A review of the effects of unilateral hearing loss on spatial hearing

Abstract

The capacity of the auditory system to extract spatial information relies principally on the detection and interpretation of binaural cues, i.e., differences in the time of arrival or level of the sound between the two ears. In this review, we consider the effects of unilateral or asymmetric hearing loss on spatial hearing, with a focus on the adaptive changes in the brain that may help to compensate for an imbalance in input between the ears. Unilateral hearing loss during development weakens the brain's representation of the deprived ear, and this may outlast the restoration of function in that ear and therefore impair performance on tasks such as sound localization and spatial release from masking that rely on binaural processing. However, loss of hearing in one ear also triggers a reweighting of the cues used for sound localization, resulting in increased dependence on the spectral cues provided by the other ear for localization in azimuth, as well as adjustments in binaural sensitivity that help to offset the imbalance in inputs between the two ears. These adaptive strategies enable the developing auditory system to compensate to a large degree for asymmetric hearing loss, thereby maintaining accurate sound localization. They can also be leveraged by training following hearing loss in adulthood. Although further research is needed to determine whether this plasticity can generalize to more realistic listening conditions and to other tasks, such as spatial unmasking, the capacity of the auditory system to undergo these adaptive changes has important implications for rehabilitation strategies in the hearing impaired.

Keywords: Auditory cortex; Binaural; Monaural spectral cue; Plasticity; Sound localization; Spatial release from masking.

Fig. 1

Binaural cues to sound source location. (A) Interaural level differences as a function of sound azimuth and frequency. (B) Interaural time differences as a function of sound azimuth and frequency. Negative values indicate azimuths and corresponding binaural cue values on the left of the midline. Data for both cues are derived from head-related transfer function measurements (0° elevation) published in the CIPIC database by Algazi et al. (2001). (Copyright (c) 2001 The Regents of the University of California. All Rights Reserved).

Fig. 2

Monaural spectral cues to sound source elevation. Pinna gain for the right ear is shown as a function of sound frequency and elevation for sounds presented at 0° azimuth. Data are derived from head-related transfer function measurements published in the CIPIC database by Algazi et al. (2001). (Copyright (c) 2001 The Regents of the University of California. All Rights Reserved).

Fig. 3

Binaural masking level difference (BMLD) in 19 patients before and after surgery to correct congenital unilateral hearing loss resulting from an abnormal external and/or middle ear on one side. The BMLD (N₀S₀ minus N₀S_π) is the difference in detection threshold of a tone presented either in phase or with the phase reversed between the ears in the presence of broadband noise, which was always presented in phase at the two ears. Some subjects had post-operative MLDs in the normal range, whereas others showed a persistent deficit in binaural processing. Modified with permission from Wilmington et al. (1994).

Fig. 4

Unaided sound-localization responses for one subject with a unilateral conductive hearing loss in the left ear. The stimulus was broadband noise (0.5–20 kHz). These data were obtained without using the subject's bone-anchored device (BCD off) (A), and in the BCD off condition with an additional muff over the impaired ear to further alter binaural cues (B). The gains of responses (obtained from the slopes of the regression lines fitted to the data) to stimuli with levels of 55 dB SPL (solid gray regression lines) and 65 dB SPL (solid black regression lines) decreased significantly when the impaired ear was covered with the muff, indicating that the subjects were relying on binaural cues for localization, whereas this was not the case at the lower level of 45 dB SPL (gray dashed regression lines), which was unlikely to be audible at the deprived ear. g = response gain. Reproduced with permission from Agterberg et al. (2012).

Fig. 5

Adaptation to asymmetric hearing loss during infancy can be achieved by reweighting auditory spatial cues. (A) Schematic of setup used for measuring sound localization in the horizontal plane by adult ferrets. Twelve loudspeakers were located at 30° intervals around the perimeter of the apparatus. 0° is straight ahead, with negative numbers indicating locations to the animal's left. A trial was initiated by the animal licking a spout at the center of the chamber. This triggered the presentation of a burst of broadband noise with a flat spectrum from one of the loudspeakers; the animal received a water reward for making a correct approach-to-target response. (B) Average joint distributions of stimulus and response location for ferrets raised wearing an earplug in the left ear (interspersed with brief periods of normal hearing); the size of the circles represents the proportion of trials for each stimulus-response combination. These data were obtained with the earplug in place; note the similarity in the accuracy of the localization responses on the plugged and non-plugged sides. (C) Percentage correct scores for control and juvenile-plugged groups, with individual animals denoted by symbols. Horizontal lines indicate mean values, with error bars showing bootstrapped 95% confidence intervals. Acutely plugging one ear (‘Plug’) in the normally-raised control ferrets caused a substantial drop in localization accuracy. Significantly higher scores were achieved by the juvenile-plugged ferrets, and these animals localized just as accurately as the control group when the earplug was removed (‘No plug’). (D) Effect of disrupting spectral cues by increasing the degree of spectral randomization in the stimuli on localization accuracy by juvenile-plugged animals with and without an earplug in place. (E) Recordings were made bilaterally in the primary auditory cortex (A1) of these animals. (F) Neurons in juvenile-plugged animals were more sensitive to the monaural spatial cues provided to the intact ear and less sensitive to the other available cues; this is indicated by the higher weighting index (mean ± 95% confidence intervals) in juvenile-plugged animals than in the control group (whose mean values are indicated by the horizontal dashed lines). Increased weighting of spectral cues in juvenile-plugged animals was observed only when a virtual earplug was introduced to the previously occluded ear during the recordings. Adapted with permission from Keating et al. (2013).

Fig. 6

Adaptation to asymmetric hearing loss during infancy by remapping the altered binaural cues onto new locations in space. (A–C) Joint distributions of stimulus and response, expressed as degrees (deg) azimuth, for a control ferret with normal hearing (A) and a control (B) and juvenile-plugged (JP) ferret (C) wearing an earplug in the left ear. Grayscale represents the number of trials (n) corresponding to each stimulus-response combination. (D) Mean unsigned error for control and earplugged ferrets, normalized so that 0 and 1 correspond to perfect and chance performance, respectively. Error bars show bootstrapped 95% confidence intervals. Controls wearing an earplug (n = 6 ferrets) made larger errors than normal hearing controls (n = 4; P < 0.001, bootstrap test). While wearing an earplug, juvenile-plugged ferrets (n = 2) made smaller errors than acutely plugged controls (P < 0.001, bootstrap test). (E) Mean binaural interaction (±s. e.m.) as a function of ILD across neurons recorded in A1 of control ferrets under normal hearing conditions. Data are plotted separately for left (n = 142 units, black) and right (n = 177 units, gray) A1. Best ILDs for each hemisphere are indicated by arrows. (F) Binaural interaction functions (mean ± s. e.m.) in juvenile-plugged ferrets under normal hearing conditions, which are shifted, relative to controls, in the appropriate direction to compensate for the hearing loss experienced during development. Adapted with permission from Keating et al. (2015).

Fig. 7

Adult human listeners can relearn to localize sound after introducing an asymmetric hearing loss by occluding one ear. (A) Sound localization performance (% correct) as a function of training session for one subject who wore an earplug in the right ear during the localization tests. Scores for each session (dots) were fitted using linear regression (lines) to calculate slope values, which quantified the rate of adaptation. Relative to flat-spectrum noise (blue), much less adaptation occurred with random-spectrum noise (pink), which limits the usefulness of spectral cues to sound location. (B) Adaptation rate is shown for flat- and random-spectrum stimuli for different subjects (gray lines; n = 11). Positive values indicate improvements in localization performance with training. Mean adaptation rates across subjects (±bootstrapped 95% confidence intervals) are shown in blue and pink for the two stimulus types. Dotted black lines indicate adaptation rates observed in a previous study (Kumpik et al., 2010). (C) Mean error magnitude plotted as a function of training session for one subject when pure tones were used as the stimuli. Data are plotted separately for low- (1 kHz, dark blue) and high-frequency (8 kHz, light blue) tones. Improved performance was associated with a reduction in error magnitude, producing negative values for the change (Δ) in error magnitude. (D) Δ error for low- and high-frequency tones plotted for each subject (gray lines; n = 11). Mean values for Δ error across subjects (±bootstrapped 95% confidence intervals) are shown in blue. Although there are pronounced individual differences for the adaptation observed at the two tone frequencies, almost all values are <0, indicating that error magnitude declined over the training sessions. Dotted red line shows Δ error values that would have been observed if human listeners had adapted as well as ferrets reared with a unilateral earplug (Keating et al., 2015). Adapted from Keating et al. (2016).