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Abnormal negative feedback processing in first episode schizophrenia: evidence from an oculomotor rule switching task

Published online by Cambridge University Press:  07 January 2011

V. C. Huddy ,
T. L. Hodgson ,
M. A. Ron ,
T. R. E. Barnes  and
E. M. Joyce
V. C. Huddy*
Affiliation:
Institute of Psychiatry, Kings College London, London, UK
T. L. Hodgson
Affiliation:
School of Psychology, University of Exeter, Exeter, UK
M. A. Ron
Affiliation:
Institute of Neurology, University College London, London, UK
T. R. E. Barnes
Affiliation:
Division of Neuroscience and Mental Health, Imperial College London, London, UK
E. M. Joyce
Affiliation:
Institute of Neurology, University College London, London, UK
*
*Address for correspondence: V. C. Huddy, Ph.D., D.Clin.Psy., Kings College London, Institute of Psychiatry, Department of Psychology, De Crespigny Park, London SE5 8AF, UK. (Email: vyv.huddy@kcl.ac.uk)
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Abstract

Background

Previous studies have shown that patients with schizophrenia are impaired on executive tasks, where positive and negative feedbacks are used to update task rules or switch attention. However, research to date using saccadic tasks has not revealed clear deficits in task switching in these patients. The present study used an oculomotor ‘rule switching’ task to investigate the use of negative feedback when switching between task rules in people with schizophrenia.

Method

A total of 50 patients with first episode schizophrenia and 25 healthy controls performed a task in which the association between a centrally presented visual cue and the direction of a saccade could change from trial to trial. Rule changes were heralded by an unexpected negative feedback, indicating that the cue-response mapping had reversed.

Results

Schizophrenia patients were found to make increased errors following a rule switch, but these were almost entirely the result of executing saccades away from the location at which the negative feedback had been presented on the preceding trial. This impairment in negative feedback processing was independent of IQ.

Conclusions

The results not only confirm the existence of a basic deficit in stimulus–response rule switching in schizophrenia, but also suggest that this arises from aberrant processing of response outcomes, resulting in a failure to appropriately update rules. The findings are discussed in the context of neurological and pharmacological abnormalities in the conditions that may disrupt prediction error signalling in schizophrenia.

Keywords

Cognitive impairmentseye movementsexecutive functionreward processingschizophreniaworking memory
Type
Original Articles
Information
Psychological Medicine , Volume 41 , Issue 9 , September 2011 , pp. 1805 - 1814
Copyright
Copyright © Cambridge University Press 2011

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References

Abi-Dargham, A, Rodenhiser, J, Printz, D, Zea-Ponce, Y, Gil, R, Kegeles, LS, Weiss, R, Cooper, B, Mann, JJ, Van Heertum, RL, Gorman, JM, Laruelle, M (2000). Increased baseline occupancy of D-2 receptors by dopamine in schizophrenia. Proceedings of the National Academy of Sciences of the United States of America 97, 8104–8109.CrossRefGoogle ScholarPubMed
Andreasen, NC (1983). The Scale for the Assessment of Negative Symptoms (SANS). The University of Iowa: Iowa City, Iowa.Google Scholar
Andreasen, N (1984). The Scale for the Assessment of Positive Symptoms (SAPS). The University of Iowa: Iowa City, IA.Google Scholar
Anden, NE, Butcher, SG, Corrodi, H, Fuxe, K, Ungerstedt, U (1970). Receptor activity and turnover of dopamine and noradrenaline after neuroleptics. European Journal of Pharmacology 11, 303–314.CrossRefGoogle ScholarPubMed
Aron, AR, Fletcher, PC, Bullmore, ET, Sahakian, BJ, Robbins, TW (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience 6, 115–116.CrossRefGoogle ScholarPubMed
Aron, AR, Robbins, TW, Poldrack, RA (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences 8, 170–177.CrossRefGoogle ScholarPubMed
Berman, KF, Ostrem, JL, Randolph, C, Gold, J, Goldberg, TE, Coppola, R, Carson, RE, Herscovitch, P, Weinberger, DR (1995). Physiological activation of a cortical network during performance of the Wisconsin Card Sorting Test – a positron emission tomography study. Neuropsychologia 33, 1027–1046.CrossRefGoogle ScholarPubMed
Blyler, CR, Gold, JM, Iannone, VN, Buchanan, RW (2000). Short form of the ‘WAIS-III for use with patients with schizophrenia. Schizophrenia Research 46, 209–215.CrossRefGoogle ScholarPubMed
Carter, CS, Barch, DM, Buchanan, RW, Bullmore, E, Krystal, JH, Cohen, J, Geyer, M, Green, M, Nuechterlein, KH, Robbins, T, Silverstein, S, Smith, EF, Strauss, M, Wykes, T, Heinssen, R (2008). Identifying cognitive mechanisms targeted for treatment development in schizophrenia: an overview of the first meeting of the Cognitive Neuroscience Treatment Research to Improve Cognition in Schizophrenia Initiative. Biological Psychiatry 64, 4–10.CrossRefGoogle ScholarPubMed
Corlett, PR, Murray, GK, Honey, GD, Aitken, MRF, Shanks, DR, Robbins, TW, Bullmore, ET, Dickinson, A, Fletcher, PC (2007). Disrupted prediction-error signal in psychosis: evidence for an associative account of delusions. Brain 130, 2387–2400.CrossRefGoogle ScholarPubMed
Creese, I, Burt, DR, Snyder, SH (1976). Dopamine receptor-binding predicts clinical and pharmacological potencies of anti-schizophrenic drugs. Science 192, 481–483.CrossRefGoogle Scholar
Dickinson, D, Harvey, PD (2009). Systemic hypotheses for generalized cognitive deficits in schizophrenia: a new take on an old problem. Schizophrenia Bulletin 35, 403–414.CrossRefGoogle Scholar
Franke, C, Reuter, B, Schulz, L, Kathmann, N (2007). Schizophrenia patients show impaired response switching in saccade tasks. Biological Psychology 76, 91–99.CrossRefGoogle ScholarPubMed
Fukushima, J, Fukushima, K, Chiba, T, Tanaka, S, Yamashita, I, Kato, M (1988). Disturbances of voluntary control of saccadic eye movements in schizophrenic patients. Biological Psychiatry 23, 670–677.CrossRefGoogle ScholarPubMed
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
Goldberg, TE, Weinberger, DR (1994). Schizophrenia, training paradigms, and the Wisconsin Card Sorting Test Redux. Schizophrenia Research 11, 291–296.CrossRefGoogle ScholarPubMed
Grant, DA, Berg, EA (1948). A behavioral analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card-sorting problem. Journal of Experimental Psychology 38, 404–411.CrossRefGoogle Scholar
Greenzang, C, Manoach, DS, Goff, DC, Barton, JJS (2007). Task-switching in schizophrenia: active switching costs and passive carry-over effects in an antisaccade paradigm. Experimental Brain Research 181, 493–502.CrossRefGoogle Scholar
Guitton, D, Buchtel, HA, Douglas, RM (1985). Frontal-lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Experimental Brain Research 58, 455–472.CrossRefGoogle ScholarPubMed
Hallett, PE, Adams, BD (1980). The predictability of saccadic latency in a novel voluntary oculomotor task. Vision Research 20, 329–339.CrossRefGoogle Scholar
Heerey, EA, Robinson, BM, McMahon, RP, Gold, JM (2007). Delay discounting in schizophrenia. Cognitive Neuropsychiatry 12, 213–221.CrossRefGoogle ScholarPubMed
Hodgson, T, Chamberlain, M, Parris, B, James, M, Gutowski, N, Husain, M, Kennard, C (2007). The role of the ventrolateral frontal cortex in inhibitory oculomotor control. Brain 130, 1525–1537.CrossRefGoogle ScholarPubMed
Hodgson, TL, Golding, C, Molyva, D, Rosenthal, CR, Kennard, C (2004). Eye movements during task switching: reflexive, symbolic, and affective contributions to response selection. Journal of Cognitive Neuroscience 16, 318–330.CrossRefGoogle ScholarPubMed
Hodgson, TL, Mort, D, Chamberlain, MM, Hutton, SB, O'Neill, KS, Kennard, C (2002). Orbitofrontal cortex mediates inhibition of return. Neuropsychologia 40, 1891–1901.CrossRefGoogle ScholarPubMed
Huddy, VC, Aron, AR, Harrison, M, Barnes, TRE, Robbins, TW, Joyce, EM (2009). Impaired conscious and preserved unconscious inhibitory processing in recent onset schizophrenia. Psychological Medicine 39, 907–916.CrossRefGoogle ScholarPubMed
Huddy, VC, Hodgson, TL, Kapasi, M, Mutsatsa, SH, Harrison, I, Barnes, TRE, Joyce, EM (2007). Gaze strategies during planning in first-episode psychosis. Journal of Abnormal Psychology 116, 589–598.CrossRefGoogle ScholarPubMed
Hunt, AR, Klein, RM (2002). Eliminating the cost of task set reconfiguration. Memory & Cognition 30, 529–539.CrossRefGoogle ScholarPubMed
Hunt, AR, Olk, B, von Muhlenen, A, Kingstone, A (2004). Integration of competing saccade programs. Cognitive Brain Research 19, 206–208.CrossRefGoogle ScholarPubMed
Husain, M, Parton, A, Hodgson, TL, Mort, D, Rees, G (2003). Self-control during response conflict by human supplementary eye field. Nature Neuroscience 6, 117–118.CrossRefGoogle ScholarPubMed
Hutton, SB, Ettinger, U (2006). The antisaccade task as a research tool in psychopathology: a critical review. Psychophysiology 43, 302–313.CrossRefGoogle ScholarPubMed
Hutton, SB, Puri, BK, Duncan, L-J, Robbins, TW, Barnes, TRE, Joyce, EM (1998). Executive function in first-episode schizophrenia. Psychological Medicine 28, 463–473.CrossRefGoogle ScholarPubMed
Jablensky, A, Sartorius, N, Ernberg, G, Anker, M, Korten, A, Cooper, JE, Day, R, Bertelsen, A (1992). Schizophrenia: manifestations, incidence and course in different cultures. A World Health Organization ten country study. Psychological Medicine (Mongraph Supplement) 20, 1–97.CrossRefGoogle ScholarPubMed
Kaladjian, A, Jeanningros, R, Azorin, JM, Grimault, S, Anton, JL, Mazzola-Pomietto, P (2007). Blunted activation in right ventrolateral prefrontal cortex during motor response inhibition in schizophrenia. Schizophrenia Research 97, 184–193.CrossRefGoogle ScholarPubMed
Kapur, S (2003). Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. American Journal of Psychiatry 160, 13–23.CrossRefGoogle ScholarPubMed
Leeson, V, Robbins, TW, Matheson, E, Hutton, SB, Ron, M, Barnes, TRE, Joyce, EM (2009). Discrimination learning, reversal and set-shifting in first episode schizophrenia: stability over six years and specific associations with medication type and disorganisation syndrome. Biological Psychiatry 15, 586–593.CrossRefGoogle Scholar
Li, C, Park, S (2004). Do schizophrenia patients make more perseverative than non-perseverative errors on the Wisconsin Card Sorting Test? A meta-analytic study. Psychiatry Research 129, 179–190.CrossRefGoogle ScholarPubMed
Manoach, DS, Lindgren, KA, Cherkasova, MV, Goff, DC, Halpern, EF, Intriligator, J, Barton, JJ (2002). Schizophrenic subjects show deficient inhibition but intact task switching on saccadic tasks. Biological Psychiatry 51, II.CrossRefGoogle ScholarPubMed
Meiran, N, Levine, J, Meiran, N, Henik, A (2000). Task set switching in schizophrenia. Neuropsychology 14, 471–482.CrossRefGoogle ScholarPubMed
Monsell, S (2003). Task switching. Trends in Cognitive Sciences 7, 134–140.CrossRefGoogle ScholarPubMed
Murray, GK, Cheng, F, Clark, L, Barnett, JH, Blackwell, AD, Fletcher, PC, Robbins, TW, Bullmore, ET, Jones, PB (2008). Reinforcement and reversal learning in first-episode psychosis. Schizophrenia Bulletin 34, 848–855.CrossRefGoogle ScholarPubMed
Nelson, HE (1976). Modified card sorting rest sensitive to frontal lobe defects. Cortex 12, 313–324.CrossRefGoogle Scholar
Nobre, AC, Coull, JT, Frith, CD, Mesulam, MM (1999). Orbitofrontal cortex is activated during breaches of expectation in tasks of visual attention. Nature Neuroscience 2, 11–12.CrossRefGoogle ScholarPubMed
Owen, AM, Downes, JJ, Sahakian, BJ, Polkey, CE, Robbins, TW (1990). Planning and spatial working memory following frontal-lobe lesions in man. Neuropsychologia 28, 1021–1034.CrossRefGoogle ScholarPubMed
Pantelis, C, Barnes, TRE, Nelson, HE, Tanner, S, Weatherley, L, Owen, AM, Robbins, TW (1997). Fronto-striatal cognitive deficits in patients with chronic schizophrenia. Brain 120, 1823–1843.CrossRefGoogle Scholar
Parton, A, Nachev, P, Hodgson, TL, Mort, D, Thomas, D, Ordidge, R, Morgan, P, Jackson, S, Rees, G, Husain, M (2007). Role of the human supplementary eye field in the control of saccadic eye movements. Neuropsychologia 45, 997–1008.CrossRefGoogle ScholarPubMed
Polli, FE, Barton, JJS, Vangel, M, Goff, DC, Iguchi, L, Manoach, DS (2006). Schizophrenia patients show intact immediate error-related performance adjustments on an antisaccade task. Schizophrenia Research 82, 191–201.CrossRefGoogle Scholar
Posner, MI, Rafal, RD, Choate, LS, Vaughan, J (1985). Inhibition of return: neural basis and function. Cognitive Neuropsychology 2, 211–238.CrossRefGoogle Scholar
Prentice, KJ, Gold, JM, Buchanan, RW (2008). The Wisconsin Card Sorting impairment in schizophrenia is evident in the first four trials. Schizophrenia Research 106, 81–87.CrossRefGoogle ScholarPubMed
Reuter, B, Jager, M, Bottlender, R, Kathmann, N (2007). Impaired action control in schizophrenia: the role of volitional saccade initiation. Neuropsychologia 45, 1840–1848.CrossRefGoogle ScholarPubMed
Reuter, B, Kathmann, N (2004). Using saccade tasks as a tool to analyze executive dysfunctions in schizophrenia. Acta Psychologica 115, 255–269.CrossRefGoogle ScholarPubMed
Schultz, W, Dickinson, A (2000). Neuronal coding of prediction errors. Annual Review of Neuroscience 23, 473–500.CrossRefGoogle ScholarPubMed
Seeman, P, Chau-Wong, M, Tedesco, J, Wong, K (1976). Dopamine receptors in human and calf brains, using [3H]apomorphine and an antipsychotic drug. Proceedings of the National Academy of Science 73, 4354–4358.CrossRefGoogle Scholar
Swainson, R, Rogers, RD, Sahakian, BJ, Summers, BA, Polkey, CE, Robbins, TW (2000). Probabilistic learning and reversal deficits in patients with Parkinson's disease or frontal or temporal lobe lesions: possible adverse effects of dopaminergic medication. Neuropsychologia 38, 596–612.CrossRefGoogle ScholarPubMed
Takahashi, YK, Roesch, MR, Stalnaker, TA, Haney, RZ, Calu, DJ, Taylor, AR, Burke, KA, Schoenbaum, G (2009). The orbitofrontal cortex and ventral tegmental area are necessary for learning from unexpected outcomes. Neuron 62, 269–280.CrossRefGoogle ScholarPubMed
Tremblay, L, Schultz, W (2000). Reward-related neuronal activity during go-nogo task performance in primate orbitofrontal cortex. Journal of Neurophysiology 83, 1864–1876.CrossRefGoogle ScholarPubMed
Waelti, P, Dickinson, A, Schultz, W (2001). Dopamine responses comply with basic assumptions of formal learning theory. Nature 412, 43–48.CrossRefGoogle ScholarPubMed
Walker, R, Husain, M, Hodgson, TL, Harrison, J, Kennard, C (1998). Saccadic eye movement and working memory deficits following damage to human prefrontal cortex. Neuropsychologia 36, 1141–1159.CrossRefGoogle ScholarPubMed
Waltz, JA, Gold, JM (2007). Probabilistic reversal learning impairments in schizophrenia: Further evidence of orbitofrontal dysfunction. Schizophrenia Research 93, 296–303.CrossRefGoogle ScholarPubMed
Wechsler, D (1999). Wechsler Adult Intelligence Scale – third edn. Psychological Corporation: London.Google Scholar
Wechsler, D (2001). Wechsler Test of Adult Reading – 3rd edn. Psychological Corporation: London.Google Scholar
Weinberger, DR, Berman, KF, Zec, RF (1986). Physiological dysfunction of dorsolateral prefrontal cortex in schizophrenia. 1. Regional cerebral blood-flow evidence. Archives of General Psychiatry 43, 114–124.CrossRefGoogle Scholar
Woodberry, KA, Giuliano, AJ, Seidman, LJ (2008). Premorbid IQ in schizophrenia: a meta-analytic review. American Journal of Psychiatry 165, 579–587.CrossRefGoogle ScholarPubMed
Wykes, T, Reeder, C, Landau, S, Everitt, B, Knapp, M, Patel, A, Romeo, R (2007). Cognitive remediation therapy in schizophrenia: randomised controlled trial. British Journal of Psychiatry 190, 421–427.CrossRefGoogle ScholarPubMed