Developmental hearing loss impairs signal detection in noise: putative central mechanisms

Abstract

Listeners with hearing loss have difficulty processing sounds in noisy environments. This is most noticeable for speech perception, but is reflected in a basic auditory processing task: detecting a tonal signal in a noise background, i.e., simultaneous masking. It is unresolved whether the mechanisms underlying simultaneous masking arise from the auditory periphery or from the central auditory system. Poor detection in listeners with sensorineural hearing loss (SNHL) is attributed to cochlear hair cell damage. However, hearing loss alters neural processing in the central auditory system. Additionally, both psychophysical and neurophysiological data from normally hearing and impaired listeners suggest that there are additional contributions to simultaneous masking that arise centrally. With SNHL, it is difficult to separate peripheral from central contributions to signal detection deficits. We have thus excluded peripheral contributions by using an animal model of early conductive hearing loss (CHL) that provides auditory deprivation but does not induce cochlear damage. When tested as adults, animals raised with CHL had increased thresholds for detecting tones in simultaneous noise. Furthermore, intracellular in vivo recordings in control animals revealed a cortical correlate of simultaneous masking: local cortical processing reduced tone-evoked responses in the presence of noise. This raises the possibility that altered cortical responses which occur with early CHL can influence even simple signal detection in noise.

Keywords: auditory cortex; conductive hearing loss; electrophysiology; gerbil; intracellular; masking; noise; signal detection.

Figure 1

Operant conditioning schematic. (A) Top: Trial structure for the simultaneous masking task, where 300 ms noise maskers were presented either with (WARN trial) or without (SAFE trial) overlapping tonal signals. Warn trials were followed by an aversive shock. Bottom: The timeline of a single warn trial is illustrated, with the masker (gray) and signal (blue) just above. For the trial to be initiated, the animal needed to maintain contact with the spout for >75% of the pre-spout check period. WARN trials contained a 300 ms masker and a 40 ms signal. A mild shock was delivered 300 ms after the offset of the signal. During the 50 ms prior to the shock, a spout check determined whether the animal was correctly off the spout (Hit) or incorrectly on the spout (Miss). For SAFE trials (not illustrated), neither the signal nor shock were presented, but the spout check determined whether the animal was correctly on the spout (Correct Rejection) or incorrectly off the spout (False Alarm). (B) During training, the duration of the signal was progressively decreased as animals reached criterion performance at each duration. The shock always occurred 300 ms after signal offset, regardless of signal duration.

Figure 2

Early CHL increases behavioral detection thresholds for simultaneously masked signals. Detection thresholds (quantified as SNR; see Section Methods) were significantly higher for conductive hearing loss (CHL; shaded orange) compared with control (CTR; cream-filled black) animals, as measured by (A) the best performance day and (B) the mean across the best 3 performance days. Thresholds from individual animals are depicted as circles or diamonds atop each bar. (C) Groups required similar numbers of training trials to reach criterion performance. (D) The amount of training did not predict final detection thresholds. Lines show non-significant linear fits. (E) Detection thresholds across testing days indicate gradual improvement which did not differ across groups. Thin lines are thresholds from individual animals, and thick lines are means. Abbreviations: CTR: controls, CHL: conductive hearing loss, n.s.: not significant, **: p < 0.01, ***: p = 0.001.

Figure 3

Performance strategies do not account for differences in behavioral detection thresholds. (A) False alarm (FA) rates, a measure of attention, did not differ across CTR (open black) and CHL (shaded orange) animals. FA rates from individual animals are depicted as circles or diamonds atop each bar. (B) FA rates did not correlate with behavioral detection thresholds for either group (lines show non-significant linear fits). (C) CTR animals adopted a less consistent licking strategy than CHL animals (quantified as the number of breaks with the water spout between WARNs: N times off spout). (D) Despite a difference in licking stragegy, the number of breaks did not correlate with final detection thresholds for either group (lines show non-significant linear fits). Abbreviations as in Figure 2.

Figure 4

Neither task proficiency nor hearing ability account for differences in detection thresholds. Detection thresholds were not correlated with either (A) d′ performance for the easiest signal levels or (B) the variability of d′ performance for the easiest signal level across testing days, for either CTR (shaded orange) or CHL (open black) groups. Thresholds from individual animals are depicted as circles or diamonds, and lines are non-significant linear fits. (C) Neural ABR thresholds measured across frequency were predictably increased in CHL animals by ~40 dB. There was no correlation in either CTRs or CHLs between neural hearing thresholds and signal detection thresholds. Abbreviations as in Figure 2.

Figure 5

Auditory cortex alters firing responses to simultaneous masked signals. (A) An example of overlaid traces (gray traces with mean in red) from a cortical neuron in response to 10 presentations of a FM tone (top; blue bar) or a FM tone occurring during a broadband noise (bottom; blue bar within gray bar). The traces show changes in voltage over time. Top: This neuron has an onset spiking response to the FM tone followed by a hyperpolarization, with rebound spikes (arrow) upon return to baseline (black dotted line). Bottom: When a simultaneous masker is presented, there is a reduced hyperpolarization and no clear rebound spikes (arrow) in response to the masked FM signal. (B) During masker presentation compared with tone alone, there was a significant reduction in the magnitude of signal-evoked hyperpolarizations. (C) When a simultaneous masker was present (gray bar), there were significantly fewer spikes immediately following hyperpolarizations, as compared with the tone presented alone (blue bar). Since hyperpolarizations arise within cortex and indicate central processing, a reduction in their magnitude, and a reduction of the number of post-inhibitory rebound spikes, are attributable to central mechanisms. **: p < 0.01, *: p < 0.05.