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Neural correlates of error-related learning deficits in individuals with psychopathy

Published online by Cambridge University Press:  09 December 2009

A. K. L. von Borries ,
I. A. Brazil ,
B. H. Bulten ,
J. K. Buitelaar ,
R. J. Verkes  and
E. R. A. de Bruijn
A. K. L. von Borries*
Affiliation:
Radboud University Nijmegen Medical Centre, Donders Institute for Brain, Cognition and Behaviour, Department of Psychiatry, Nijmegen, The Netherlands Pompestichting, Nijmegen, The Netherlands
I. A. Brazil
Affiliation:
Pompestichting, Nijmegen, The Netherlands Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
B. H. Bulten
Affiliation:
Pompestichting, Nijmegen, The Netherlands
J. K. Buitelaar
Affiliation:
Radboud University Nijmegen Medical Centre, Donders Institute for Brain, Cognition and Behaviour, Department of Psychiatry, Nijmegen, The Netherlands
R. J. Verkes
Affiliation:
Radboud University Nijmegen Medical Centre, Donders Institute for Brain, Cognition and Behaviour, Department of Psychiatry, Nijmegen, The Netherlands Pompestichting, Nijmegen, The Netherlands
E. R. A. de Bruijn
Affiliation:
Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, The Netherlands
*
*Address for correspondence: A. K. L. von Borries, M.Sc., Pompekliniek, PO Box 31435, 6503CKNijmegen, The Netherlands. (Email: k.v.borries@pompestichting.nl)
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Abstract

Background

Psychopathy (PP) is associated with a performance deficit in a variety of stimulus–response and stimulus–reinforcement learning paradigms. We tested the hypothesis that failures in error monitoring underlie these learning deficits.

Method

We measured electrophysiological correlates of error monitoring [error-related negativity (ERN)] during a probabilistic learning task in individuals with PP (n=13) and healthy matched control subjects (n=18). The task consisted of three graded learning conditions in which the amount of learning was manipulated by varying the degree to which the response was predictive of the value of the feedback (50, 80 and 100%).

Results

Behaviourally, we found impaired learning and diminished accuracy in the group of individuals with PP. Amplitudes of the response ERN (rERN) were reduced. No differences in the feedback ERN (fERN) were found.

Conclusions

The results are interpreted in terms of a deficit in initial rule learning and subsequent generalization of these rules to new stimuli. Negative feedback is adequately processed at a neural level but this information is not used to improve behaviour on subsequent trials. As learning is degraded, the process of error detection at the moment of the actual response is diminished. Therefore, the current study demonstrates that disturbed error-monitoring processes play a central role in the often reported learning deficits in individuals with PP.

Keywords

Behavioural adaptationerror-monitoringerror-related negativityfeedback learningpsychopathyreinforcement learning
Type
Original Articles
Information
Psychological Medicine , Volume 40 , Issue 9 , September 2010 , pp. 1559 - 1568
Copyright
Copyright © Cambridge University Press 2009

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References

Blair, KS, Morton, J, Leonard, A, Blair, RJR (2006). Impaired decision-making on the basis of both reward and punishment information in individuals with psychopathy. Personality and Individual Differences 41, 155–165.Google Scholar
Blair, RJR (2003). Neurobiological basis of psychopathy. British Journal of Psychiatry 182, 5–7.Google Scholar
Blair, RJR (2005). Applying a cognitive neuroscience perspective to the disorder of psychopathy. Development and Psychopathology 17, 865–891.CrossRefGoogle Scholar
Blair, RJR, Mitchell, DGH, Blair, KS (2005). The Psychopath: Emotion and the Brain. Blackwell Publishing: Oxford, UK.Google Scholar
Blair, RJR, Mitchell, DGH, Leonard, A, Budhani, S, Peschardt, KS, Newman, C (2004). Passive avoidance learning in individuals with psychopathy: modulation by reward but not by punishment. Personality and Individual Differences 37, 1179–1192.Google Scholar
Brazil, IA, de Bruijn, ERA, Bulten, BH, von Borries, AKL, van Lankveld, JJM, Buitelaar, JK, Verkes, RJ (2009). Early and late components of error-monitoring in violent offenders with psychopathy. Biological Psychiatry 65, 137–143.CrossRefGoogle ScholarPubMed
Budhani, S, Richell, RA, Blair, RJR (2006). Impaired reversal but intact acquisition: probabilistic response reversal deficits in adult individuals with psychopathy. Journal of Abnormal Psychology 115, 552–558.Google Scholar
Carter, CS, Braver, TS, Barch, DM, Botvinick, MM, Noll, D, Cohen, JD (1998). Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 28, 747.CrossRefGoogle Scholar
Clarke, HF, Robbins, TW, Roberts, AC (2008). Lesions of the medial striatum in monkeys produce perseverative impairments during reversal learning similar to those produced by lesions in the orbitofrontal cortex. Journal of Neuroscience 28, 10972–10982.Google Scholar
Cleckley, H (1976). The Mask of Sanity, 5th edn. Mosby: St Louis.Google Scholar
Cools, R, Clark, L, Owen, AM, Robbins, TW (2002). Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. Journal of Neuroscience 22, 4563–4567.CrossRefGoogle ScholarPubMed
de Bruijn, ERA, Hulstijn, W, Verkes, RJ, Ruigt, GS, Sabbe, BG (2004). Drug-induced stimulation and suppression of action monitoring in healthy volunteers. Psychopharmacology 177, 151–160.Google Scholar
de Bruijn, ERA, Schubotz, RU, Ullsperger, M (2007). An event-related potential study on the observation of erroneous everyday actions. Cognitive, Affective, and Behavioral Neuroscience 4, 278–285.CrossRefGoogle Scholar
Dehaene, S, Posner, MI, Tucker, DM (1994). Localization of a neural system for error detection and compensation. Psychological Science 5, 303–305.Google Scholar
Dikman, ZA, Allen, JJB (2000). Error monitoring during reward and avoidance learning in high- and low-socialized individuals. Psychophysiology 27, 43–54.CrossRefGoogle Scholar
D'Silva, K, Duggan, C, McCarthy, L (2004). Does treatment really make psychopaths worse? A review of evidence. Journal of Personality Disorders 18, 163–177.CrossRefGoogle Scholar
Flor, H, Birbaumer, N, Hermann, C, Ziegler, S, Patrick, CJ (2002). Aversive Pavlovian conditioning in psychopaths: peripheral and central correlates. Psychophysiology 39, 505–518.Google Scholar
Gehring, WJ, Fencsik, DE (2001). Function of the medial frontal cortex in the processing of conflict and errors. Journal of Neuroscience 21, 9430–9437.Google Scholar
Gratton, G, Coles, MGH, Donchin, E (1983). A new method for off-line removal of ocular artifacts. Electroencephalography and Clinical Neurophysiology 55, 468–484.CrossRefGoogle Scholar
Groenestijn, MAC, Akkerhuis, GW, Kupka, RW, Schneider, N, Nolen, WA (1999). Structured Clinical Interview for DSM-IV Axis I Disorders (SCID-I) [in Dutch]. Swets Test Publishers: Lisse, The Netherlands.Google Scholar
Hall, JR, Bernat, EM, Patrick, CJ (2007). Externalizing psychopathology and the error-related negativity. Psychological Science 18, 326–333.CrossRefGoogle ScholarPubMed
Hare, R (1991). The Hare Psychopathy Checklist – Revised. Multi-Health Systems: Toronto.Google Scholar
Hildebrand, M (2005). Summary of research report: Escapes during leave, escapes and recidivism during TBS treatment in 2000–2005. Expertisecentrum Forensische Psychiatrie.Google Scholar
Holroyd, CB, Coles, MGH (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, Dien, J, Coles, MGH (1998). Error-related scalp potentials elicited by hand and foot movements: evidence for an output-independent error-processing system in humans. Neuroscience Letters 242, 65–68.Google Scholar
Holroyd, CB, Nieuwehuis, S, Yeung, N, Nystrom, L, Mars, RB, Coles, MGH, Cohen, JD (2004). Dorsal anterior cingulated cortex shows fMRI response to internal and external error signals. Nature Neuroscience 7, 497–498.CrossRefGoogle ScholarPubMed
Kiehl, KA, Smith, AM, Hare, RD, Forster, BB, Brink, J, Liddle, PF (2001). Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging. Biological Psychiatry 50, 677–684.CrossRefGoogle ScholarPubMed
Kosson, DS, Newman, JP (1989). Socialization and attentional deficits under focusing and divided attention conditions. Journal of Personality and Social Psychology 57, 175–184.Google Scholar
Lykken, DT (1957). A study of anxiety in the sociopathic personality. Journal of Abnormal and Social Psychology 55, 6–10.CrossRefGoogle ScholarPubMed
Mars, RB, Coles, MGH, Grol, MJ, Holroyd, CB, Nieuwenhuis, S, Hulstijn, W, Toni, I (2005). Neural dynamics of error processing in medial frontal cortex. NeuroImage 29, 1007–1013.CrossRefGoogle Scholar
Mars, RB, de Bruijn, ERA, Hulstijn, W, Milter, WHR, Coles, MGH (2004). What if I told you: ‘You were wrong’? Brain potentials and behavioral adjustments elicited by feedback in a time-estimation task. In Errors, Conflict and the Brain. Current Opinions on Performance Monitoring (ed. Ullsperger, M. and Falkenstein, M.), pp. 129–134. Sächsisches Digitaldruck Zentrum GmbH: Dresden, Germany.Google Scholar
Miltner, WHR, Braun, CH, Coles, MGH (1997). Event-related brain potentials following incorrect feedback in a time-estimation task: evidence for a ‘generic’ neural system for error detection. Journal of Cognitive Neuroscience 9, 788–798.CrossRefGoogle Scholar
Mitchell, DGV, Fine, C, Richell, RA, Newman, C, Lumsden, J, Blair, KS, Blair, RJR (2006). Instrumental learning and relearning in individuals with psychopathy and in patients with lesions involving the amygdala or orbitofrontal cortex. Neuropsychology 20, 280–289.CrossRefGoogle ScholarPubMed
Munro, GE, Dywan, J, Harris, GT, McKee, S, Unsal, A, Segalowitz, SJ (2007). ERN varies with degree of psychopathy in an emotion discrimination task. Biological Psychiatry 76, 31–42.Google Scholar
Newman, JP (1987). Reaction to punishment in extraverts and psychopaths: implications for the impulsive behavior of disinhibited individuals. Journal of Research in Personality 21, 464–480.CrossRefGoogle Scholar
Newman, JP, Kosson, DS (1986). Passive avoidance learning in psychopathic and nonpsychopathic offenders. Journal of Abnormal Psychology 95, 252–256.CrossRefGoogle ScholarPubMed
Nieuwenhuis, S, Nielen, MM, Mol, N, Hajcak, G, Veltman, DJ (2005). Performance monitoring in obsessive-compulsive disorder. Psychiatry Research 134, 111–122.Google Scholar
Nieuwenhuis, S, Ridderinkhof, KR, Talsma, D, Coles, MGH, Holroyd, CB, Kok, A, van der Molen, MW (2002). A computational account of altered error processing in older age: dopamine and the error-related negativity. Cognitive, Affective, and Behavioral Neuroscience 2, 19–36.Google Scholar
Pailing, PE, Segalowitz, SJ (2004). The effects of uncertainty in error monitoring on associated ERPs. Brain and Cognition 56, 215–233.CrossRefGoogle ScholarPubMed
Pridmore, S, Chambers, A, McArthur, M (2005). Neuroimaging in psychopathy. Australian and New Zealand Journal of Psychiatry 39, 856–865.Google Scholar
Rushworth, MFS, Behrens, TEJ, Rudebeck, PH, Walton, ME (2007). Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behavior. Trends in Cognitive Sciences 11, 168–176.CrossRefGoogle Scholar
Ullsperger, M, Falkenstein, M (2004). Errors, Conflict and the Brain. Current Opinions on Performance Monitoring. MPI Special Issue. Sächsisches Digitaldruck Zentrum GmbH: Dresden, Germany.Google Scholar
Ullsperger, M, von Cramon, DY (2006). The role of intact frontostriatal circuits in error processing. Journal of Cognitive Neuroscience 18, 651–664.CrossRefGoogle ScholarPubMed
van Vliet, IM, Leroy, H, van Megen, HJGM (2000). M.I.N.I. International Neuropsychiatric Interview, Dutch Version 5.0.0 [in Dutch]. LUMC: Leiden.Google Scholar