Skip to main content
SpringerLink
Log in

Smoking impacts on prefrontal attentional network function in young adult brains

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

There is abundant evidence from clinical and preclinical studies that acute administration of nicotine has beneficial effects on attentional network function in the brain. In contrast, little is known about potentially neurotoxic effects on the attentional network during neurodevelopmentally critical periods, such as during adolescence and early adulthood.

Methods

Using event-related functional MRI (fMRI), we investigated prefrontal attentional network function in young adults (n=15 regular smokers and n=12 never-smokers; age: 22.6±1.5 years). Duration of smoking was 6.9±2.3 years (range of 2–10). Smokers were allowed to smoke ad libitum before the fMRI scanning was conducted.

Results

As expected from literature, prefrontal attentional network activity was significantly reduced in smokers compared to nonsmokers (Z=2.1; P=0.036). In smokers, we found that the history of smoking duration (years) is directly related to the extent of diminished attentional network activity (R=−0.67; P=0.012).

Conclusions

To our best knowledge, the relationship between the duration of smoking history and prefrontal attentional network function has not yet been reported. This finding might suggest that several years of chronic nicotine abuse may be sufficient to exert long-lasting effects on the brain function of adolescents and young adults.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adan A, Prat G, Sanchez-Turet M (2004) Effects of nicotine dependence on diurnal variations of subjective activation and mood. Addiction 99:1599–1607

    Article  PubMed  Google Scholar 

  • Adriani W, Laviola G (2004) Windows of vulnerability to psychopathology and therapeutic strategy in adolescent rodent models. Behav Pharmacol 15:341–352

    Article  PubMed  CAS  Google Scholar 

  • Adriani W, Spijker S, Deroche-Gamonet V, Laviola G, Le Moal M, Smit AB, Piazza PV (2003) Evidence for enhanced neurobehavioral vulnerability to nicotine during periadolescence in rats. J Neurosci 23:4712–4716

    PubMed  CAS  Google Scholar 

  • Adriani W, Granstrem O, Macri S, Izykenova G, Dambinova S, Laviola G (2004) Behavioral and neurochemical vulnerability during adolescence in mice: studies with nicotine. Neuropsychopharmacology 29:869–878

    Article  PubMed  CAS  Google Scholar 

  • Arseneault L, Cannon M, Poulton R, Murray R, Caspi A, Moffitt TE (2002) Cannabis use in adolescence and risk for adult psychosis: longitudinal prospective study. Br Med J 325:1212–1213

    Article  Google Scholar 

  • Barron S, White A, Swartzwelder HS, Bell RL, Rodd ZA, Slawecki CJ, Ehlers CL, Levin ED, Rezvani AH, Spear LP (2005) Adolescent vulnerabilities to chronic alcohol or nicotine exposure: findings from rodent models. Alcohol Clin Exp Res 29:1720–1725

    Article  PubMed  CAS  Google Scholar 

  • Behrens T, Woolrich MW, Smith S (2003) Multi-testing using a fully subject null hypothesis Bayesian framework: theory. In: Human Brain Mapping Meeting, New York Marriott Marquis, New York, 18–22 June 2003

  • Braak H, Del Tredici K, Schultz C, Braak E (2000) Vulnerability of select neuronal types to Alzheimer’s disease. Ann N Y Acad Sci 924:53–61

    Article  PubMed  CAS  Google Scholar 

  • Coull JT (1998) Neural correlates of attention and arousal: insights from electrophysiology, functional neuroimaging, and psychopharmacology. Prog Neurobiol 55:343–361

    Article  PubMed  CAS  Google Scholar 

  • Coull JT, Frith CD, Frackowiak RSJ, Grasby PM (1996) A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory. Neuropsychologia 34:1085–1095

    Article  PubMed  CAS  Google Scholar 

  • Edwards JA, Wesnes K, Warburton DM, Gale A (1985) Evidence of more rapid stimulus evaluation following cigarette smoking. Addict Behav 10:113–26

    Article  PubMed  CAS  Google Scholar 

  • Eisenberg T, Griffiths RR, Stitzer M (1996) Mecamylamine does not precipitate withdrawal in cigarette smokers. Psychopharmacology 127:328–336

    Article  Google Scholar 

  • Ernst M, Moolchan ET, Robinson ML (2001a) Behavioral and neural consequences of prenatal exposure to nicotine. J Am Acad Child Adolesc Psychiatry 44:630–641

    Article  Google Scholar 

  • Ernst M, Matochik JA, Heishman SJ, Van Horn JD, Jons PH, Henningfield JE, London ED (2001b) Effect of nicotine on brain activation during performance of a working memory task. Proc Natl Acad Sci USA 98:4728–4733

    Article  PubMed  CAS  Google Scholar 

  • Ernst M, Heishman SJ, Spurgeon L, London ED (2001c) Smoking history and nicotine effects on cognitve performance. Neuropsychopharmacology 25:313–319

    Article  PubMed  CAS  Google Scholar 

  • First MB, Spitzer RL, Gibbon M, Williams JB (1995) The structured clinical interview for DSM-IV axis I disorders research version (SCID-1). American Psychiatric Press, New York

    Google Scholar 

  • Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33:636–647

    PubMed  CAS  Google Scholar 

  • Friston KJ, Worsley KJ, Frakowiak RSJ, Mazziotta JC, Evans AC (1994) Assessing the significance of focal activations using their spatial extent. Hum Brain Mapp 1:214–220

    Article  Google Scholar 

  • Gardner TW, Dishion TJ, Posner MI (2006) Attention and adolescent tobacco use: a potential self-regulatory dynamic underlying nicotine addiction. Addict Behav 31:531–536

    Article  PubMed  Google Scholar 

  • Gilbert D, McClernon J, Rabinovich N, Sugai C, Plath L, Asgaard G, Zuo Y, Huggenvik J, Botros N (2004) Effects of quitting smoking on EEG activation and attention last for more than 31 days and are more severe with stress, dependence, DRD2 A1 allele, and depressive traits. Nicotine Tob Res 6:249–267

    Article  PubMed  CAS  Google Scholar 

  • Hahn B, Shoaib M, Stolerman IP (2002) Nicotine-induced enhancement of attention in the five-choice serial reaction time task: the influence of task demands. Psychopharmacology (Berl) 162:129–37

    Article  CAS  Google Scholar 

  • Hahn B, Sharples CG, Wonnacott S, Shoaib M, Stolerman IP (2003) Attentional effects of nicotinic agonists in rats. Neuropharmacology 44:1054–1067

    Article  PubMed  CAS  Google Scholar 

  • 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 29:1378–1385

    Article  PubMed  CAS  Google Scholar 

  • Houlihan ME, Pritchard WS, Krieble KK, Robinson JH, Duke DW (1996a) Effects of cigarette smoking on EEG spectral-band power, dimensional complexity, and nonlinearity during reaction-time task performance. Psychophysiology 33:740–746

    Article  PubMed  CAS  Google Scholar 

  • Houlihan ME, Pritchard WS, Robinson JH (1996b) Faster P300 latency after smoking in visual but not auditory oddball tasks. Psychopharmacology 123:231–238

    Article  PubMed  CAS  Google Scholar 

  • 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 55:850–858

    Article  PubMed  CAS  Google Scholar 

  • 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 57:56–66

    Article  PubMed  Google Scholar 

  • Jacobsen LK, Slotkin TA, Westerveld M, Mencl WE, Pugh KR (2006) Visuospatial memory deficits emerging during nicotine withdrawal in adolescents with prenatal exposure to active maternal smoking. Neuropsychopharmacology 31:1550–1561

    Article  PubMed  CAS  Google Scholar 

  • Jenkinson M, Bannister P, Brady J, Smith S (2002) Improved optimisation for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841

    Article  PubMed  Google Scholar 

  • Kandel DB, Chen K (2000) Extent of smoking and nicotine dependence in the United States: 1991–1993. Nicotine Tob Res 2:263–274

    Article  PubMed  CAS  Google Scholar 

  • Kaplan E, Fein D, Morris R, Delis D (1991) WAIS-R as a neuropsychological instrument. The Psychological Corporation, New York

    Google Scholar 

  • Kumari V, Gray JA, Ffytche DH, Mitterschiffthaler MT, Das M, Zachariah E, Vythelingum GN, Williams SC, Simmons A, Sharma T (2003) Cognitive effects of nicotine in humans: an fMRI study. Neuroimage 19:1002–1013

    Article  PubMed  Google Scholar 

  • Kwon H, Reiss AL, Menon V (2002) Neural basis of protracted developmental changes in visuospatial working memory. Proc Natl Acad Sci USA 99:13336–13341

    Article  PubMed  CAS  Google Scholar 

  • Lambert NM, Hartsough CS (1998) Prospektive study of tobacco smoking and substance dependencies among samples of ADHD and non-ADHD participants. J Learn Disabil 31:533–544

    PubMed  CAS  Google Scholar 

  • Laviola G, Adriani W, Terranova ML, Gerra G (1999) Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models. Neurosci Biobehav Rev 23:993–1010

    Article  PubMed  CAS  Google Scholar 

  • Lawrence NS, Ross TJ, Stein EA (2002) Cognitive mechanisms of nicotine on visual attention. Neuron 36:539–548

    Article  PubMed  CAS  Google Scholar 

  • Muir JL, Everitt BJ, Robbins TW (1994) AMPA-induced excitotoxic lesions of the basal forebrain: a significant role fort he cortical cholinergic system in attentional function. J Neurosci 14:2313–2326

    PubMed  CAS  Google Scholar 

  • Mulert C, Gallinat J, Pascual-Marqui R, Dorn H, Frick K, Schlattmann P, Mientus S, Herrmann WM, Winterer G (2001) Reduced event-related current density in the anterior cingulate cortex in schizophrenia. Neuroimage 13:589–600

    Article  PubMed  CAS  Google Scholar 

  • Musso F, Konrad A, Vucurevic G, Schäffner C, Friedrich B, Frech P, Stoeter P, Winterer G (2006) Distributed BOLD response in association cortex vector state space predicts reaction time during selective attention. Neuroimage 29:1311–1318

    Article  PubMed  Google Scholar 

  • Nyback H, Nordberg A, Langstrom B, Halldin C, Hartvig P, Ahlin A, Swahn CG, Sedvall G (1989) Attempts to visualize nicotinic receptors in the brain of monkey and man by positron emission tomography. Prog Brain Res 79:313–319

    Article  PubMed  CAS  Google Scholar 

  • O’Loughlin J, DiFranza J, Tyndale RF, Meshfedjian G, McMillan-Davey E, Clarke PB, Hanley J, Paradis G (2003) Nicotine-dependence symptoms are associated with smoking frequency in adolescents. Am J Prev Med 25:219–225

    Article  PubMed  Google Scholar 

  • Piasecki TM, Jorenby DE, Smith SS, Fiore MC (2005) Smoking withdrawal dynamics: III. Correlates of withdrawal heterogeneity. Exp Clin Psychopharmacol 11:276–285

    Google Scholar 

  • Rezvani AH, Levin ED (2001) Cognitive effects of nicotine. Biol Psychiatry 49:258–267

    Article  PubMed  CAS  Google Scholar 

  • Rezvani AH, Levin ED (2004) Adolescent and adult rats respond differently to nicotine and alcohol: motor activity and body temperature. Int J Dev Neurosci 22:349–354

    Article  PubMed  CAS  Google Scholar 

  • Sacco KA, Bannon KL, George TP (2004) Nicotinic receptor mechanisms and cognition in normal states and neuropsychiatric disorders. J Psychopharmacol 18:457–474

    Article  PubMed  CAS  Google Scholar 

  • Sarter M, Givens B, Bruno JP (2001) The cognitive neuroscience of sustained attention: where top-down meets bottom-up. Brain Res Rev 35:146–160

    Article  PubMed  CAS  Google Scholar 

  • Sherwood N, Kerr JS, Hindmarch I (1992) Psychomotor performance in smokers following single and repeated doses of nicotine gum. Psychopharmacology (Berl) 108:432–436

    Article  CAS  Google Scholar 

  • Shoaib M, Bizarro L (2004) Deficits in a sustained attention task following nicotine withdrawal in rats. Psychopharmacology (Berl) 178:211–222

    Article  CAS  Google Scholar 

  • Slawecki CJ, Thorsell A, Ehlers CL (2004) Long-term neurobehavioral effects of alcohol or nicotine exposure in adolescent animal models. Ann N Y Acad Sci 1021:448–452

    Article  PubMed  CAS  Google Scholar 

  • Slawecki CJ, Thorsell AK, Khoury AE, Mathe AA, Ehlers CL (2005) Increased CRF-like and NPY-like immunoreactivity in adult rats exposed to nicotine during adolescence: relation to anxiety-like and depressive-like behavior. Neuropeptides 39:369–377

    Article  PubMed  CAS  Google Scholar 

  • Smith S (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155

    Article  PubMed  Google Scholar 

  • Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW (1999) In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 2:859–861

    Article  PubMed  CAS  Google Scholar 

  • Sowell ER, Thompson PM, Tessner KD, Toga AW (2001) Mapping continued brain growth and gray matter density reduction in dorsal frontalcortex: inverse relationships during postadolescent brain maturation. J Neurosci 21:8819–8829

    PubMed  CAS  Google Scholar 

  • Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463

    Article  PubMed  CAS  Google Scholar 

  • 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 155:1009–1015

    PubMed  CAS  Google Scholar 

  • Stolerman IP, Mirza NR, Hahn B, Shoaib M (2000) Nicotine in an animal model of attention. Eur J Pharmacol 393:147–154

    Article  PubMed  CAS  Google Scholar 

  • Tewes U (1991) Hamburg-Wechsler-Intelligenztest für Erwachsene. HAWIE-R. Huber, Bern

    Google Scholar 

  • Thiel CM, Zilles K, Fink GR (2005) Nicotine modulates reorienting of visuospatial attention and neural activity in human parietal cortex. Neuropsychopharmacology 30:810–820

    PubMed  CAS  Google Scholar 

  • Trauth JA, Seidler FJ, McCook EC, Slotkin TA (1999) Adolescent nicotine exposure causes persistent upregulation of nicotinic cholinergic receptors in rat brain regions. Brain Res 851:9–19

    Article  PubMed  CAS  Google Scholar 

  • Tregellas JR, Tanabe JL, Martin LF, Freedman R (2005) FMRI of response to nicotine during a smooth pursuit eye movement task in schizophrenia. Am J Psychiatry 162:391–393

    Article  PubMed  Google Scholar 

  • Voytko ML, Olton DS, Richardson RT, Gorman LK, Tobin JR, Price DL (1994) Basal forebrain lesions disrupt attention but not learning and memory. J Neurosci 14:167–186

    PubMed  CAS  Google Scholar 

  • Webster MJ, Weickert CS, Herman MM, Kleinman JE (2002) BDNF mRNA expression during postnatal development, maturation and aging of the human prefrontal cortex. Brain Res Dev Brain Res 139:139–150

    Article  PubMed  CAS  Google Scholar 

  • Wesnes K, Warburton DM (1983) Effects of smoking on rapid information processing performance. Neuropsychobiology 9:223–229

    Article  PubMed  CAS  Google Scholar 

  • Winterer G, Mulert C, Mientus S, Gallinat J, Schlattmann P, Dorn H, Herrmann WM (2001) P300 and LORETA: comparison of normal subjects and schizophrenic patients. Brain Topogr 13:299–313

    Article  PubMed  CAS  Google Scholar 

  • Winterer G, Adams CA, Jones DW, Knutson B (2002) Volition to action—an event-related fMRI study. Neuroimage 17:851–858

    Article  PubMed  Google Scholar 

  • Winterer G, Musso F, Beckmann C, Mattay V, Egan MF, Jones DW, Callicott JH, Coppola R, Weinberger DR (2006a) Instability of prefrontal signal processing in schizophrenia. Am J Psychiatry (in press)

  • Winterer G, Hariri AR, Goldman D, Weinberger DR (2006b) Neuroimaging and human genetics. Int Rev Neurobiol 67PB:325–383

    Google Scholar 

  • Woolrich MW, Ripley BD, Brady JM, Smith SM (2001) Temporal autocorrelation in univariate linear modelling of FMRI data. Neuroimage 14:1370–1386

    Article  PubMed  CAS  Google Scholar 

  • Worsley KJ, Evans AC, Marrett S, Neelin P (1992) A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab 12:900–918

    PubMed  CAS  Google Scholar 

  • Zubieta J, Lombardi U, Minoshima S, Guthrie S, Ni L, Ohl LE, Koeppe RA, Domino EF (2001) Regional cerebral blood flow effects of nicotine in overnight abstinent smokers. Biol Psychiatry 49:906–913

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Psychiatry, Heinrich-Heine University, Bergische Landstr. 2, 40629, Duesseldorf, Germany

    Francesco Musso, Franziska Bettermann & Georg Winterer

  2. Institute of Neuroradiology, Johannes Gutenberg-University, Mainz, Germany

    Goran Vucurevic & Peter Stoeter

  3. Department of Psychiatry, Johannes Gutenberg-University, Mainz, Germany

    Francesco Musso, Andreas Konrad & Georg Winterer

Authors
  1. Francesco Musso
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Franziska Bettermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Goran Vucurevic
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peter Stoeter
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andreas Konrad
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Georg Winterer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Georg Winterer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Musso, F., Bettermann, F., Vucurevic, G. et al. Smoking impacts on prefrontal attentional network function in young adult brains. Psychopharmacology 191, 159–169 (2007). https://doi.org/10.1007/s00213-006-0499-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-006-0499-8

Keywords

Search

Navigation