Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-23T22:03:48.647Z Has data issue: false hasContentIssue false
  • English
  • Français

Tobacco smoking in schizophrenia: investigating the role of incentive salience

Published online by Cambridge University Press:  01 November 2013

T. P. Freeman ,
J. M. Stone ,
B. Orgaz ,
L. A. Noronha ,
S. L. Minchin  and
H. V. Curran
T. P. Freeman*
Affiliation:
Clinical Psychopharmacology Unit, University College London, UK
J. M. Stone
Affiliation:
Department of Medicine, Division of Brain Sciences, Hammersmith Hospital, Imperial College London, UK Institute of Psychiatry, King's College London, UK
B. Orgaz
Affiliation:
Clinical Psychopharmacology Unit, University College London, UK
L. A. Noronha
Affiliation:
Clinical Psychopharmacology Unit, University College London, UK
S. L. Minchin
Affiliation:
Clinical Psychopharmacology Unit, University College London, UK
H. V. Curran
Affiliation:
Clinical Psychopharmacology Unit, University College London, UK
*
* Address for correspondence: Dr T. P. Freeman, Clinical Psychopharmacology Unit, University College London, Gower Street, London WC1E 6BT, UK. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Smoking is highly prevalent in people diagnosed with schizophrenia, but the reason for this co-morbidity is currently unclear. One possible explanation is that a common abnormality underpins the development of psychosis and independently enhances the incentive motivational properties of drugs and their associated cues. This study aimed to investigate whether incentive salience attribution towards smoking cues, as assessed by attentional bias, is heightened in schizophrenia and associated with delusions and hallucinations.

Method

Twenty-two smokers diagnosed with schizophrenia and 23 control smokers were assessed for smoking-related attentional bias using a modified Stroop task. Craving, nicotine dependence, smoking behaviour and positive and negative symptoms of schizophrenia were also recorded.

Results

Both groups showed similar craving scores and smoking behaviour according to self-report and expired carbon monoxide (CO), although the patient group had higher nicotine dependence scores. Attentional bias, as evidenced by significant interference from smoking-related words on the modified Stroop task, was similar in both groups and correlated with CO levels. Attentional bias was positively related to severity of delusions but not hallucinations or other symptoms in the schizophrenia group.

Conclusions

This study supports the hypothesis that the development of delusions and the incentive motivational aspects of smoking may share a common biological substrate. These findings may offer some explanation for the elevated rates of smoking and other drug use in people with psychotic illness.

Keywords

Aberrant salienceaddictionassociative learningattentional biasdelusionsdopaminedrug cueincentive motivationpsychosissmoking
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 10 , July 2014 , pp. 2189 - 2197
Copyright
Copyright © Cambridge University Press 2013 

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

Andreasen, NC (1984 a). The Scale for the Assessment of Negative Symptoms (SANS). University of Iowa: Iowa City, IA.Google Scholar
Andreasen, NC (1984 b). The Scale for the Assessment of Positive Symptoms (SAPS). University of Iowa: Iowa City, IA.Google Scholar
Awad, AG (2012). Is it time to consider comorbid substance abuse as a new indication for antipsychotic drug development? Journal of Psychopharmacology 26, 953–957.Google Scholar
Berg, SA, Chambers, RA (2008). Accentuated behavioral sensitization to nicotine in the neonatal ventral hippocampal lesion model of schizophrenia. Neuropharmacology 54, 1201–1207.Google Scholar
Berg, SA, Sentir, AM, Cooley, BS, Engleman, EA, Chambers, RA (2013). Nicotine is more addictive, not more cognitively therapeutic in a neurodevelopmental model of schizophrenia produced by neonatal ventral hippocampal lesions. Addiction Biology. Published online: 6 August 2013 . doi: 10.1111/adb.12082.Google Scholar
Chambers, RA, Krystal, JH, Self, DW (2001). A neurobiological basis for substance abuse comorbidity in schizophrenia. Biological Psychiatry 50, 71–83.Google Scholar
Chatterton, R, Sanderson, L, Van Leent, S, Plant, K (1998). Does clozapine affect smoking rates? Australian and New Zealand Journal of Psychiatry 32, 890–891.Google Scholar
Copersino, ML, Serper, MR, Vadhan, N, Goldberg, BR, Richarme, D, Chou, JC, Stitzer, M, Cancro, R (2004). Cocaine craving and attentional bias in cocaine-dependent schizophrenic patients. Psychiatry Research 128, 209–218.Google Scholar
Dawe, S, Gerda, C, Russell, MA, Gray, J (1995). Nicotine intake in smokers increases following a single dose of haloperidol. Psychopharmacology 117, 110–115.Google Scholar
de Leon, J, Diaz, FJ (2005). A meta-analysis of worldwide studies demonstrates an association between schizophrenia and tobacco smoking behaviors. Schizophrenia Research 76, 135–157.Google Scholar
de Leon, J, Diaz, FJ, Josiassen, RC, Cooper, TB, Simpson, GM (2005). Does clozapine decrease smoking? Progress in Neuro-Psychopharmacology and Biological Psychiatry 29, 757–762.Google Scholar
Field, M, Cox, WM (2008). Attentional bias in addictive behaviors: a review of its development, causes, and consequences. Drug and Alcohol Dependence 97, 1–20.Google Scholar
Field, M, Munafò, MR, Franken, IHA (2009). A meta-analytic investigation of the relationship between attentional bias and subjective craving in substance abuse. Psychological Bulletin 135, 589–607.Google Scholar
Fonder, MA, Sacco, KA, Termine, A, Boland, BS, Seyal, AA, Dudas, MM, Vessicchio, JC, George, TP (2005). Smoking cue reactivity in schizophrenia: effects of a nicotinic receptor antagonist. Biological Psychiatry 57, 802–808.Google Scholar
Franken, IHA (2003). Drug craving and addiction: integrating psychological and neuropsychopharmacological approaches. Progress in Neuro-Psychopharmacology and Biological Psychiatry 27, 563–579.Google Scholar
Franken, IHA, Hendriks, VM, Stam, CJ, Van den Brink, W (2004). A role for dopamine in the processing of drug cues in heroin dependent patients. European Neuropsychopharmacology 14, 503–508.Google Scholar
Freeman, TP, Morgan, CJA, Pepper, F, Howes, OD, Stone, JM, Curran, HV (2012). Associative blocking to reward-predicting cues is attenuated in ketamine users but can be modulated by images associated with drug use. Psychopharmacology 225, 41–50.Google Scholar
George, TP, Sernyak, MJ, Ziedonis, DM, Woods, SW (1995). Effects of clozapine on smoking in chronic schizophrenic outpatients. Journal of Clinical Psychiatry 56, 344–346.Google Scholar
Gray, J, Feldon, J, Rawlins, J, Hemsley, D, Smith, A (1991). The neuropsychology of schizophrenia. Behavioral and Brain Sciences 14, 1–20.Google Scholar
Green, A, Drake, R, Brunette, M, Noordsy, D (2007). Schizophrenia and co-occurring substance use disorder. American Journal of Psychiatry 164, 402–408.Google Scholar
Hahn, B, Harvey, AN, Concheiro-Guisan, M, Huestis, MA, Holcomb, HH, Gold, JM (2013). A test of the cognitive self-medication hypothesis of tobacco smoking in schizophrenia. Biological Psychiatry 74, 436–443.Google Scholar
Heatherton, TF, Kozlowski, LT, Frecker, RC, Fagerström, KO (1991). The Fagerström Test for Nicotine Dependence: a revision of the Fagerström Tolerance Questionnaire. British Journal of Addiction 86, 1119–1127.Google Scholar
Heinz, A, Schlagenhauf, F (2010). Dopaminergic dysfunction in schizophrenia: salience attribution revisited. Schizophrenia Bulletin 36, 472–485.CrossRefGoogle ScholarPubMed
Hennekens, CH, Hennekens, AR, Hollar, D, Casey, DE (2005). Schizophrenia and increased risks of cardiovascular disease. American Heart Journal 150, 1115–1121.Google Scholar
Irving, C, Adams, C, Lawrie, S (2006). Haloperidol versus placebo for schizophrenia. Cochrane Database of Systematic Reviews. Issue 4, Art. No. CD003082.Google Scholar
Janes, AC, Pizzagalli, DA, Richardt, S (2010). Brain reactivity to smoking cues prior to smoking cessation predicts ability to maintain tobacco abstinence. Biological Psychiatry 67, 722–729.Google Scholar
Jensen, J, Willeit, M, Zipursky, RB, Savina, I, Smith, AJ, Menon, M, Crawley, AP, Kapur, S (2007). The formation of abnormal associations in schizophrenia: neural and behavioral evidence. Neuropsychopharmacology 33, 473–479.Google Scholar
Jentsch, JD, Taylor, JR (1999). Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology 146, 373–390.Google Scholar
Jones, SH, Gray, JA, Hemsley, DR (1992). Loss of the Kamin blocking effect in acute but not chronic schizophrenics. Biological Psychiatry 32, 739–755.Google Scholar
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.Google Scholar
Kelly, DL, McMahon, RP, Wehring, HJ, Liu, F, Mackowick, KM, Boggs, DL, Warren, KR, Feldman, S, Shim, JC, Love, RC, Dixon, L (2011). Cigarette smoking and mortality risk in people with schizophrenia. Schizophrenia Bulletin 37, 832–838.Google Scholar
Kotov, R, Guey, LT, Bromet, EJ, Schwartz, JE (2010). Smoking in schizophrenia: diagnostic specificity, symptom correlates, and illness severity. Schizophrenia Bulletin 36, 173–181.Google Scholar
Kotz, D, Brown, J, West, R (2012). Predictive validity of the Motivation To Stop Scale (MTSS): a single-item measure of motivation to stop smoking. Drug and Alcohol Dependence 128, 15–19.Google Scholar
Krishnadas, R, Jauhar, S, Telfer, S, Shivashankar, S, McCreadie, RG (2012). Nicotine dependence and illness severity in schizophrenia. British Journal of Psychiatry 201, 306–312.Google Scholar
Kumari, V, Postma, P (2005). Nicotine use in schizophrenia: the self medication hypotheses. Neuroscience and Biobehavioral Reviews 29, 1021–1034.Google Scholar
Leweke, FM, Piomelli, D, Pahlisch, F, Muhl, D, Gerth, CW, Hoyer, C, Klosterkötter, J, Hellmich, M, Koethe, D (2012). Cannabidiol enhances anandamide signaling and alleviates psychotic symptoms of schizophrenia. Translational Psychiatry 2, e94.Google Scholar
Luijten, M, Veltman, DJ, den Brink, W, Hester, R, Field, M, Smits, M, Franken, IHA (2011). Neurobiological substrate of smoking-related attentional bias. NeuroImage 54, 2374–2381.Google Scholar
Luijten, M, Veltman, DJ, Hester, R, Smits, M, Pepplinkhuizen, L, Franken, IHA (2012). Brain activation associated with attentional bias in smokers is modulated by a dopamine antagonist. Neuropsychopharmacology 37, 2772–2779.Google Scholar
Mason, O, Linney, Y, Claridge, G (2005). Short scales for measuring schizotypy. Schizophrenia Research 78, 293–296.Google Scholar
McEvoy, JP, Freudenreich, O, Levin, ED, Rose, JE (1995 a). Haloperidol increases smoking in patients with schizophrenia. Psychopharmacology 119, 124–126.CrossRefGoogle ScholarPubMed
McEvoy, JP, Freudenreich, O, McGee, M, VanderZwaag, C, Levin, ED, Rose, JE (1995 b). Clozapine decreases smoking in patients with chronic schizophrenia. Biological Psychiatry 119, 124–126.Google Scholar
Morgan, CJA, Das, RK, Joye, A, Curran, HV, Kamboj, SK (2013). Cannabidiol reduces cigarette consumption in tobacco smokers: preliminary findings. Addictive Behaviors 38, 2433–2436.Google Scholar
Morgan, CJA, Freeman, TP, Schafer, GL, Curran, HV (2010). Cannabidiol attenuates the appetitive effects of Δ9-tetrahydrocannabinol in humans smoking their chosen cannabis. Neuropsychopharmacology 35, 1879–1885.CrossRefGoogle ScholarPubMed
Murray, G, Corlett, P, Clark, L, Pessiglione, M, Blackwell, AD, Honey, G, Jones, PB, Bullmore, ET, Robbins, TW, Fletcher, PC (2007). Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Molecular Psychiatry 13, 267–276.Google Scholar
Nelson, HE (1991). National Adult Reading Test (NART). NFER-Nelson: Windsor, UK.Google Scholar
Powell, J, Dawkins, L, West, R, Powell, J, Pickering, A (2010). Relapse to smoking during unaided cessation: clinical, cognitive and motivational predictors. Psychopharmacology 212, 537–549.Google Scholar
Robinson, TE, Berridge, KC (1993). The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Research Reviews 18, 247–291.Google Scholar
Roiser, JP, Howes, OD, Chaddock, CA, Joyce, EM, McGuire, P (2012). Neural and behavioral correlates of aberrant salience in individuals at risk for psychosis. Schizophrenia Bulletin. Published online: 12 December 2012 . doi: 10.1093/schbul/sbs147 Google Scholar
Roiser, JP, Stephan, KE, den Ouden, HE, Barnes, TR, Friston, KJ, Joyce, EM (2009). Do patients with schizophrenia exhibit aberrant salience? Psychological Medicine 39, 199–209.Google Scholar
Romaniuk, L, Honey, GD, King, JR, Whalley, HC, McIntosh, AM, Levita, L, Hughes, M, Johnstone, EC, Day, M, Lawrie, SM, Hall, J (2010). Midbrain activation during Pavlovian conditioning and delusional symptoms in schizophrenia. Archives of General Psychiatry 67, 1246–1254.Google Scholar
Tidey, JW, Rohsenow, DJ, Kaplan, GB, Swift, RM, Adolfo, AB (2008). Effects of smoking abstinence, smoking cues and nicotine replacement in smokers with schizophrenia and controls. Nicotine and Tobacco Research 10, 1047–1056.Google Scholar
Tsapakis, EM, Guillin, O, Murray, RM (2003). Does dopamine sensitization underlie the association between schizophrenia and drug abuse? Current Opinion in Psychiatry 16, S45–S52.Google Scholar
Tseng, KY, Chambers, RA, Lipska, BK (2009). The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia. Behavioural Brain Research 204, 295–305.Google Scholar
van Os, J (2009). ‘Salience syndrome’ replaces ‘schizophrenia’ in DSM-V and ICD-11: psychiatry's evidence-based entry into the 21st century? Acta Psychiatrica Scandinavica 120, 363–372.Google Scholar
Vollstädt-Klein, S, Loeber, S, Winter, S, Leménager, T, von der Goltz, C, Dinter, C, Koopmann, A, Wied, C, Winterer, G, Kiefer, F (2011). Attention shift towards smoking cues relates to severity of dependence, smoking behavior and breath carbon monoxide. European Addiction Research 17, 217–224.Google Scholar
Waters, AJ, Shiffman, S, Sayette, MA, Paty, JA, Gwaltney, CJ, Balabanis, MH (2003). Attentional bias predicts outcome in smoking cessation. Health Psychology 22, 378–387.Google Scholar
WHO (1993). The ICD-10 Classification of Mental and Behavioural Disorders: Diagnostic Criteria for Research. World Health Organization: Geneva.Google Scholar
Wing, VC, Wass, CE, Soh, DW, George, TP (2012). A review of neurobiological vulnerability factors and treatment implications for comorbid tobacco dependence in schizophrenia. Annals of the New York Academy of Sciences 1248, 89–106.CrossRefGoogle ScholarPubMed