Abstract
Rationale
Several studies provide evidence that nicotine alleviates the detrimental effects of distracting sensory stimuli. It is been suggested that nicotine may either act as a stimulus filter that prevents irrelevant stimuli entering awareness or by enhancing the attentional focus to relevant stimuli via a boost in processing capacity.
Objectives
To differentiate between these two accounts, we administered nicotine to healthy non-smokers and investigated distractor interference in a visual search task with low and high perceptual load to tax processing capacity.
Methods
Thirty healthy non-smokers received either 7 mg transdermal nicotine or a matched placebo in a double blind within subject design 1 h prior to performing the visual search task with different fixation distractors.
Results
Nicotine reduced interference of incongruent distractors, but only under low-load conditions, where distractor effects were large. No effects of nicotine were observed under high-load conditions. Highly distractible subjects showed the largest effects of nicotine.
Conclusions
The findings suggest that nicotine acts primarily as a stimulus filter that prevents irrelevant stimuli from entering awareness in situations of high distractor interference.
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References
Beck DM, Lavie N (2005) Look here but ignore what you see: effects of distractors at fixation. J Exp Psychol Hum Percept Perform 31:592–607
Berry AS, Demeter E, Sabhapathy S, English BA, Blakely RD, Sarter M, Lustig C (2014) Disposed to distraction: genetic variation in the cholinergic system influences distractibility but not time-on-task effects. J Cogn Neurosci 26(9):1981–1991
Bond A, Lader M (1974) The use of analogue scales in rating subjective feelings. Br J Med Psychol 47:211–218
De la Salle S, Smith D, Choueiry J, Impey D, Philippe T, Dort H, Millar A, Albert P, Knott V (2013) Effects of COMT genotype on sensory gating and its modulation by nicotine: Differences in low and high P50 suppressors. Neuroscience 241:147–156
Dumas JA, Newhouse PA (2011) The cholinergic hypothesis of cognitive aging revisited again: cholinergic functional compensation. Pharmacol Biochem Behav 99:254–261
Duncan J, Humphreys GW (1989) Visual search and stimulus similarity. Psychol Rev 96:433–458
Eriksen BA, Eriksen CW (1974) Effects of noise letters upon the identification of a target letter in a nonsearch task. Percept Psychophys 16:143–149
Espeseth T, Sneve MH, Rootwelt H, Laeng B (2010) Nicotinic receptor gene CHRNA4 interacts with processing load in attention. PLoS One 5:e14407
Forster S, Lavie N (2007) High perceptual load makes everybody equal: eliminating individual differences in distractibility with load. Psychol Sci 18:377–381
Forster S, Lavie N (2008) Failures to ignore entirely irrelevant distractors: the role of load. J Exp Psy 14:73–83
Foulds J, Stapleton J, Swettenham J, Bell N, McSorley K, Russell MA (1996) Cognitive performance effects of subcutaneous nicotine in smokers and never-smokers. Psychopharmacology (Berl) 127:31–38
Giessing C, Fink GR, Rosler F, Thiel CM (2007) fMRI data predict individual differences of behavioral effects of nicotine: a partial least square analysis. J Cogn Neurosci 19:658–670
Gilbert DG, Izetelny A, Radtke R, Hammersley J, Rabinovich NE, Jameson TR, Huggenvik JI (2005) Dopamine receptor (DRD2) genotype-dependent effects of nicotine on attention and distraction during rapid visual information processing. Nicotine Tob Res: Off J Soc Res Nicotine Tob 7:361–379
Gill TM, Sarter M, Givens B (2000) Sustained visual attention performance-associated prefrontal neuronal activity: evidence for cholinergic modulation. J Neurosci 20:4745–4757
Gorsline J, Okerholm RA, Rolf CN, Moos CD, Hwang SS (1992) Comparison of plasma nicotine concentrations after application of nicoderm (nicotine transdermal system) to different skin sites. J Clin Pharmacol 32:576–581
Gorsline J, Gupta SK, Dye D, Rolf CN (1993) Steady-state pharmacokinetics and dose relationship of nicotine delivered from Nicoderm (Nicotine Transdermal System). J Clin Pharmacol 33:161–168
Grobe JE, Perkins KA, Goettler-Good J, Wilson A (1998) Importance of environmental distractors in the effects of nicotine on short-term memory. Exp Clin Psychopharmacol 6:209–216
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) 162:129–137
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 19:1990–2000
Hammersley JJ, Rzetelny A, Gilbert DG, Rabinovich NE, Small SL, Huggenvik JI (2013) Effects of nicotine on emotional distraction of attentional orienting: evidence of possible moderation by dopamine type 2 receptor genotype. Pharmacol Biochem Behav 105:199–204
Heishman SJ, Henningfield JE (2000) Tolerance to repeated nicotine administration on performance, subjective, and physiological responses in nonsmokers. Psychopharmacology (Berl) 152:321–333
Heishman SJ, Kleykamp BA, Singleton EG (2010) Meta-analysis of the acute effects of nicotine and smoking on human performance. Psychopharmacology (Berl) 210:453–469
Howe WM, Ji J, Parikh V, Williams S, Mocaer E, Trocme-Thibierge C, Sarter M (2010) Enhancement of attentional performance by selective stimulation of alpha4beta2(*) nAChRs: underlying cholinergic mechanisms. Neuropsychopharmacology 35:1391–1401
Jacobsen LK, Pugh KR, Mencl WE, Gelernter J (2006) C957T polymorphism of the dopamine D2 receptor gene modulates the effect of nicotine on working memory performance and cortical processing efficiency. Psychopharmacology (Berl) 188:530–540
Kassel JD (1997) Smoking and attention: a review and reformulation of the stimulus-filter hypothesis. Clin Psychol Rev 17:451–478
Knott VJ, Scherling CS, Blais CM, Camarda J, Fisher DJ, Millar A, McIntosh JF (2006) Acute nicotine fails to alter event-related potential or behavioral performance indices of auditory distraction in cigarette smokers. Nicotine Tob Res: Off J Soc Res Nicotine Tob 8:263–273
Knott VJ, Bolton K, Heenan A, Shah D, Fisher DJ, Villeneuve C (2009) Effects of acute nicotine on event-related potential and performance indices of auditory distraction in nonsmokers. Nicotine Tob Res 11:519–530
Knott V, Heenan A, Shah D, Bolton K, Fisher D, Villeneuve C (2011) Electrophysiological evidence of nicotine’s distracter-filtering properties in non-smokers. J Psychopharmacol 25:239–248
Knott V, del la Salle S, Smith D, Philippe T, Dort H, Choueiry J, Impey D (2013) Baseline dependency of nicotine’s sensory gating actions: similarities and differences in low, medium and high P50 suppressors. J Psychopharmacol 27:790–800
Lavie N (1995) Perceptual load as a necessary condition for selective attention. J Exp Psy 3:451–468
Lavie N, Cox S (1997) On the efficiency of attentional selection: efficient visual search results in inefficient rejection of distraction. Psychol Sci 8:395–398
Lawrence NS, Ross TJ, Stein EA (2002) Cognitive mechanisms of nicotine on visual attention. Neuron 36:539–548
Levin ED, Conners CK, Silva D, Hinton SC, Meck WH, March J, Rose JE (1998) Transdermal nicotine effects on attention. Psychopharmacology (Berl) 140:135–141
Levin ED, McClernon FJ, Rezvani AH (2006) Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology (Berl) 184:523–539
Mancuso G, Warburton DM, Melen M, Sherwood N, Tirelli E (1999) Selective effects of nicotine on attentional processes. Psychopharmacology (Berl) 146:199–204
Markett S, Montag C, Diekmann C, Reuter M (2014) Dazed and confused: a molecular genetic approach to everyday cognitive failure. Neurosci Lett 566:216–220
Mathalon DH, Ahn KH, Perry EB Jr, Cho HS, Roach BJ, Blais RK, Bhakta S, Ranganathan M, Ford JM, D’Souza DC (2014) Effects of nicotine on the neurophysiological and behavioral effects of ketamine in humans. Front Psychiatry 5:3. doi:10.3389/fpsyt.2014.00003. eCollection 2014
Maylor EA, Lavie N (1998) The influence of perceptual load on age differences in selective attention. Psychol Aging 13:563–573
Meinke A, Thiel CM, Fink GR (2006) Effects of nicotine on visuo-spatial selective attention as indexed by event-related potentials. Neuroscience 141:201–212
Miller J (1991) The flanker compatibility effect as a function of visual angle, attentional focus, visual transients, and perceptual load: a search for boundary conditions. Percept Psychophys 49:270–288
Murphy FC, Klein RM (1998) The effects of nicotine on spatial and non-spatial expectancies in a covert orienting task. Neuropsychologia 36:1103–1114
Newhouse PA, Potter A, Singh A (2004) Effects of nicotinic stimulation on cognitive performance. Curr Opin Pharmacol 4:36–46
Parikh V, St Peters M, Blakely RD, Sarter M (2013) The presynaptic choline transporter imposes limits on sustained cortical acetylcholine release and attention. J Neurosci 33:2326–2337
Perkins KA (1999) Baseline-dependency of nicotine effects: a review. Behav Pharmacol 10:597–615
Phillips JM, McAlonan K, Robb WG, Brown VJ (2000) Cholinergic neurotransmission influences covert orientation of visuospatial attention in the rat. Psychopharmacology (Berl) 150:112–116
Poltavski DV, Petros T (2006) Effects of transdermal nicotine on attention in adult non-smokers with and without attentional deficits. Physiol Behav 87:614–624
Potter AS, Bucci DJ, Newhouse PA (2012) Manipulation of nicotinic acetylcholine receptors differentially affects behavioral inhibition in human subjects with and without disordered baseline impulsivity. Psychopharmacology (Berl) 220:331–340
Prendergast MA, Jackson WJ, Terry AV Jr, Decker MW, Arneric SP, Buccafusco JJ (1998) Central nicotinic receptor agonists ABT-418, ABT-089, and (−)-nicotine reduce distractibility in adult monkeys. Psychopharmacology (Berl) 136:50–58
Rycroft N, Rusted JM, Hutton SB (2005) Acute effects of nicotine on visual search tasks in young adult smokers. Psychopharmacology (Berl) 181:160–169
St Peters M, Demeter E, Lustig C, Bruno JP, Sarter M (2011) Enhanced control of attention by stimulating mesolimbic-corticopetal cholinergic circuitry. J Neurosci 31:9760–9771
Thiel CM, Fink GR (2008) Effects of the cholinergic agonist nicotine on reorienting of visual spatial attention and top-down attentional control. Neuroscience 152:381–390
Thiel CM, Zilles K, Fink GR (2005) Nicotine modulates reorienting of visuospatial attention and neural activity in human parietal cortex. Neuropsychopharmacology 30:810–820
Treisman A, Gormican S (1988) Feature analysis in early vision: evidence from search asymmetries. Psychol Rev 95:15–48
Trimmel M, Wittberger S (2004) Effects of transdermally administered nicotine on aspects of attention, task load, and mood in women and men. Pharmacol Biochem Behav 78:639–645
Tsal Y, Benoni H (2010) Diluting the burden of load: perceptual load effects are simply dilution effects. J Exp Psychol Hum Percept Perform 36:1645–1656
Vangkilde S, Bundesen C, Coull JT (2011) Prompt but inefficient: nicotine differentially modulates discrete components of attention. Psychopharmacology (Berl) 218:667–680
Vossel S, Thiel CM, Fink GR (2008) Behavioral and neural effects of nicotine on visuospatial attentional reorienting in non-smoking subjects. Neuropsychopharmacology 33:731–738
Wesnes K, Warburton DM (1984) Effects of scopolamine and nicotine on human rapid information processing performance. Psychoparmacologia 82:147–150
Witte EA, Davidson MC, Marrocco RT (1997) Effects of altering brain cholinergic activity on covert orienting of attention: comparison of monkey and human performance. Psychopharmacology Berl 132:324–334
Acknowledgments
This work was supported by a grant from the German Research Foundation DFG TH766/6-1. The authors would wish to thank T. Espeseth for the advice on the paradigm.
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The authors have no conflict of interest to declare.
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Behler, O., Breckel, T.P.K. & Thiel, C.M. Nicotine reduces distraction under low perceptual load. Psychopharmacology 232, 1269–1277 (2015). https://doi.org/10.1007/s00213-014-3761-5
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DOI: https://doi.org/10.1007/s00213-014-3761-5