Rev. 2018;28:496–506.
pubmed: 30255220
pmcid: 6327084
doi: 10.1007/s11065-018-9385-5
Graf H, Metzger CD, Walter M, Abler B. Serotonergic antidepressants decrease hedonic signals but leave learning signals in the nucleus accumbens unaffected. Neuroreport. 2016. https://doi.org/10.1097/WNR.0000000000000487 .
McCabe C, Mishor Z, Cowen PJ, Harmer CJ. Diminished neural processing of aversive and rewarding stimuli during selective serotonin reuptake inhibitor treatment. Biol Psychiatry. 2010. https://doi.org/10.1016/j.biopsych.2009.11.001 .
Ikeda Y, Funayama T, Tateno A, Fukayama H, Okubo Y, Suzuki H. Bupropion increases activation in nucleus accumbens during anticipation of monetary reward. Psychopharmacology. 2019. https://doi.org/10.1007/s00213-019-05337-6 .
Admon R, Kaiser RH, Dillon DG, Beltzer M, Goer F, Olson DP, et al. Dopaminergic enhancement of striatal response to reward in major depression. Am J Psychiatry. 2017. https://doi.org/10.1176/appi.ajp.2016.16010111 .
Wang C, Xu P, Zhang L, Huang J, Zhu K, Luo C. Current strategies and applications for precision drug design. Front Pharmacol. 2018;9:787.
pubmed: 30072901
pmcid: 6060444
doi: 10.3389/fphar.2018.00787
Bell EC, Willson MC, Wilman AH, Dave S, Silverstone PH. Differential effects of chronic lithium and valproate on brain activation in healthy volunteers. Hum Psychopharmacol. 2005;20:415–24.
pubmed: 16106488
doi: 10.1002/hup.710
pmcid: 16106488
Moore GJ, Bebchuk JM, Wilds IB, Chen G, Menji HK. Lithium-induced increase in human brain grey matter. Lancet. 2000;356:1241–2.
pubmed: 11072948
doi: 10.1016/S0140-6736(00)02793-8
pmcid: 11072948
Sassi RB, Nicoletti M, Brambilla P, Mallinger AG, Frank E, Kupfer DJ, et al. Increased gray matter volume in lithium-treated bipolar disorder patients. Neurosci Lett. 2002;329:243–5.
pubmed: 12165422
doi: 10.1016/S0304-3940(02)00615-8
pmcid: 12165422
Bearden CE, Thompson PM, Dalwani M, Hayashi KM, Lee AD, Nicoletti M, et al. Greater cortical gray matter density in lithium-treated patients with bipolar disorder. Biol Psychiatry. 2007;62:7–16.
pubmed: 17240360
pmcid: 3586797
doi: 10.1016/j.biopsych.2006.10.027
Phatak P, Shaldivin A, King LS, Shapiro P, Regenold WT. Lithium and inositol: effects on brain water homeostasis in the rat. Psychopharmacology. 2006;186:41–7.
pubmed: 16572264
doi: 10.1007/s00213-006-0354-y
pmcid: 16572264
Wu CC, Samanez-Larkin GR, Katovich K, Knutson B. Affective traits link to reliable neural markers of incentive anticipation. Neuroimage. 2014;84:279–89.
pubmed: 24001457
doi: 10.1016/j.neuroimage.2013.08.055
pmcid: 24001457
Plichta MM, Schwarz AJ, Grimm O, Morgen K, Mier D, Haddad L, et al. Test–retest reliability of evoked BOLD signals from a cognitive–emotive fMRI test battery. Neuroimage. 2012;60:1746–58.
pubmed: 22330316
doi: 10.1016/j.neuroimage.2012.01.129
pmcid: 22330316
Tivarus ME, Pester B, Schmidt C, Lehmann T, Zhu T, Zhong J, et al. Are structural changes induced by lithium in the HIV brain accompanied by changes in functional connectivity? PLoS ONE. 2015;10:e0139118.
pubmed: 26436895
pmcid: 4593570
doi: 10.1371/journal.pone.0139118
Vernon AC, Hajek T. Effects of lithium on magnetic resonance imaging signal might not preclude increases in brain volume after chronic lithium treatment. Biol Psychiatry. 2013;74:e39–40.
pubmed: 23998561
doi: 10.1016/j.biopsych.2012.12.028
pmcid: 23998561