Hostname: page-component-848d4c4894-v5vhk Total loading time: 0 Render date: 2024-07-08T05:18:56.118Z Has data issue: false hasContentIssue false
  • English
  • Français

Impulsivity and neural correlates of response inhibition in schizophrenia

Published online by Cambridge University Press:  21 April 2010

A. Kaladjian ,
R. Jeanningros ,
J.-M. Azorin ,
J.-L. Anton  and
P. Mazzola-Pomietto
A. Kaladjian*
Affiliation:
Institut de Neurosciences Cognitives de la Méditerranée, UMR 6193 CNRS – Université de la Méditerranée, Marseille, France Pôle Universitaire de Psychiatrie Adulte, Hôpital Sainte Marguerite, Marseille, France
R. Jeanningros
Affiliation:
Institut de Neurosciences Cognitives de la Méditerranée, UMR 6193 CNRS – Université de la Méditerranée, Marseille, France
J.-M. Azorin
Affiliation:
Institut de Neurosciences Cognitives de la Méditerranée, UMR 6193 CNRS – Université de la Méditerranée, Marseille, France Pôle Universitaire de Psychiatrie Adulte, Hôpital Sainte Marguerite, Marseille, France
J.-L. Anton
Affiliation:
Centre d'Imagerie par Résonance Magnétique fonctionnelle, IFR 131, Marseille, France
P. Mazzola-Pomietto
Affiliation:
Institut de Neurosciences Cognitives de la Méditerranée, UMR 6193 CNRS – Université de la Méditerranée, Marseille, France
*
*Address for correspondence: A. Kaladjian, M.D., Ph.D., Institut de Neurosciences Cognitives de la Méditerranée, UMR 6193 CNRS – Université de la Méditerranée, 31, chemin Joseph Aiguier13402Marseillecedex 20, France (Email: arthur.kaladjian@univmed.fr)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

The clinical picture of schizophrenia is frequently worsened by manifestations of impulsivity. However, the neural correlates of impulsivity in this disorder are poorly known. Although impulsivity has been related to disturbances of the neural processes underlying response inhibition, no studies have yet examined the relationship between these processes and psychometric measures of impulsivity in schizophrenia. This was the aim of the current investigation.

Method

Event-related functional magnetic resonance imaging in conjunction with a Go/NoGo task was employed to probe the neural activity associated with response inhibition in 26 patients with schizophrenia and 30 healthy comparison subjects. All participants also completed the Barratt Impulsiveness Scale – version 11 (BIS-11). Voxel-wise regression analyses were used to examine the relationship between the BIS-11 score and brain activation during response inhibition in each group.

Results

Patients with schizophrenia were more impulsive than healthy subjects, as indicated by higher BIS-11 scores. Patients, but not healthy subjects, were found to display a positive correlation between these scores and cerebral activation associated with response inhibition. This correlation involves a unique cluster localized within the right ventrolateral prefrontal cortex (VLPFC), a key node of the brain network subserving response inhibition.

Conclusions

We evidenced in patients with schizophrenia that greater BIS-11 scores are associated with greater activation within the right VLPFC during response inhibition. This finding suggests that the efficiency of this brain region to process inhibitory control is reduced in the more impulsive patients.

Keywords

Barrattbrain activationfMRIimpulsivityresponse inhibitionschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 41 , Issue 2 , February 2011 , pp. 291 - 299
Copyright
Copyright © Cambridge University Press 2010

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

Altshuler, LL, Bookheimer, SY, Townsend, J, Proenza, MA, Eisenberger, N, Sabb, F, Mintz, J, Cohen, MS (2005). Blunted activation in orbitofrontal cortex during mania: a functional magnetic resonance imaging study. Biological Psychiatry 58, 763–769.CrossRefGoogle Scholar
Arce, E, Leland, DS, Miller, DA, Simmons, AN, Winternheimer, KC, Paulus, MP (2006). Individuals with schizophrenia present hypo- and hyperactivation during implicit cueing in an inhibitory task. Neuroimage 32, 704–713.Google Scholar
Aron, AR, Robbins, TW, Poldrack, RA (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences 8, 170–177.Google Scholar
Asahi, S, Okamoto, Y, Okada, G, Yamawaki, S, Yokota, N (2004). Negative correlation between right prefrontal activity during response inhibition and impulsiveness: a fMRI study. European Archives of Psychiatry and Clinical Neuroscience 254, 245–251.CrossRefGoogle ScholarPubMed
Barkataki, I, Kumari, V, Das, M, Sumich, A, Taylor, P, Sharma, T (2008). Neural correlates of deficient response inhibition in mentally disordered violent individuals. Behavioral Sciences and the Law 26, 51–64.CrossRefGoogle ScholarPubMed
Bigelow, DA, Cutler, DL, Moore, LJ, McComb, P, Leung, P (1988). Characteristics of state hospital patients who are hard to place. Hospital and Community Psychiatry 39, 181–185.Google ScholarPubMed
Bowers, L, Jeffery, D, Bilgin, H, Jarrett, M, Simpson, A, Jones, J (2008). Psychiatric intensive care units: a literature review. The international Journal of Social Psychiatry 54, 56–68.Google Scholar
Braver, TS, Barch, DM, Gray, JR, Molfese, DL, Snyder, A (2001). Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. Cerebral Cortex 11, 825–836.CrossRefGoogle ScholarPubMed
Brown, SM, Manuck, SB, Flory, JD, Hariri, AR (2006). Neural basis of individual differences in impulsivity: contributions of corticolimbic circuits for behavioral arousal and control. Emotion 6, 239–245.Google Scholar
Callicott, JH, Bertolino, A, Mattay, VS, Langheim, FJ, Duyn, J, Coppola, R, Goldberg, TE, Weinberger, DR (2000). Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. Cerebral Cortex 10, 1078–1092.Google Scholar
Chamberlain, SR, Sahakian, BJ (2007). The neuropsychiatry of impulsivity. Current Opinion in Psychiatry 20, 255–261.Google Scholar
Chambers, CD, Bellgrove, MA, Stokes, MG, Henderson, TR, Garavan, H, Robertson, IH, Morris, AP, Mattingley, JB (2006). Executive ‘brake failure’ following deactivation of human frontal lobe. Journal of Cognitive Neuroscience 18, 444–455.Google Scholar
Chengappa, KN, Vasile, J, Levine, J, Ulrich, R, Baker, R, Gopalani, A, Schooler, N (2002). Clozapine: its impact on aggressive behavior among patients in a state psychiatric hospital. Schizophrenia Research 53, 1–6.CrossRefGoogle Scholar
Dervaux, A, Bayle, FJ, Laqueille, X, Bourdel, MC, Le Borgne, MH, Olie, JP, Krebs, MO (2001). Is substance abuse in schizophrenia related to impulsivity, sensation seeking, or anhedonia? American Journal of Psychiatry 158, 492–494.Google Scholar
Dimoska, A, Johnstone, SJ (2007). Neural mechanisms underlying trait impulsivity in non-clinical adults: stop-signal performance and event-related potentials. Progress in Neuropsychopharmacology and Biological Psychiatry 31, 443–454.CrossRefGoogle ScholarPubMed
Dursun, SM, Szemis, A, Andrews, H, Whitaker, P, Reveley, MA (2000). Effects of clozapine and typical antipsychotic drugs on plasma 5-HT turnover and impulsivity in patients with schizophrenia: a cross-sectional study. Journal of Psychiatry and Neuroscience 25, 347–352.Google Scholar
Enticott, PG, Ogloff, JR, Bradshaw, JL (2008). Response inhibition and impulsivity in schizophrenia. Psychiatry Research 157, 251–254.CrossRefGoogle ScholarPubMed
Evenden, JL (1999). Varieties of impulsivity. Psychopharmacology (Berlin) 146, 348–361.CrossRefGoogle ScholarPubMed
Eysenck, SBG, Pearson, PR, Easting, G, Allsopp, JF (1985). Age norms for impulsiveness, venturesomeness and empathy in adults. Personality and Individual Differences 6, 613–619.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1996). Structured Clinical Interview for DSM-IV Axis I Disorders, Research Version, Patient Edition (SCID-I/P) and Non-patient Edition (SCID-I/NP). Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Ford, JM, Gray, M, Whitfield, SL, Turken, AU, Glover, G, Faustman, WO, Mathalon, DH (2004). Acquiring and inhibiting prepotent responses in schizophrenia: event-related brain potentials and functional magnetic resonance imaging. Archives of General Psychiatry 61, 119–129.Google Scholar
Friston, KJ, Holmes, AP, Worsley, KJ, Poline, JB, Frith, CD, Frakowiack, RSJ (1995). Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping 2, 189–210.Google Scholar
Garavan, H, Ross, TJ, Stein, EA (1999). Right hemispheric dominance of inhibitory control: an event-related functional MRI study. Proceedings of the National Academy of Sciences USA 96, 8301–8306.Google Scholar
Goethals, I, Audenaert, K, Jacobs, F, Van den Eynde, F, Bernagie, K, Kolindou, A, Vervaet, M, Dierckx, R, Van Heeringen, C (2005). Brain perfusion SPECT in impulsivity-related personality disorders. Behavioral Brain Research 157, 187–192.Google Scholar
Greenfield, TK, McNiel, DE, Binder, RL (1989). Violent behavior and length of psychiatric hospitalization. Hospital and Community Psychiatry 40, 809–814.Google Scholar
Gut-Fayand, A, Dervaux, A, Olie, JP, Loo, H, Poirier, MF, Krebs, MO (2001). Substance abuse and suicidality in schizophrenia: a common risk factor linked to impulsivity. Psychiatry Research 102, 65–72.Google Scholar
Hoptman, MJ, Volavka, J, Johnson, G, Weiss, E, Bilder, RM, Lim, KO (2002). Frontal white matter microstructure, aggression, and impulsivity in men with schizophrenia: a preliminary study. Biological Psychiatry 52, 9–14.Google Scholar
Horn, NR, Dolan, M, Elliott, R, Deakin, JF, Woodruff, PW (2003). Response inhibition and impulsivity: an fMRI study. Neuropsychologia 41, 1959–1966.Google Scholar
Joyal, CC, Putkonen, A, Mancini-Marie, A, Hodgins, S, Kononen, M, Boulay, L, Pihlajamaki, M, Soininen, H, Stip, E, Tiihonen, J, Aronen, HJ (2007). Violent persons with schizophrenia and comorbid disorders: a functional magnetic resonance imaging study. Schizophrenia Research 91, 97–102.Google Scholar
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.Google Scholar
Karch, S, Jager, L, Karamatskos, E, Graz, C, Stammel, A, Flatz, W, Lutz, J, Holtschmidt-Taschner, B, Genius, J, Leicht, G, Pogarell, O, Born, C, Moller, HJ, Hegerl, U, Reiser, M, Soyka, M, Mulert, C (2008). Influence of trait anxiety on inhibitory control in alcohol-dependent patients: simultaneous acquisition of ERPs and BOLD responses. Journal of Psychiatric Research 42, 734–745.Google Scholar
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.CrossRefGoogle ScholarPubMed
Konishi, S, Nakajima, K, Uchida, I, Sekihara, K, Miyashita, Y (1998). No-go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging. European Journal of Neuroscience 10, 1209–1213.Google Scholar
Krakowski, MI, Czobor, P, Citrome, L, Bark, N, Cooper, TB (2006). Atypical antipsychotic agents in the treatment of violent patients with schizophrenia and schizoaffective disorder. Archives of General Psychiatry 63, 622–629.Google Scholar
Lansbergen, MM, Bocker, KB, Bekker, EM, Kenemans, JL (2007). Neural correlates of stopping and self-reported impulsivity. Clinical Neurophysiology 118, 2089–2103.CrossRefGoogle ScholarPubMed
Laurens, KR, Ngan, ET, Bates, AT, Kiehl, KA, Liddle, PF (2003). Rostral anterior cingulate cortex dysfunction during error processing in schizophrenia. Brain 126, 610–622.CrossRefGoogle ScholarPubMed
Liddle, PF, Kiehl, KA, Smith, AM (2001). Event-related fMRI study of response inhibition. Human Brain Mapping 12, 100–109.Google Scholar
Logan, GD, Schacher, RJ, Tannock, R (1997). Impulsivity and inhibitory control. Psychological Science 8, 60–64.Google Scholar
Mackinnon, A, Ritchie, K, Mulligan, R (1999). The measurement properties of a French language adaptation of the national adult reading test. International Journal of Methods in Psychiatric Research 8, 27–38.CrossRefGoogle Scholar
Manoach, DS (2003). Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophrenia Research 60, 285–298.CrossRefGoogle ScholarPubMed
Mazzola-Pomietto, P, Kaladjian, A, Azorin, JM, Anton, JL, Jeanningros, R (2009). Bilateral decrease in ventrolateral prefrontal cortex activation during motor response inhibition in mania. Journal of Psychiatric Research 43, 432–441.Google Scholar
Moeller, FG, Barratt, ES, Dougherty, DM, Schmitz, JM, Swann, AC (2001). Psychiatric aspects of impulsivity. American Journal of Psychiatry 158, 1783–193.Google Scholar
Naudts, K, Hodgins, S (2006). Neurobiological correlates of violent behavior among persons with schizophrenia. Schizophrenia Bulletin 32, 562–572.Google Scholar
Nieuwenhuis, S, Yeung, N, van den Wildenberg, W, Ridderinkhof, KR (2003). Electrophysiological correlates of anterior cingulate function in a go/no-go task: effects of response conflict and trial type frequency. Cognitive, Affective and Behavioral Neuroscience 3, 17–26.CrossRefGoogle Scholar
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113.Google Scholar
Passamonti, L, Fera, F, Magariello, A, Cerasa, A, Gioia, MC, Muglia, M, Nicoletti, G, Gallo, O, Provinciali, L, Quattrone, A (2006). Monoamine oxidase-a genetic variations influence brain activity associated with inhibitory control: new insight into the neural correlates of impulsivity. Biological Psychiatry 59, 334–340.Google Scholar
Patton, JH, Stanford, MS, Barratt, ES (1995). Factor structure of the Barratt impulsiveness scale. Journal of Clinical Psychology 51, 768–774.Google Scholar
Potkin, SG, Turner, JA, Brown, GG, McCarthy, G, Greve, DN, Glover, GH, Manoach, DS, Belger, A, Diaz, M, Wible, CG, Ford, JM, Mathalon, DH, Gollub, R, Lauriello, J, O'Leary, D, van Erp, TG, Toga, AW, Preda, A, Lim, KO (2009). Working memory and DLPFC inefficiency in schizophrenia: the FBIRN study. Schizophrenia Bulletin 35, 19–31.Google Scholar
Quanbeck, CD, McDermott, BE, Lam, J, Eisenstark, H, Sokolov, G, Scott, CL (2007). Categorization of aggressive acts committed by chronically assaultive state hospital patients. Psychiatric Services 58, 521–528.Google Scholar
Raemaekers, M, Ramsey, NF, Vink, M, van den Heuvel, MP, Kahn, RS (2006). Brain activation during antisaccades in unaffected relatives of schizophrenic patients. Biological Psychiatry 59, 530–535.CrossRefGoogle ScholarPubMed
Rubia, K, Lee, F, Cleare, AJ, Tunstall, N, Fu, CH, Brammer, M, McGuire, P (2005 a). Tryptophan depletion reduces right inferior prefrontal activation during response inhibition in fast, event-related fMRI. Psychopharmacology (Berlin) 179, 791–803.CrossRefGoogle ScholarPubMed
Rubia, K, Russell, T, Bullmore, ET, Soni, W, Brammer, MJ, Simmons, A, Taylor, E, Andrew, C, Giampietro, V, Sharma, T (2001). An fMRI study of reduced left prefrontal activation in schizophrenia during normal inhibitory function. Schizophrenia Research 52, 47–55.Google Scholar
Rubia, K, Smith, AB, Brammer, MJ, Toone, B, Taylor, E (2005 b). Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. American Journal of Psychiatry 162, 1067–1075.Google Scholar
Spivak, B, Shabash, E, Sheitman, B, Weizman, A, Mester, R (2003). The effects of clozapine versus haloperidol on measures of impulsive aggression and suicidality in chronic schizophrenia patients: an open, nonrandomized, 6-month study. Journal of Clinical Psychiatry 64, 755–760.Google Scholar
Stanislaw, H, Todorov, N (1999). Calculation of signal detection theory measures. Behavior Research Methods, Instruments and Computers 31, 137–149.CrossRefGoogle ScholarPubMed
Volavka, J, Citrome, L (2008). Heterogeneity of violence in schizophrenia and implications for long-term treatment. International Journal of Clinical Practice 62, 1237–1245.Google Scholar
Watanabe, J, Sugiura, M, Sato, K, Sato, Y, Maeda, Y, Matsue, Y, Fukuda, H, Kawashima, R (2002). The human prefrontal and parietal association cortices are involved in NO-GO performances: an event-related fMRI study. Neuroimage 17, 1207–1216.Google Scholar
Supplementary material: PDF

Kaladjian supplementary material

Figure S1.pdf

Download Kaladjian supplementary material(PDF)
PDF 95.3 KB
Supplementary material: PDF

Kaladjian supplementary material

Figure S2.pdf

Download Kaladjian supplementary material(PDF)
PDF 77.4 KB
Supplementary material: File

Kaladjian supplementary material

Figure legends.doc

Download Kaladjian supplementary material(File)
File 51.7 KB