A sensitive period for the impact of hearing loss on auditory perception

Abstract

Manipulations of the sensory environment typically induce greater changes to the developing nervous system than they do in adulthood. The relevance of these neural changes can be evaluated by examining the age-dependent effects of sensory experience on quantitative measures of perception. Here, we measured frequency modulation (FM) detection thresholds in adult gerbils and investigated whether diminished auditory experience during development or in adulthood influenced perceptual performance. Bilateral conductive hearing loss (CHL) of ≈30 dB was induced either at postnatal day 10 or after sexual maturation. All animals were then trained as adults to detect a 5 Hz FM embedded in a continuous 4 kHz tone. FM detection thresholds were defined as the minimum deviation from the carrier frequency that the animal could reliably detect. Normal-hearing animals displayed FM thresholds of 25 Hz. Inducing CHL, either in juvenile or adult animals, led to a deficit in FM detection. However, this deficit was greater for juvenile onset hearing loss (89 Hz) relative to adult onset hearing loss (64 Hz). The effects could not be attributed to sensation level, nor were they correlated with proxies for attention. The thresholds displayed by CHL animals were correlated with shallower psychometric function slopes, suggesting that hearing loss was associated with greater variance of the decision variable, consistent with increased internal noise. The results show that decreased auditory experience has a greater impact on perceptual skills when initiated at an early age and raises the possibility that altered development of CNS synapses may play a causative role.

Keywords: critical period; deafness; frequency discrimination; temporal processing.

Figure 1.

Overview of FM detection task. The target (a sinusoidally frequency modulated tone) is embedded in a continuous 4 kHz carrier at a rate of 5 Hz. Task difficulty was modulated by adjusting the maximum frequency deviation from 4 kHz (arrow, modulation depth). Examples of the fine structure for a pure and FM tone waveform are shown above the center frequency plot. Trials, each lasting 1 s, were presented at a rate of ∼1/s while the animal was drinking from the water spout. Three to five no go trials were delivered between each go trial. Trials were suspended when animals broke contact with the spout for >50 ms. To determine whether the animal detected the target, spout contact was monitored during the last 100 ms of each trial (cross-hatched region) and scored as a “yes” response if they were off the spout for at least 50 ms. A 300 ms aversive stimulus followed each go trial (black). Middle and bottom images are shown on the same timescale; the temporal relationship of the fine structure examples in the top image are indicated by the gray background.

Figure 2.

FM depth detection thresholds were worse in animals with CHL. A, Example psychometric functions from a single test session for a control (black) and P10 CHL (red) animal. FM depth threshold was estimated by fitting a psychometric function (solid line) to the percent-correct data (individual points). The fitted psychometric function was transformed into sensitivity (d′) using the fitted FA rate. Threshold was defined as the FM depth where d′ = 1. The slope is indicated next to both curves. B, FM depth threshold for each session for a representative control (black) and adult CHL animal (orange). The first session was devoted to test cage habituation (dark gray), followed by several sessions of procedural learning (i.e., training at a single FM depth of 500 Hz, light gray). Filled markers indicate the three best sessions. C, Average of the three best FM depth thresholds for each animal. Bars indicate ± SEM. The aged adult CHL group is plotted separately (diamond marker). In all other panels and figures, the aged adult CHL group was combined with the adult CHL group. D, Average FM depth threshold for each group. Bars indicate ± SEM.

Figure 3.

Psychometric function slopes were shallower and performance was more variable for animals with CHL. Each animal's FM psychometric function slope, d′/log₁₀(Hz), is plotted against the FM detection threshold. The psychometric function slopes were steepest for control animals. Furthermore, there was a significant correlation between threshold and slope for all animals. Values were obtained from the psychometric functions with the three best FM depth threshold values, as described in Figure 2B. Error bars indicate ± SEM.

Figure 4.

The FM depth detection thresholds were not correlated with sensation level (A) and there was no between-group difference for FA rate (B), lapse rate on the easiest FM depth (C), or sensitivity at the easiest stimulus depth (D). Data presented in all plots are averaged from the animal's three best sessions, as described in Figure 2B. Error bars indicate SEM.

Figure 5.

Reaction time was nearly identical across control and CHL groups. A, Average probability of spout contact relative to onset of frequency modulation is shown for hit trials near the animals' threshold. For reference, spout contact on miss trials are plotted as well. Although we required the animal to be on the spout before presenting a trial, there is a non-negligible chance of the animal leaving the spout just before the trial begins. Even though the animal may have been off the spout by the end of some miss trials, it was not scored as a hit because it did not meet the criterion of being off the spout for at least 50 ms. B, Reaction time for individual trials was computed as the time at which the animal first left the spout regardless of whether they chose to return to the spout. Reaction time at threshold was not correlated with the animal's FM depth threshold and there were no between-group differences. Error bars indicate ± SEM.