Neonatal nicotine exposure impairs development of auditory temporal processing

Abstract

Accurate temporal processing of sound is essential for detecting word structures in speech. Maternal smoking affects speech processing in newborns and may influence child language development; however, it is unclear how neonatal exposure to nicotine, present in cigarettes, affects the normal development of temporal processing. The present study used the gap-induced prepulse inhibition (gap-PPI) of the acoustic startle response to investigate the effects of neonatal nicotine exposure on the normal development of gap detection, a behavioral testing procedure of auditory temporal resolution. Neonatal rats were injected twice per day with saline (control), 1 mg/kg nicotine (N-1mg) or 5 mg/kg nicotine (N-5mg) from postnatal day 8 to 12 (P8-P12). During the first month after birth, rats showed poor gap-PPI in all three groups. At P45 and P60, gap-PPI in control rats improved significantly, whereas rats exposed to nicotine exhibited less improvement. At P60, the gap-detection threshold in the N-5mg group was significantly higher than in the control group, suggesting that neonatal nicotine exposure affects the normal development of gap detection acuity. Additionally, 1 hour after receiving an acute nicotine injection (1 mg/kg), gap-PPI recorded in adult rats from the N-5mg group showed a temporary significant improvement. These results suggest that neonatal nicotine exposure reduces gap-PPI implying an impairment of the normal development of auditory temporal processing by inducing changes in cholinergic systems.

Environmental noise affects auditory temporal processing development and NMDA-2B receptor expression in auditory cortex

“…Behavioral studies on both humans and rats have shown that temporal processing acuity improves during normal development, such that both adult humans [22] and rats [21, 23] demonstrate a gap detection threshold of ~5 ms. The results from our adult control rats are consistent with this age-related decrease in gap detection threshold (P-2m: 6 ±2 ms; P-3m: 3.4 ± 1.9 ms).…”

“…Gap detection is a well-accepted and reliable behavioral measure to assess temporal processing acuity [21]. As described in our recent paper [23], the Gap-PPI paradigm exploits an animal’s abrupt motoric response to a sudden, startle-eliciting sound. More specifically, if the rat is able to detect a brief silent gap in an otherwise continuous background noise that precedes the startle-eliciting sound, the magnitude of the startle response is inhibited (i.e., gap prepulse inhibition).…”

“…We used a behavioral paradigm, the gap-induced prepulse inhibition of the acoustic startle reflex (Gap-PPI), to assess the gap detection threshold [23], and provide a comparison of temporal processing acuity between environmental noise-reared rats and controls. In addition, using standard laboratory techniques described in our recent study [24], we compared the level of NR2A and NR2B subunit protein expression in the AC between groups.…”

Fetal and Maternal Physiology and Ultrasound Diagnosis

“…It was noted that the development of the auditory system can be disrupted by the influence of adverse factors (cigarette consumption) and also in some pathological conditions (intrauterine growth retardation, maternal hypertension). [190][191][192] It is important to mention also that development of the auditory system affects the subsequent learning of speech and language acquisition. Animal experiments have indicated that the intrauterine environment is not completely deprived of light.…”

Effects of intravenous nicotine on prepulse inhibition in smokers and non-smokers: relationship with familial smoking

“…Finally, genes regulating the dopaminergic system also appear to be involved in both PPI and smoking. For instance, a polymorphism of the catechol-o-methyl-transferase (COMT) gene (Val 108/158 Met) predicts PPI (Quednow et al 2010) and has been associated with smoking phenotypes (Munafo et al 2008; Suriyaprom et al 2012) as well as smoking cessation outcomes (Johnstone et al 2007; Munafo et al 2008; Sun et al 2008). …”