Abstract
Reward motivation in individuals with high levels of negative schizotypal traits (NS) has been found to be lower than that in their counterparts. But it is unclear that whether their reward motivation adaptively changes with external effort-reward ratio, and what resting-state functional connectivity (rsFC) is associated with this change. Thirty-five individuals with high levels of NS and 44 individuals with low levels of NS were recruited. A 3T resting-state functional brain scan and a novel reward motivation adaptation behavioural task were administrated in all participants. The behavioural task was manipulated with three conditions (effort > reward condition vs. effort < reward condition vs. effort = reward condition). Under each condition were rated ‘wanting’ and ‘liking’ for rewards. The seed-based voxel-wise rsFC analysis was conducted to explore the rsFCs associated with the ‘wanting’ and ‘liking’ ratings in individuals with high levels of NS. ‘Wanting’ and ‘liking’ ratings of individuals with high levels of NS significantly declined in the effort > reward condition but did not rebound as high as their counterparts in the effort < reward condition. The rsFCs in NS group associated with these ratings were altered. The altered rsFCs in NS group involved regions in the prefrontal lobe, dopaminergic brain regions (ventral tegmental area, substantia nigra), hippocampus, thalamus and cerebellum. Individuals with high levels of NS manifested their reward motivation adaptation impairment as a failure of adjustment adaptively during effort-reward imbalance condition and altered rsFCs in prefrontal, dopaminergic and other brain regions.
Similar content being viewed by others
Data availability
Data could be available if emailing the correspondence author.
References
Abbasi Sarajehlou S, Khajeh S, Masrour C, Azizi M (2023) Comparison of executive functions in individuals with high and low levels of schizotypal trait. Front Psychol 27(13):1071777. https://doi.org/10.3389/fpsyg.2022.1071777
Adrián-Ventura J, Costumero V, Parcet MA, Avila C (2019) Reward network connectivity “at rest” is associated with reward sensitivity in healthy adults: a resting-state fMRI study. Cogn Affect Behav Neurosci 19(3):726–736. https://doi.org/10.3758/s13415-019-00688-1
Arias-Carrión O, Pŏppel E (2007) Dopamine, learning, and reward-seeking behavior. Acta Neurobiol Exp 67(4):481–488
Ashburner J, Barnes G, Chen C-C, Daunizeau J, Flandin G, Friston K (2016) SPM 12 manual. http://www.fil.ion.ucl.ac.uk/spm/doc/manual.pdf
Barch DM, Dowd EC (2010) Goal representations and motivational drive in schizophrenia: the role of prefrontal–striatal interactions. Schizophr Bull 36(5):919–934. https://doi.org/10.1093/schbul/sbq068
Bohon C, Stice E, Spoor S (2009) Female emotional eaters show abnormalities in consummatory and anticipatory food reward: a functional magnetic resonance imaging study. Int J Eat Disord 42(3):210–221. https://doi.org/10.1002/eat.20615
Cai XL, Weigl M, Liu BH, Cheung EFC, Ding JH, Chan RCK (2019) Delay discounting and affective priming in individuals with negative schizotypy. Schizophr Res 210:180–187. https://doi.org/10.1016/j.schres.2018.12.040
Chan RC, Wang Y, Yan C, Zhao Q, McGrath J, Hsi X, Stone WS (2012) A study of trait anhedonia in non-clinical Chinese samples: evidence from the Chapman scales for physical and social anhedonia. PLoS ONE 7(4):e34275. https://doi.org/10.1371/journal.pone.0034275
Chapman LJ, Chapman JP (1983) Infrequency Scale. Unpublished test
Chapman LJ, Chapman JP, Raulin ML (1976) Scales for physical and social anhedonia. J Abnorm Psychol 85(4):374–382. https://doi.org/10.1037//0021-843x.85.4.374
Chen GM, Zhao LP, Jia YB, Zhong SM, Chen F, Luo XM, Wang Y (2019) Abnormal cerebellum-DMN regions connectivity in unmedicated bipolar II disorder. J Affect Disord 243:441–447. https://doi.org/10.1016/j.jad.2018.09.076
Dobryakova E, DeLuca J, Genova HM, Wylie GR (2013) Neural correlates of cognitive fatigue: cortico-striatal circuitry and effort-reward imbalance. J Int Neuropsychol Soc JINS 19(8):849–853. https://doi.org/10.1017/S1355617713000684
Düzel E, Bunzeck N, Guitart-Masip M, Wittmann B, Schott BH, Tobler PN (2009) Functional imaging of the human dopaminergic midbrain. Trends Neurosci 32(6):321–328. https://doi.org/10.1016/j.tins.2009.02.005
Haber SN (2016) Corticostriatal circuitry. Dialogues Clin Neurosci 18(1):7–21. https://doi.org/10.31887/DCNS.2016.18.1/shaber
Horan WP, Brown SA, Blanchard JJ (2007) Social anhedonia and schizotypy: the contribution of individual differences in affective traits, stress, and coping. Psychiatry Res 149(1–3):147–156. https://doi.org/10.1016/j.psychres.2006.06.002
Kemp KC, Gross GM, Barrantes-Vidal N, Kwapil TR (2018) Association of positive, negative, and disorganized schizotypy dimensions with affective symptoms and experiences. Psychiatry Res 270:1143–1149. https://doi.org/10.1016/j.psychres.2018.10.031
Kwapil TR, Kemp KC, Mielock A, Sperry SH, Chun CA, Gross GM, Barrantes-Vidal N (2020) Association of multidimensional schizotypy with psychotic-like experiences, affect, and social functioning in daily life: comparable findings across samples and schizotypy measures. J Abnorm Psychol 129(5):492–504. https://doi.org/10.1037/abn0000522
Kwon HG, Jang SH (2014) Differences in neural connectivity between the substantia nigra and ventral tegmental area in the human brain. Front Hum Neurosci 8:41. https://doi.org/10.3389/fnhum.2014.00041
Laricchiuta D, Petrosini L, Picerni E, Cutuli D, Iorio M, Chiapponi C, Caltagirone C, Piras F, Spalletta G (2015) The embodied emotion in cerebellum: a neuroimaging study of alexithymia. Brain Struct Funct 220(4):2275–2287. https://doi.org/10.1007/s00429-014-0790-0
Llerena K, Park SG, McCarthy JM, Couture SM, Bennett ME, Blanchard JJ (2013) The Motivation and Pleasure Scale-Self-Report (MAP-SR): reliability and validity of a self-report measure of negative symptoms. Compr Psychiatry 54(5):568–574. https://doi.org/10.1016/j.comppsych.2012.12.001
Lopez-Gamundi P, Wardle MC (2018) The cognitive effort expenditure for rewards task (C-EEfRT): a novel measure of willingness to expend cognitive effort. Psychol Assess 30(9):1237–1248. https://doi.org/10.1037/pas0000563
McCarthy JM, Treadway MT, Blanchard JJ (2015) Motivation and effort in individuals with social anhedonia. Schizophr Res 165(1):70–75. https://doi.org/10.1016/j.schres.2015.03.030
Miller AB, Lenzenweger MF (2012) Schizotypy, social cognition, and interpersonal sensitivity. Personal Disord 3(4):379–392. https://doi.org/10.1037/a0027955
Murty VP, Shermohammed M, Smith DV, Carter RM, Huettel SA, Adcock RA (2014) Resting state networks distinguish human ventral tegmental area from substantia nigra. Neuroimage 100:580–589. https://doi.org/10.1016/j.neuroimage.2014.06.047
O’Doherty JP (2011) Contributions of the ventromedial prefrontal cortex to goal-directed action selection. Ann N Y Acad Sci 1239:118–129. https://doi.org/10.1111/j.1749-6632.2011.06290.x
Olivito G, Lupo M, Iacobacci C, Clausi S, Romano S, Masciullo M, Molinari M, Cercignani M, Bozzali M, Leggio M (2018) Structural cerebellar correlates of cognitive functions in spinocerebellar ataxia type 2. J Neurol 265(3):597–606. https://doi.org/10.1007/s00415-018-8738-6
Peters SK, Dunlop K, Downar J (2016) Cortico-striatal-thalamic loop circuits of the salience network: a central pathway in psychiatric disease and treatment. Front Syst Neurosci 10:104. https://doi.org/10.3389/fnsys.2016.00104
Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59(3):2142–2154. https://doi.org/10.1016/j.neuroimage.2011.10.018
Premkumar P, Williams SC, Lythgoe D, Andrew C, Kuipers E, Kumari V (2013) Neural processing of criticism and positive comments from relatives in individuals with schizotypal personality traits. World J Biol Psychiatry 14(1):57–70. https://doi.org/10.3109/15622975.2011.604101
Pruessner M, Cullen AE, Aas M, Walker EF (2017) The neural diathesis-stress model of schizophrenia revisited: an update on recent findings considering illness stage and neurobiological and methodological complexities. Neurosci Biobehav Rev 73:191–218. https://doi.org/10.1016/j.neubiorev.2016.12.013
Reddy LF, Horan WP, Barch DM, Buchanan RW, Dunayevich E, Gold JM, Green MF (2015) Effort-based decision-making paradigms for clinical trials in schizophrenia: part 1-psychometric characteristics of 5 paradigms. Schizophr Bull 41(5):1045–1054. https://doi.org/10.1093/schbul/sbv089
Rolls ET (2015) Limbic systems for emotion and for memory, but no single limbic system. Cortex 62:119–157. https://doi.org/10.1016/j.cortex.2013.12.005
Schifani C, Tseng HH, Kenk M, Tagore A, Kiang M, Wilson AA, Mizrahi R (2018) Cortical stress regulation is disrupted in schizophrenia but not in clinical high risk for psychosis. Brain 141(7):2213–2224. https://doi.org/10.1093/brain/awy133
Schmahmann JD (2019) The cerebellum and cognition. Neurosci Lett 688:62–75. https://doi.org/10.1016/j.neulet.2018.07.005
Stoodley CJ, Schmahmann JD (2009) Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 44(2):489–501. https://doi.org/10.1016/j.neuroimage
Studer B, Knecht S (2016) A benefit-cost framework of motivation for a specific activity. Prog Brain Res 229:25–47. https://doi.org/10.1016/bs.pbr.2016.06.014
Treadway MT, Buckholtz JW, Schwartzman AN, Lambert WE, Zald DH (2009) Worth the “EEfRT”? The effort expenditure for rewards task as an objective measure of motivation and anhedonia. PLoS ONE 4(8):e6598. https://doi.org/10.1371/journal.pone.0006598
Treadway MT, Zald DH (2011) Reconsidering anhedonia in depression: lessons from translational neuroscience. Neurosci Biobehav Rev 35(3):537–555. https://doi.org/10.1016/j.neubiorev.2010.06.006
Tseng HH, Watts JJ, Kiang M, Suridjan I, Wilson AA, Houle S, Mizrahi R (2018) Nigral stress-induced dopamine release in clinical high risk and antipsychotic-naive schizophrenia. Schizophr Bull 44(3):542–551. https://doi.org/10.1093/schbul/sbx042
Walker EF, Diforio D (1997) Schizophrenia: a neural diathesis-stress model. Psychol Rev 104(4):667–685. https://doi.org/10.1037/0033-295x.104.4.667
Walker E, Mittal V, Tessner K (2008) Stress and the hypothalamic pituitary adrenal axis in the developmental course of schizophrenia. Annu Rev Clin Psychol 4:189–216. https://doi.org/10.1146/annurev.clinpsy.4.022007.141248
Walton ME, Bannerman DM, Alterescu K, Rushworth MF (2003) Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. J Neurosci 23(16):6475–6479. https://doi.org/10.1523/JNEUROSCI.23-16-06475.2003
Wang J, Huang J, Yang XH, Lui SS, Cheung EF, Chan RC (2015) Anhedonia in schizophrenia: deficits in both motivation and hedonic capacity. Schizophr Res 168(1–2):465–474. https://doi.org/10.1016/j.schres.2015.06.019
Wang LL, Ma EPY, Lui SSY, Cheung EFC, Cheng KS, Chan RCK (2020) Validation and extension of the Motivation and Pleasure Scale-Self Report (MAP-SR) across the schizophrenia spectrum in the Chinese context. Asian J Psychiatr 49:101971. https://doi.org/10.1016/j.ajp.2020.101971
Wang Y, Liu WH, Li Z, Wei XH, Jiang XQ, Geng FL, Chan RCK (2016) Altered corticostriatal functional connectivity in individuals with high social anhedonia. Psychol Med 46(1):125–135. https://doi.org/10.1017/S0033291715001592
Wang Y, Yan C, Yin DZ, Fan MX, Cheung EF, Pantelis C, Chan RCK (2015) Neurobiological changes of schizotypy: evidence from both volume-based morphometric analysis and resting-state functional connectivity. Schizophr Bull 41(Suppl 2):S444-454. https://doi.org/10.1093/schbul/sbu178
Waugh CE, Gotlib IH (2008) Motivation for reward as a function of required effort: dissociating the ‘liking’ from the ‘wanting’ system in humans. Motiv Emot 32(4):323–330. https://doi.org/10.1007/s11031-008-9104-2
Williams CJ, Dziurawiec S, Heritage B (2018) More pain than gain: effort–reward imbalance, burnout, and withdrawal intentions within a university student population. J Educ Psychol 110(3):378–394. https://doi.org/10.1037/edu0000212
Wolf DH, Satterthwaite TD, Kantrowitz JJ, Katchmar N, Vandekar L, Elliott MA, Ruparel K (2014) Amotivation in schizophrenia: integrated assessment with behavioral, clinical, and imaging measures. Schizophr Bull 40(6):1328–1337. https://doi.org/10.1093/schbul/sbu026
Xie DJ, Shi HS, Lui S, Shi C, Li Y, Ho K, Hung K, Li WX, Yi ZH, Cheung E, Kring AM, Chan RCK (2018) Cross cultural validation and extension of the clinical assessment interview for negative symptoms (CAINS) in the Chinese context: evidence from a spectrum perspective. Schizophr Bull 44(suppl 2):S547–S555. https://doi.org/10.1093/schbul/sby013
Xie WZ, Yan C, Ying XY, Zhu SY, Shi HS, Wang Y, Chan RCK (2014) Domain-specific hedonic deficits towards social affective but not monetary incentives in social anhedonia. Sci Rep 4:4056. https://doi.org/10.1038/srep04056
Yan C, Lui S, Zou LQ, Wang CY, Zhou FC, Cheung E, Shum D, Chan RCK (2019) Anticipatory pleasure for future rewards is attenuated in patients with schizophrenia but not in individuals with schizotypal traits. Schizophr Res 206:118–126. https://doi.org/10.1016/j.schres.2018.12.003
Yan C, Wang Y, Su L, Xu T, Yin DZ, Fan MX, Chan RCK (2016) Differential mesolimbic and prefrontal alterations during reward anticipation and consummation in positive and negative schizotypy. Psychiatry Res Neuroimaging 254:127–136. https://doi.org/10.1016/j.pscychresns.2016.06.014
Yan CG, Cheung B, Kelly C, Colcombe S, Craddock RC, Di Martino A, Milham MP (2013) A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage 76:183–201. https://doi.org/10.1016/j.neuroimage.2013.03.004
Yan CG, Zang YF (2010) DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4(13):1–7. https://doi.org/10.3389/fnsys.2010.00013
Yan YJ, Hu HX, Wang LL, Zhang YJ, Lui SSY, Huang J, Chan RCK (2023) Negative schizotypal traits predict the reduction of reward motivation in effort-reward imbalance. Eur Arch Psychiatry Clin Neurosci 273(2):439–445. https://doi.org/10.1007/s00406-022-01419-3
Yang ZY, Zhang RT, Wang YM, Huang J, Zhou HY, Cheung EFC, Chan RCK (2021) Altered activation and functional connectivity in individuals with social anhedonia when envisioning positive future episodes. Psychol Med. https://doi.org/10.1017/S0033291721000970
Zhang P, Liu Y, Yu FX, Wu GW, Li MY, Wang Z, Wang ZC (2021) Hierarchical integrated processing of reward-related regions in obese males: a graph-theoretical-based study. Appetite 159:105055. https://doi.org/10.1016/j.appet.2020.105055
Zhang RT, Zhou HY, Wang YM, Yang ZY, Wang Y, So SH, Chan RCK (2019) Network analysis of schizotypal personality traits and their association with other subclinical psychiatric features. Asian J Psychiatr 44:209–216. https://doi.org/10.1016/j.ajp.2019.08.005
Zhang S, Ide JS, Li CS (2012) Resting-state functional connectivity of the medial superior frontal cortex. Cereb Cortex 22(1):99–111. https://doi.org/10.1093/cercor/bhr088
Acknowledgements
This study was supported by the CAS Key Laboratory of Mental Health, Institute of Psychology, the Scientific Foundation of Institute of Psychology, Chinese Academy of Sciences (E2CX3415CX), and Philip K. H. Wong Foundation. We also thank Miss Hui Wang for her help in revision editing.
Author information
Authors and Affiliations
Contributions
Y-jY conceptualization, methodology, software, data collection and analysis, writing-original draft preparation. H-xH, Y-jZ, L-lW, Y-mP data collection. SSYL writing-reviewing and editing. JH conceptualization, methodology, supervision, writing-reviewing and editing. RCKC conceptualization, supervision, writing- reviewing and editing.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that there are no conflicts of interest.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yan, Yj., Hu, Hx., Zhang, Yj. et al. Reward motivation adaptation in people with negative schizotypal features: development of a novel behavioural paradigm and identifying its neural correlates using resting-state functional connectivity analysis. Eur Arch Psychiatry Clin Neurosci (2023). https://doi.org/10.1007/s00406-023-01640-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00406-023-01640-8