Abstract
Both positive psychotic symptoms and anhedonia are associated with striatal functioning, but few studies have linked risk for psychotic disorders to a neural measure evoked during a striatal dopamine-related reward and punishment-based learning task, such as a reversal learning task (RLT; Cools et al, 2009). The feedback-related negativity (FRN) is a neural response that in part reflects striatal dopamine functioning. We recorded EEG during the RLT in three groups: (a) people with psychotic experiences (PE; n=20) at increased risk for psychotic disorders; (b) people with extremely elevated social anhedonia (SocAnh; n=22); and (c) controls (n=20). Behaviorally, consistent with increased striatal dopamine, the PE group exhibited better behavioral learning (ie, faster responses) after unexpected reward than after unexpected punishment. Moreover, although the control and SocAnh groups showed a larger FRN to punishment than reward, the PE group showed similar FRNs to punishment and reward, with a numerically larger FRN to reward than punishment (with similar results on these trials also found for a P3a component). These results are among the first to link a neural response evoked by a reward and punishment-based learning task specifically with elevated psychosis risk.
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References
Baker TE, Holroyd CB (2011). Dissociated roles of the anterior cingulate cortex in reward and conflict processing as revealed by the feedback error-related negativity and N200. Biol Psychol 87: 25–34.
Bates DM (2010). lme4: Mixed-effects modeling with R. Retrieved from http://lme4.r-forge.r-project.org/lMMwR/lrgprt.pdf.
Becker MP, Nitsch AM, Miltner WH, Straube T (2014). A single-trial estimation of the feedback-related negativity and its relation to BOLD responses in a time-estimation task. J Neurosci 34: 3005–3012.
Bismark AW, Hajcak G, Whitworth NM, Allen JJ (2013). The role of outcome expectations in the generation of the feedback‐related negativity. Psychophysiology 50: 125–133.
Carlson JM, Foti D, Mujica-Parodi LR, Harmon-Jones E, Hajcak G (2011). Ventral striatal and medial prefrontal BOLD activation is correlated with reward-related electrocortical activity: a combined ERP and fMRI study. Neuroimage 57: 1608–1616.
Chapman LJ, Chapman JP, Kwapil TR, Eckblad M, Zinser MC (1994). Putatively psychosis-prone subjects 10 years later. J Abnorm Psychol 103: 171–183.
Chapman LJ, Chapman JP, Raulin ML (1978). Body-image aberration in schizophrenia. J Abnorm Psychol 87: 399–407.
Collins AG, Frank MJ (2014). Opponent actor learning (OpAL): modeling interactive effects of striatal dopamine on reinforcement learning and choice incentive. Psychol Rev 121: 337–366.
Cools R, Frank MJ, Gibbs SE, Miyakawa A, Jagust W, D’Esposito M (2009). Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. J Neurosci 29: 1538–1543.
Debbané M, Eliez S, Badoud D, Conus P, Flückiger R, Schultze-Lutter F (2015). Developing psychosis and its risk states through the lens of schizotypy. Schizophr Bull 41: S396–S407.
Demjaha A, Murray RM, McGuire PK, Kapur S, Howes OD (2012). Dopamine synthesis capacity in patients with treatment-resistant schizophrenia. Am J Psychiatry 169: 1203–1210.
Dowd EC, Barch DM (2012). Pavlovian reward prediction and receipt in schizophrenia: relationship to anhedonia. PLoS ONE 7: e35622.
Eckblad M, Chapman LJ (1983). Magical ideation as an indicator of schizotypy. J Consult Clin Psychol 51: 215–225.
Eckblad M, Chapman LJ, Chapman JP, Mishlove M (1982). The revised social anhedonia scale. Unpublished test, University of Wisconsin, Madison, WI.
Evans DE, Maxfield ND, Van Rensburg KJ, Oliver JA, Jentink KG, Drobes DJ (2013). Nicotine deprivation influences P300 markers of cognitive control. Neuropsychopharmacology 38: 2525–2531.
Frank MJ, Seeberger LC, O'Reilly RC (2004). By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 306: 1940–1943.
Gratton G (2007) Biosignal processing. In: Cacioppo J, Tassinary L, Berntson G (eds). Handbook of Psychophysiology. Cambridge University Press: New York. pp 900–923.
Holroyd CB, Coles MG (2002). The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol Rev 109: 679–709.
Holroyd CB, Nieuwenhuis S, Yeung N, Cohen JD (2003). Errors in reward prediction are reflected in the event-related brain potential. Neuroreport 14: 2481–2484.
Howes O, Kapur S (2009). The dopamine hypothesis of schizophrenia: Version III—The final common pathway. Schizophr Bull 35: 549–562.
Jennings JR, Wood CC (1976). The e-adjustment procedure for repeated-measures analyses of variance. Psychophysiology 76: 277–278.
Juckel G, Schlagenhauf F, Koslowski M, Wustenberg T, Villringer A, Knutson B et al (2006). Dysfunction of ventral striatal reward prediction in schizophrenia. Neuroimage 29: 409–416.
Karcher NR, Cicero D, Kerns JG (2015a). An experimental examination of the aberrant salience hypothesis using a salience manipulation and a behavioral magical thinking task. J Exp Psychopathol 6: 297–312.
Karcher NR, Martin EA, Kerns JG (2015b). Examining associations between psychosis risk, social anhedonia, and performance of striatum-related behavioral tasks. J Abnorm Psychol 124: 507–518.
Kaymaz N, Drukker M, Lieb R, Wittchen HU, Werbeloff N, Weiser M et al (2012). Do subthreshold psychotic experiences predict clinical outcomes in unselected non-help-seeking population-based samples? A systematic review and meta-analysis, enriched with new results. Psychol Med 42: 2239–2253.
Luck SJ (2005) An Introduction to the Event-Related Potential Technique. MIT Press: Cambridge.
Miller TJ, McGlashan TH, Rosen JL, Cadenhead K, Cannon T, Ventura J et al (2003). Prodromal assessment with the structured interview for prodromal syndromes and the scale of prodromal symptoms: predictive validity, interrater reliability, and training to reliability. Schizophr Bull 29: 703–715.
Nieuwenhuis S, Slagter HA, von Geusau NJ, Heslenfeld DJ, Holroyd CB (2005). Knowing good from bad: differential activation of human cortical areas by positive and negative outcomes. Eur J Neurosci 21: 3161–3168.
Padrao G, Mallorqui A, Cucurell D, Marco-Pallares J, Rodriguez-Fornells A (2013). Neurophysiological differences in reward processing in anhedonics. Cogn Affect Behav Neurosci 13: 102–115.
Page-Gould E Multilevel modeling . Cacioppo JT, Tassinary L, Berntson G (eds). The Handbook of Psychophysiology (in press)4th edn. Cambridge University Press: New York.
Pfabigan DM, Seidel EM, Paul K, Grahl A, Sailer U, Lanzenberger R et al (2015). Context-sensitivity of the feedback-related negativity for zero-value feedback outcomes. Biol Psychol 104: 184–192.
Polich J (2007). Updating P300: An integrative theory of P3a and P3b. Clin Neurophysiol 118: 2128–2148.
Proudfit GH (2015). The reward positivity: From basic research on reward to a biomarker for depression. Psychophysiology 52: 449–459.
Psychology Software Tools, Inc. (2006). E-prime v. 2.0. Pittsburg, PA.
Santesso DL, Evins AE, Frank MJ, Schetter EC, Bogdan R, Pizzagalli DA (2009). Single dose of a dopamine agonist impairs reinforcement learning in humans: evidence from event-related potentials and computational modeling of striatal-cortical function. Hum Brain Mapp 30: 1963–1976.
Smillie LD, Cooper AJ, Pickering AD (2011). Individual differences in reward-prediction-error: extraversion and feedback-related negativity. Soc Cogn Affect Neurosci 6: 646–652.
van der Schaaf ME, van Schouwenburg MR, Geurts DE, Schellekens AF, Buitelaar JK, Verkes RJ et al (2014). Establishing the dopamine dependency of human striatal signals during reward and punishment reversal learning. Cereb Cortex 24: 633–642.
von Borries AK, Verkes RJ, Bulten BH, Cools R, de Bruijn ER (2013). Feedback-related negativity codes outcome valence, but not outcome expectancy, during reversal learning. Cogn Affect Behav Neurosci 13: 737–746.
Wagshal D, Knowlton B, Cohen J, Poldrack R, Bookheimer S, Bilder R et al (2012). Deficits in probabilistic classification learning and liability for schizophrenia. Psychiatry Res 200: 167–172.
Walsh MM, Anderson JR (2012). Learning from experience: event-related potential correlates of reward processing, neural adaptation, and behavioral choice. Neurosci Biobehav Rev 36: 1870–1884.
Weickert TW, Goldberg TE, Egan MF, Apud JA, Meeter M, Myers CE et al (2010). Relative risk of probabilistic category learning deficits in patients with schizophrenia and their siblings. Biol Psychiatry 67: 948–955.
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Karcher, N., Bartholow, B., Martin, E. et al. Associations between Electrophysiological Evidence of Reward and Punishment-Based Learning and Psychotic Experiences and Social Anhedonia in At-Risk Groups. Neuropsychopharmacol 42, 925–932 (2017). https://doi.org/10.1038/npp.2016.192
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DOI: https://doi.org/10.1038/npp.2016.192
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