Abstract
Rationale
Smoking is highly prevalent in schizophrenia, and there is evidence for beneficial effects on neurocognition. Smoking is therefore hypothesized a self-medication in schizophrenia. Although much effort is devoted to characterize those cognitive domains that potentially benefit from smoking, divided attention has not yet been investigated.
Objectives
The aim of this study was to analyze the interactional effects of diagnosis of schizophrenia and smoking history on divided attention.
Methods
We investigated behavioral measures of divided attention in a sample of 48 schizophrenic patients and 48 controls (24 current smokers and non-smokers each) carefully matched for age, sex, education, verbal IQ, and smoking status with general linear models.
Results
Most important within the scope of this study, significant interactions were found for valid reactions and errors of omission: Performance substantially increased in smoking schizophrenic patients, but not in controls. Further, these interactions were modified by sex, driven by female schizophrenic patients who showed a significant behavioral advantage of smokers over non-smokers, other than male schizophrenic patients or healthy controls who did not express this sex-specific pattern.
Conclusions
Results suggest a positive effect of smoking history on divided attention in schizophrenic patients. This study provides first evidence that the complex attention domain of divided attention is improved by smoking, which further substantiates the self-medication hypothesis of smoking in schizophrenia, although this has been shown mainly for sustained and selective attention. Gender-specific effects on cognition need to be further investigated.
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References
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. Biol Psychiatry 67(3):255–262
Avila MT, Sherr JD, Hong E, Myers CS, Thaker GK (2003) Effects of nicotine on leading saccades during smooth pursuit eye movements in smokers and nonsmokers with schizophrenia. Neuropsychopharmacology 28(12):2184–2191
Barr RS, Culhane MA, Jubelt LE, Mufti RS, Dyer MA, Weiss AP, Deckersbach T, Kelly JF, Freudenreich O, Goff DC, Evins AE (2008) The effects of transdermal nicotine on cognition in nonsmokers with schizophrenia and nonpsychiatric controls. Neuropsychopharmacology 33(3):480–490
Chambers RA, Krystal JH, Self DW (2001) A neurobiological basis for substance abuse comorbidity in schizophrenia. Biol Psychiatry 50(2):71–83
Coull JT, Frith CD, Dolan RJ, Frackowiak RS, Grasby PM (1997) The neural correlates of the noradrenergic modulation of human attention, arousal and learning. Eur J Neurosci 9(3):589–598
Depatie L, O'Driscoll GA, Holahan AL, Atkinson V, Thavundayil JX, Kin NN, Lal S (2002) Nicotine and behavioral markers of risk for schizophrenia: a double-blind, placebo-controlled, cross-over study. Neuropsychopharmacology 27(6):1056–1070
Ernst M, Heishman SJ, Spurgeon L, London ED (2001) Smoking history and nicotine effects on cognitive performance. Neuropsychopharmacology 25(3):313–319
George TP, Vessicchio JC, Termine A, Sahady DM, Head CA, Pepper WT, Kosten TR, Wexler BE (2002) Effects of smoking abstinence on visuospatial working memory function in schizophrenia. Neuropsychopharmacology 26(1):75–85
Goldstein JM, Seidman LJ, Goodman JM, Koren D, Lee H, Weintraub S, Tsuang MT (1998) Are there sex differences in neuropsychological functions among patients with schizophrenia? Am J Psychiatry 155(10):1358–1364
Hahn B, Ross TJ, Wolkenberg FA, Shakleya DM, Huestis MA, Stein EA (2009) Performance effects of nicotine during selective attention, divided attention, and simple stimulus detection: an fMRI study. Cereb Cortex 19(9):1990–2000
Hahn C, Hahn E, Dettling M, Gunturkun O, Ta TM, Neuhaus AH (2012) Effects of smoking history on selective attention in schizophrenia. Neuropharmacology 62(4):1897–1902
Harris JG, Kongs S, Allensworth D, Martin L, Tregellas J, Sullivan B, Zerbe G, Freedman R (2004) Effects of nicotine on cognitive deficits in schizophrenia. Neuropsychopharmacology 29(7):1378–1385
Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom KO (1991) The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br J Addict 86(9):1119–1127
Imperato A, Mulas A, Di Chiara G (1986) Nicotine preferentially stimulates dopamine release in the limbic system of freely moving rats. Eur J Pharmacol 132(2–3):337–338
Jacobs E, D'Esposito M (2011) Estrogen shapes dopamine-dependent cognitive processes: implications for women's health. J Neurosci 31(14):5286–5293
Jacobsen LK, D'Souza DC, Mencl WE, Pugh KR, Skudlarski P, Krystal JH (2004) Nicotine effects on brain function and functional connectivity in schizophrenia. Biol Psychiatry 55(8):850–858
Jacobsen LK, Krystal JH, Mencl WE, Westerveld M, Frost SJ, Pugh KR (2005) Effects of smoking and smoking abstinence on cognition in adolescent tobacco smokers. Biol Psychiatry 57(1):56–66
Lawrence NS, Ross TJ, Stein EA (2002) Cognitive mechanisms of nicotine on visual attention. Neuron 36(3):539–548
Lehrl S, Triebig G, Fischer B (1995) Multiple choice vocabulary test MWT as a valid and short test to estimate premorbid intelligence. Acta Neurol Scand 91(5):335–345
Leonard S, Mexal S, Freedman R (2007) Smoking, genetics and schizophrenia: evidence for self medication. J Dual Diagn 3(3–4):43–59
Lu Y, Wang SS, Reynolds P, Chang ET, Ma H, Sullivan-Halley J, Clarke CA, Bernstein L (2011) Cigarette smoking, passive smoking, and non-Hodgkin lymphoma risk: evidence from the California teachers study. Am J Epidemiol 174(5):563–573
Neuhaus AH, Opgen-Rhein C, Urbanek C, Gross M, Hahn E, Ta TM, Koehler S, Dettling M (2009) Spatiotemporal mapping of sex differences during attentional processing. Hum Brain Mapp 30(9):2997–3008
Newhouse PA, Potter A, Singh A (2004) Effects of nicotinic stimulation on cognitive performance. Curr Opin Pharmacol 4(1):36–46
Palomero-Gallagher N, Vogt BA, Schleicher A, Mayberg HS, Zilles K (2009) Receptor architecture of human cingulate cortex: evaluation of the four-region neurobiological model. Hum Brain Mapp 30(8):2336–2355
Rezvani AH, Levin ED (2001) Cognitive effects of nicotine. Biol Psychiatry 49(3):258–267
Roesch-Ely D, Hornberger E, Weiland S, Hornstein C, Parzer P, Thomas C, Weisbrod M (2009) Do sex differences affect prefrontal cortex associated cognition in schizophrenia? Schizophr Res 107(2–3):255–261
Sacco KA, Termine A, Seyal A, Dudas MM, Vessicchio JC, Krishnan-Sarin S, Jatlow PI, Wexler BE, George TP (2005) Effects of cigarette smoking on spatial working memory and attentional deficits in schizophrenia: involvement of nicotinic receptor mechanisms. Arch Gen Psychiatry 62(6):649–659
Sacher J, Okon-Singer H, Villringer A (2013) Evidence from neuroimaging for the role of the menstrual cycle in the interplay of emotion and cognition. Front Hum Neurosci 7:374
Segarra R, Zabala A, Eguiluz JI, Ojeda N, Elizagarate E, Sanchez P, Ballesteros J, Gutierrez M (2011) Cognitive performance and smoking in first-episode psychosis: the self-medication hypothesis. Eur Arch Psychiatry Clin Neurosci 261(4):241–250
Shen C, Popescu FC, Hahn E, Ta TT, Dettling M, Neuhaus AH (2013) Neurocognitive pattern analysis reveals classificatory hierarchy of attention deficits in schizophrenia. Schizophr Bull
Smith RC, Singh A, Infante M, Khandat A, Kloos A (2002) Effects of cigarette smoking and nicotine nasal spray on psychiatric symptoms and cognition in schizophrenia. Neuropsychopharmacology 27(3):479–497
Stein EA, Pankiewicz J, Harsch HH, Cho JK, Fuller SA, Hoffmann RG, Hawkins M, Rao SM, Bandettini PA, Bloom AS (1998) Nicotine-induced limbic cortical activation in the human brain: a functional MRI study. Am J Psychiatry 155(8):1009–1015
Uban KA, Rummel J, Floresco SB, Galea LA (2012) Estradiol modulates effort-based decision making in female rats. Neuropsychopharmacology 37(2):390–401
Vijayraghavan S, Wang M, Birnbaum SG, Williams GV, Arnsten AF (2007) Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nat Neurosci 10(3):376–384
Vohn R, Fimm B, Weber J, Schnitker R, Thron A, Spijkers W, Willmes K, Sturm W (2007) Management of attentional resources in within-modal and cross-modal divided attention tasks: An fMRI study. Hum Brain Mapp 28(12):1267–1275
Winterer G (2010) Why do patients with schizophrenia smoke? Curr Opin Psychiatry 23(2):112–119
Zimmermann P, Fimm B (1992) Testbatterie zur Aufmerksamkeitsprüfung (tap). Psytest, Freiburg
Acknowledgments
We would like to thank all participants of this study for contributing their time and effort. This study is part of the doctoral thesis of Elnaz Goudarzi.
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There is no conflict of interest for any of the authors.
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Eike Ahlers and Eric Hahn contributed equally to this work.
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Ahlers, E., Hahn, E., Ta, T.M.T. et al. Smoking improves divided attention in schizophrenia. Psychopharmacology 231, 3871–3877 (2014). https://doi.org/10.1007/s00213-014-3525-2
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DOI: https://doi.org/10.1007/s00213-014-3525-2