Skip to main content
Log in

Nicotine enhances auditory processing in healthy and normal-hearing young adult nonsmokers

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

Abstract

Rationale

Electrophysiological studies show that systemic nicotine narrows frequency receptive fields and increases gain in neural responses to characteristic frequency stimuli. We postulated that nicotine enhances related auditory processing in humans.

Objectives

The main hypothesis was that nicotine improves auditory performance. A secondary hypothesis was that the degree of nicotine-induced improvement depends on the individual’s baseline performance.

Methods

Young (18–27 years old), normal-hearing nonsmokers received nicotine (Nicorette gum, 6mg) or placebo gum in a single-blind, randomized, crossover design. Subjects performed four experiments involving tone-in-noise detection, temporal gap detection, spectral ripple discrimination, and selective auditory attention before and after treatment. The perceptual differences between posttreatment nicotine and placebo conditions were measured and analyzed as a function of the pre-treatment baseline performance.

Results

Nicotine significantly improved performance in the more difficult tasks of tone-in-noise detection and selective attention (effect size = − 0.3) but had no effect on relatively easier tasks of temporal gap detection and spectral ripple discrimination. The two tasks showing significant nicotine effects further showed no baseline-dependent improvement.

Conclusions

Nicotine improves auditory performance in difficult listening situations. The present results support future investigation of nicotine effects in clinical populations with auditory processing deficits or reduced cholinergic activation.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aronoff JM, Landsberger DM (2013) The development of a modified spectral ripple test. J Acoust Soc Am 134:EL217–EL222

    Article  Google Scholar 

  • Askew C, Intskirveli I, Metherate R (2017) Systemic nicotine increases gain and narrows receptive fields in A1 via integrated cortical and subcortical actions. eNeuro 4(3). https://doi.org/10.1523/ENEURO.0192-17.2017

    Article  Google Scholar 

  • Baschnagel JS, Hawk LW Jr (2008) The effects of nicotine on the attentional modification of the acoustic startle response in nonsmokers. Psychopharmacology 198:93–101

    Article  CAS  Google Scholar 

  • Behler O, Breckel TP, Thiel CM (2015) Nicotine reduces distraction under low perceptual load. Psychopharmacology 232:1269–1277

    Article  CAS  Google Scholar 

  • Benowitz NL, Lessov-Schlaggar CN, Swan GE, Jacob P 3rd (2006) Female sex and oral contraceptive use accelerate nicotine metabolism. Clin Pharmacol Ther 79:480–488

    Article  CAS  Google Scholar 

  • Bramer SL, Kallungal BA (2003) Clinical considerations in study designs that use cotinine as a biomarker. Biomarkers 8:187–203

    Article  CAS  Google Scholar 

  • Disney AA, Aoki C, Hawken MJ (2007) Gain modulation by nicotine in macaque v1. Neuron 56:701–713

    Article  CAS  Google Scholar 

  • Dwyer JB, McQuown SC, Leslie FM (2009) The dynamic effects of nicotine on the developing brain. Pharmacol Ther 122:125–139

    Article  CAS  Google Scholar 

  • Fletcher H (1938) The mechanism of hearing as revealed through experiment of the masking effect of thermal noise. Proc Natl Acad Sci U S A 24:265–274

    Article  CAS  Google Scholar 

  • Harkrider AW, Champlin CA (2001a) Acute effect of nicotine on non-smokers: II. MLRs and 40-Hz responses. Hear Res 160:89–98

    Article  CAS  Google Scholar 

  • Harkrider AW, Champlin CA (2001b) Acute effect of nicotine on non-smokers: III. LLRs and EEGs. Hear Res 160:99–110

    Article  CAS  Google Scholar 

  • Harkrider AW, Champlin CA, McFadden D (2001) Acute effect of nicotine on non-smokers: I. OAEs and ABRs. Hear Res 160:73–88

    Article  CAS  Google Scholar 

  • Harkrider AW, Hedrick MS (2005) Acute effect of nicotine on auditory gating in smokers and non-smokers. Hear Res 202:114–128

    Article  CAS  Google Scholar 

  • 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 86:1119–1127

    Article  CAS  Google Scholar 

  • Heishman SJ, Kleykamp BA, Singleton EG (2010) Meta-analysis of the acute effects of nicotine and smoking on human performance. Psychopharmacology 210:453–469

    Article  CAS  Google Scholar 

  • Hong LE, Schroeder M, Ross TJ, Buchholz B, Salmeron BJ, Wonodi I, Thaker GK, Stein EA (2011) Nicotine enhances but does not normalize visual sustained attention and the associated brain network in schizophrenia. Schizophr Bull 37:416–425

    Article  Google Scholar 

  • Hukkanen J, Jacob P 3rd, Benowitz NL (2005) Metabolism and disposition kinetics of nicotine. Pharmacol Rev 57:79–115

    Article  CAS  Google Scholar 

  • Intskirveli I, Metherate R (2012) Nicotinic neuromodulation in auditory cortex requires MAPK activation in thalamocortical and intracortical circuits. J Neurophysiol 107:2782–2793

    Article  CAS  Google Scholar 

  • Kassel JD (1997) Smoking and attention: a review and reformulation of the stimulus-filter hypothesis. Clin Psychol Rev 17:451–478

    Article  CAS  Google Scholar 

  • Kawai HD, Kang HA, Metherate R (2011) Heightened nicotinic regulation of auditory cortex during adolescence. J Neurosci 31:14367–14377

    Article  CAS  Google Scholar 

  • Knott V, Choueiry J, Dort H, Smith D, Impey D, de la Salle S, Philippe T (2014a) Baseline-dependent modulating effects of nicotine on voluntary and involuntary attention measured with brain event-related P3 potentials. Pharmacol Biochem Behav 122:107–117

    Article  CAS  Google Scholar 

  • Knott V, de la Salle S, Choueiry J, Impey D, Smith D, Smith M, Beaudry E, Saghir S, Ilivitsky V, Labelle A (2015) Neurocognitive effects of acute choline supplementation in low, medium and high performer healthy volunteers. Pharmacol Biochem Behav 131:119–129

    Article  CAS  Google Scholar 

  • Knott V, Smith D, de la Salle S, Impey D, Choueiry J, Beaudry E, Smith M, Saghir S, Ilivitsky V, Labelle A (2014b) CDP-choline: effects of the procholine supplement on sensory gating and executive function in healthy volunteers stratified for low, medium and high P50 suppression. J Psychopharmacol 28:1095–1108

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Levin ED, McClernon FJ, Rezvani AH (2006) Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology 184:523–539

    Article  CAS  Google Scholar 

  • Metherate R, Intskirveli I, Kawai HD (2012) Nicotinic filtering of sensory processing in auditory cortex. Front Behav Neurosci 6:44

    Article  CAS  Google Scholar 

  • Myers CS, Taylor RC, Moolchan ET, Heishman SJ (2008) Dose-related enhancement of mood and cognition in smokers administered nicotine nasal spray. Neuropsychopharmacology 33:588–598

    Article  CAS  Google Scholar 

  • Newhouse P, Kellar K, Aisen P, White H, Wesnes K, Coderre E, Pfaff A, Wilkins H, Howard D, Levin ED (2012) Nicotine treatment of mild cognitive impairment: a 6-month double-blind pilot clinical trial. Neurology 78:91–101

    Article  CAS  Google Scholar 

  • Newhouse PA, Potter A, Singh A (2004) Effects of nicotinic stimulation on cognitive performance. Curr Opin Pharmacol 4:36–46

    Article  CAS  Google Scholar 

  • Parrott AC, Garnham NJ, Wesnes K, Pincock C (1996) Cigarette smoking and abstinence: comparative effects upon cognitive task performance and mood state over 24 hours. Hum Psychopharm Clin 11:391–400

    Article  Google Scholar 

  • Phillips DP, Taylor TL, Hall SE, Carr MM, Mossop JE (1997) Detection of silent intervals between noises activating different perceptual channels: some properties of “central” auditory gap detection. J Acoust Soc Am 101:3694–3705

    Article  CAS  Google Scholar 

  • Sarter M, Parikh V, Howe WM (2009) nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms. Biochem Pharmacol 78:658–667

    Article  CAS  Google Scholar 

  • Smucny J, Olincy A, Eichman LS, Tregellas JR (2015) Neuronal effects of nicotine during auditory selective attention. Psychopharmacology 232:2017–2028

    Article  CAS  Google Scholar 

  • Smucny J, Olincy A, Rojas DC, Tregellas JR (2016) Neuronal effects of nicotine during auditory selective attention in schizophrenia. Hum Brain Mapp 37:410–421

    Article  Google Scholar 

  • Thiel CM, Fink GR (2007) Visual and auditory alertness: modality-specific and supramodal neural mechanisms and their modulation by nicotine. J Neurophysiol 97:2758–2768

    Article  Google Scholar 

  • Zhang YX, Barry JG, Moore DR, Amitay S (2012) A new test of attention in listening (TAIL) predicts auditory performance. PLoS One 7:e53502

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Barbara Bodenhoefer, Sahara George, and Zekiye Onsan for subject recruitment assistance, Dr. Thomas Lu for technical assistance, Dr. Jonathan Venezia for statistical assistance, and the reviewers for helpful suggestions.

Funding

This research was supported by grants from the National Institutes of Health to FGZ (5R01DC015587), to RM (4R01-DC013200) and a pre-doctoral fellowship to CQP (UL1-TR000153).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fan-Gang Zeng.

Ethics declarations

Conflict of interest

F.G.Z. owns stock in Axonics, Nurotron, Syntiant, and Velox Biosystems. The other authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pham, C.Q., Kapolowicz, M.R., Metherate, R. et al. Nicotine enhances auditory processing in healthy and normal-hearing young adult nonsmokers. Psychopharmacology 237, 833–840 (2020). https://doi.org/10.1007/s00213-019-05421-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-019-05421-x

Keywords

Navigation