Hostname: page-component-745bb68f8f-mzp66 Total loading time: 0 Render date: 2025-01-07T09:17:13.823Z Has data issue: false hasContentIssue false
  • English
  • Français

Impaired neural response to internal but not external feedback in schizophrenia

Published online by Cambridge University Press:  08 December 2011

W. P. Horan ,
D. Foti ,
G. Hajcak ,
J. K. Wynn  and
M. F. Green
W. P. Horan*
Affiliation:
VA Greater Los Angeles Healthcare System, University of California, Los Angeles, CA, USA
D. Foti
Affiliation:
Stony Brook University, New York, NY, USA
G. Hajcak
Affiliation:
Stony Brook University, New York, NY, USA
J. K. Wynn
Affiliation:
VA Greater Los Angeles Healthcare System, University of California, Los Angeles, CA, USA
M. F. Green
Affiliation:
VA Greater Los Angeles Healthcare System, University of California, Los Angeles, CA, USA
*
*Address for correspondence: W. P. Horan, Ph.D., University of California, Los Angeles and VA Greater Los Angeles Healthcare System, MIRECC 210A, Bldg 210, 11301 Wilshire Blvd, Los Angeles, CA 90073, USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Accurate monitoring and integration of both internal and external feedback is crucial for guiding current and future behavior. These aspects of performance monitoring are commonly indexed by two event-related potential (ERP) components: error-related negativity (ERN) and feedback negativity (FN). The ERN indexes internal response monitoring and is sensitive to the commission of erroneous versus correct responses, and the FN indexes external feedback monitoring of positive versus negative outcomes. Although individuals with schizophrenia consistently demonstrate a diminished ERN, the integrity of the FN has received minimal consideration.

Method

The current research sought to clarify the scope of feedback processing impairments in schizophrenia in two studies: study 1 examined the ERN elicited in a flanker task in 16 out-patients and 14 healthy controls; study 2 examined the FN on a simple monetary gambling task in expanded samples of 35 out-patients and 33 healthy controls.

Results

Study 1 replicated prior reports of an impaired ERN in schizophrenia. By contrast, patients and controls demonstrated comparable FN differentiation between reward and non-reward feedback in study 2.

Conclusions

The differential pattern across tasks suggests that basic sensitivity to external feedback indicating reward versus non-reward is intact in schizophrenia, at least under the relatively simple task conditions used in this study. Further efforts to specify intact and impaired reward-processing subcomponents in schizophrenia may help to shed light on the diminished motivation and goal-seeking behavior that are commonly seen in this disorder.

Keywords

Error-related negativityevent-related potential (ERP)feedback negativityreward sensitivityschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 42 , Issue 8 , August 2012 , pp. 1637 - 1647
Copyright
Copyright © Cambridge University Press 2011

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

Alain, C, McNeely, HE, He, Y, Christensen, BK, West, R (2002). Neurophysiological evidence of error-monitoring deficits in patients with schizophrenia. Cerebral Cortex 12, 840–846.CrossRefGoogle ScholarPubMed
Andreasen, NC, Pressler, M, Nopoulos, P, Miller, D, Ho, BC (2010). Antipsychotic dose equivalents and dose-years: a standardized method for comparing exposure to different drugs. Biological Psychiatry 67, 255–262.CrossRefGoogle ScholarPubMed
Barch, DM, Dowd, EC (2010). Goal representations and motivational drive in schizophrenia: the role of prefrontal-striatal interactions. Schizophrenia Bulletin 36, 919–934.CrossRefGoogle ScholarPubMed
Blanchard, JJ, Kring, AM, Horan, WP, Gur, R (2011). Toward the next generation of negative symptom assessments: the collaboration to advance negative symptom assessment in schizophrenia. Schizophrenia Bulletin 37, 291–299.CrossRefGoogle Scholar
Burbach, JPH, van der Zwaag, B (2009). Contact in genetics of autism and schizophrenia. Trends in Neurosciences 32, 69–72.CrossRefGoogle ScholarPubMed
Burle, B, Roger, C, Allain, S, Vidal, F, Hasbroucq, T (2008). Error negativity does not reflect conflict: a reappraisal of conflict monitoring and anterior cingulate cortex activity. Journal of Cognitive Neuroscience 20, 1637–1655.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Carter, CS, MacDonald, AW, Ross, LL, Stenger, VA (2001). Anterior cingulate cortex activity and impaired self-monitoring of performance in patients with schizophrenia: an event-related fMRI study. American Journal of Psychiatry 158, 1423–1428.CrossRefGoogle ScholarPubMed
Eriksen, BA, Eriksen, CW (1974). Effects of noise letters on the identification of target letters in a non-search task. Perception and Psychophysics 16, 143–149.CrossRefGoogle Scholar
Falkenstein, M, Hohnsbein, J, Hoormann, J, Blanke, L (1990). Effects of errors in choice reaction tasks on the ERP under focused and divided attention. In Psychophysiological Brain Research (ed. Brunia, C. H. M., Gaillard, A. W. K. and Kok, A.), pp. 192–195. Tilburg University Press: Tilburg, The Netherlands.Google Scholar
First, MB, Gibbon, M, Spitzer, RL, Williams, JBW (1996). Structured Clinical Interview for DSM-IV Axis I Disorders. Patient Edition. Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW, Benjamin, L (1994). Structured Clinical Interview for DSM-IV Axis II Personality Disorders (Version 2.0). Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Foti, D, Hajcak, G (2009). Depression and reduced sensitivity to non-rewards versus rewards: evidence from event-related potentials. Biological Psychology 81, 1–8.CrossRefGoogle ScholarPubMed
Foti, D, Hajcak, G (2010). State sadness reduces neural sensitivity to nonrewards versus rewards. Neuroreport 21, 143–147.CrossRefGoogle ScholarPubMed
Foti, D, Weinberg, A, Dien, J, Hajcak, G (2011). Event-related potential activity in the basal ganglia differentiates rewards from nonrewards: temporospatial principal components analysis and source localization of the feedback negativity. Human Brain Mapping. Published online: 8 February 2011. doi: 10.1002/hbm.21182.Google ScholarPubMed
Gehring, WJ, Goss, B, Coles, MGH, Meyer, DE, Donchin, E (1993). A neural system for error detection and compensation. Psychological Science 4, 385–390.CrossRefGoogle Scholar
Gold, JM, Waltz, JA, Prentice, KJ, Morris, SE, Heerey, EA (2008). Reward processing in schizophrenia: a deficit in the representation of value. Schizophrenia Bulletin 34, 835–847.CrossRefGoogle ScholarPubMed
Gratton, G, Coles, MG, Donchin, E (1983). A new method for off-line removal of occular artifact. Electroencephalography and Clinical Neurophysiology 55, 468–484.CrossRefGoogle Scholar
Hajcak, G, Moser, JS, Holroyd, CB, Simons, RF (2006). The feedback-related negativity reflects the binary evaluation of good versus bad outcomes. Biological Psychology 71, 148–154.CrossRefGoogle ScholarPubMed
Hajcak, G, Moser, JS, Yeung, N, Simons, RF (2005). On the ERN and the significance of errors. Psychophysiology 42, 151–160.CrossRefGoogle ScholarPubMed
Holroyd, CB, Coles, MG (2002). The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychological Review 109, 679–709.CrossRefGoogle ScholarPubMed
Holroyd, CB, Pakzad-Vaezi, KL, Krigolson, OE (2008). The feedback correct-related positivity: sensitivity of the event-related brain potential to unexpected positive feedback. Psychophysiology 45, 688–697.CrossRefGoogle ScholarPubMed
Horan, WP, Wynn, JK, Kring, AM, Simons, RF, Green, MF (2010). Electrophysiological correlates of emotional responding in schizophrenia. Journal of Abnormal Psychology 119, 18–30.CrossRefGoogle ScholarPubMed
Juckel, G, Schlagenhauf, F, Koslowski, M, Filonov, D, Wustenberg, T, Villringer, A, Knutson, B, Kienast, T, Gallinat, J, Wrase, J, Heinz, A (2006 a). Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacology (Berlin) 187, 222–228.CrossRefGoogle Scholar
Juckel, G, Schlagenhauf, F, Koslowski, M, Wustenberg, T, Villringer, A, Knutson, B, Wrase, J, Heinz, A (2006 b). Dysfunction of ventral striatal reward prediction in schizophrenia. Neuroimage 29, 409–416.CrossRefGoogle ScholarPubMed
Koch, K, Schachtzabel, C, Wagner, G, Schikora, J, Schultz, C, Reichenbach, JR, Sauer, H, Schlosser, RGM (2010). Altered activation in association with reward-related trial-and-error learning in patients with schizophrenia. NeuroImage 50, 223–232.CrossRefGoogle ScholarPubMed
Kopelowicz, A, Ventura, J, Liberman, RP, Mintz, J (2008). Consistency of Brief Psychiatric Rating Scale factor structure across a broad spectrum of schizophrenia patients. Psychopathology 41, 77–84.CrossRefGoogle ScholarPubMed
Kring, AM, Moran, EK (2008). Emotional response deficits in schizophrenia: insights from affective science. Schizophrenia Bulletin 34, 819–834.CrossRefGoogle ScholarPubMed
Larson, MJ, South, M, Krauskopf, E, Clawson, A, Crowley, MJ (2011). Feedback and reward processing in high-functioning autism. Psychiatry Research 187, 198–203.CrossRefGoogle ScholarPubMed
Laurens, KR, Hodgins, S, Mould, GL, West, SA, Schoenberg, PLA, Murray, RM, Taylor, EA (2010). Error-related processing dysfunction in children aged 9 to 12 years presenting putative antecedents of schizophrenia. Biological Psychiatry 67, 238–245.CrossRefGoogle ScholarPubMed
Luck, SJ (2005). An Introduction to the Event-Related Potential Technique. MIT Press: Cambridge, MA.Google Scholar
Lukoff, D, Nuechterlein, KH, Ventura, J (1986). Manual for the expanded Brief Psychiatric Rating Scale. Schizophrenia Bulletin 12, 578–602.CrossRefGoogle Scholar
Mathalon, DH, Fedor, M, Faustman, WO, Gray, M, Askari, N, Ford, JM (2002 a). Response-monitoring dysfunction in schizophrenia: an event-related brain potential study. Journal of Abnormal Psychology 111, 22–41.CrossRefGoogle ScholarPubMed
Mathalon, DH, Jorgensen, KW, Roach, BJ, Ford, JM (2009). Error detection failures in schizophrenia: ERPs and FMRI. International Journal of Psychophysiology 73, 109–117.CrossRefGoogle ScholarPubMed
Mathalon, DH, Whitfield, SL, Gray, EM, Faustman, WO, Glover, G, Ford, JM (2002 b). Frontal lobe dysfunction and reduced error-related negativity in schizophrenia. Schizophrenia Research 53, 222.Google Scholar
Morris, SE, Heerey, EA, Gold, JA, Holroyd, CB (2008). Learning-related changes in brain activity following errors and performance feedback in schizophrenia. Schizophrenia Research 99, 274–285.CrossRefGoogle ScholarPubMed
Morris, SE, Yee, CM, Nuechterlein, KH (2006). Electrophysiological analysis of error monitoring in schizophrenia. Journal of Abnormal Psychology 115, 239–250.CrossRefGoogle ScholarPubMed
Nylander, L, Lugnegard, T, Hallerback, MU (2008). Autism spectrum disorders and schizophrenia spectrum disorders in adults – is there a connection? A literature review and some suggestions for future clinical research. Clinical Neuropsychiatry 5, 43–54.Google Scholar
Olvet, DM, Hajcak, G (2009). The stability of error-related brain activity with increasing trials. Psychophysiology 46, 957–961.CrossRefGoogle ScholarPubMed
Overall, JE, Gorham, DR (1962). The Brief Psychiatric Rating Scale. Psychological Reports 10, 799–812.CrossRefGoogle Scholar
Overbeek, TJM, Nieuwenhuis, S, Ridderinkhof, KR (2005). Dissociable components of error processing: on the functional significance of the Pe vis-à-vis the ERN/Ne. Journal of Psychophysiology 19, 319–329.CrossRefGoogle Scholar
Polli, FE, Barton, JJS, Thakkar, KN, Greve, DN, Goff, DC, Rauch, SL, Manoach, DS (2008). Reduced error-related activation in two anterior cingulate circuits is related to impaired performance in schizophrenia. Brain 131, 971–986.CrossRefGoogle ScholarPubMed
Ridderinkhof, KR, Ramautar, JR, Wijnen, JG (2009). To PE or not to PE: a P3-like ERP component reflecting the processing of response errors. Psychophysiology 46, 531–538.CrossRefGoogle ScholarPubMed
Sato, A, Yasuda, A, Ohira, H, Miyawaki, K, Nishikawa, M, Kumano, H, Kuboki, T (2005). Effects of value and reward magnitude on feedback negativity and P300. Neuroreport 16, 407–411.CrossRefGoogle ScholarPubMed
Schlagenhauf, F, Juckel, G, Koslowski, M, Kahnt, T, Knutson, B, Dembler, T, Kienast, T, Gallinat, J, Wrase, J, Heinz, A (2008). Reward system activation in schizophrenic patients switched from typical neuroleptics to olanzapine. Psychopharmacology (Berlin) 196, 673–684.CrossRefGoogle ScholarPubMed
Simons, RF (2010). The way of our errors: theme and variations. Psychophysiology 47, 1–14.CrossRefGoogle ScholarPubMed
Taylor, SF, Stern, ER, Gehring, WJ (2007). Neural systems for error monitoring: recent findings and theoretical perspectives. Neuroscientist 13, 160–172.CrossRefGoogle ScholarPubMed
van Veen, V, Carter, CS (2006). Error detection, correction, and prevention in the brain: a brief review of data and theories. Clinical EEG and Neuroscience 37, 330–335.CrossRefGoogle Scholar
Ventura, J, Green, MF, Shaner, A, Liberman, RP (1993). Training and quality assurance with the brief psychiatric rating scale: ‘The Drift Busters’. International Journal of Methods in Psychiatric Research 3, 221–224.Google Scholar
Ventura, J, Liberman, RP, Green, MF, Shaner, A (1998). Training and quality assurance with the Structured Clinical Interview for DSM-IV. Psychiatry Research 79, 163–173.CrossRefGoogle ScholarPubMed
Yeung, N, Sanfey, AG (2004). Independent coding of reward magnitude and valence in the human brain. Journal of Neuroscience 24, 6258–6264.CrossRefGoogle ScholarPubMed