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

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 singleblind, 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.

Task-dependent effects of nicotine treatment on auditory performance in young-adult and elderly human nonsmokers

“…Moreover, the nicotine effect may depend on the task. Pham et al 12 found that nicotine improved performance for auditory selective attention and tone-innoise detection but not for easier temporal or spectral resolution tasks. Similar to the previous studies, the present study found a signi cant nicotine effect on intensity discrimination but not on frequency-related tasks (see Limitations and Future Directions later).…”

“…All procedures leading up to experiments, including method of drug delivery and time between sessions to allow for drug clearance followed those speci ed by Pham et al 12 . Brie y, six mg of nicotine was delivered in the form of two pieces of mint-avored polacrilex gum (4 mg and 2 mg; Nicorette®, Johnson & Johnson, Inc).…”

“…Human electrophysiological studies did not nd consistent evidence for the stimuluslter model in auditory processing 10,11 . Human behavioral studies in younger adults found that nicotinic effects depend upon task di culty, with a greater bene t in more di cult conditions, such as tone-innoise detection and auditory selective attention tasks 11,12 .…”

α3β4* Nicotinic acetylcholine receptors strongly modulate the excitability of VIP neurons in the mouse inferior colliculus

“…Because activity in the PMT is influenced by the sleep-wake cycle, attention, rewards, and sensory novelty, it is hypothesized that PMT neurons regulate auditory processing in the IC as a function of behavioral state (Jones, 1991;Kozak et al, 2005;Schofield et al, 2011;Boucetta et al, 2014). Consistent with this, in vivo studies have shown that nicotinic drugs alter the gain of input-output functions in IC neurons (Farley et al, 1983;Habbicht & Vater, 1996), and human psychophysics studies indicate that nicotine improves performance in auditory attention and discrimination tasks (Knott et al, 2012;Smucny et al, 2016;Pham et al, 2020), an effect partly attributable to alterations in the IC (Askew et al, 2017). In addition, temporal coding of auditory stimuli is degraded in the IC of α7 knockout mice (Felix et al, 2019).…”

“…Previous studies have identified clear roles for muscarinic signaling in the IC, including roles in cortically driven plasticity (Ji et al, 2001;Ji & Suga, 2009) and stimulus specific adaptation (Ayala & Malmierca, 2015), but the roles of nicotinic signaling in the IC are less clear. Psychophysical studies indicate that systemic nicotine exposure in non-smokers can enhance performance in auditory tasks (Harkrider & Hedrick, 2005;Knott et al, 2009;Pham et al, 2020). Intriguingly, recent work from Askew and colleagues suggests that systemic nicotine sharpens frequency tuning in the IC, which likely contributes to sharper tuning in auditory cortex and improved discrimination in behavioral tasks (Askew et al, 2017).…”