Children With Bilateral Cochlear Implants Show Emerging Spatial Hearing of Stationary and Moving Sound

Abstract

Spatial hearing in children with bilateral cochlear implants (BCIs) was assessed by: (a) comparing localization of stationary and moving sound, (b) investigating the relationship between sound localization and sensitivity to interaural level and timing differences (ILDs/ITDs), (c) evaluating effects of aural preference on sound localization, and (d) exploring head and eye (gaze) movements during sound localization. Children with BCIs (n = 42, M_Age = 12.3 years) with limited duration of auditory deprivation and peers with typical hearing (controls; n = 37, M_Age = 12.9 years) localized stationary and moving sound with unrestricted head and eye movements. Sensitivity to binaural cues was measured by a lateralization task to ILDs and ITDs. Spatial separation effects were measured by spondee-word recognition thresholds (SNR thresholds) when noise was presented in front (colocated/0°) or with 90° of left/right separation. BCI users had good speech reception thresholds (SRTs) in quiet but higher SRTs in noise than controls. Spatial separation of noise from speech revealed a greater advantage for the right ear across groups. BCI users showed increased errors localizing stationary sound and detecting moving sound direction compared to controls. Decreased ITD sensitivity occurred with poorer localization of stationary sound in BCI users. Gaze movements in BCI users were more random than controls for stationary and moving sounds. BCIs support symmetric hearing in children with limited duration of auditory deprivation and promote spatial hearing which is albeit impaired. Spatial hearing was thus considered to be "emerging." Remaining challenges may reflect disruptions in ITD sensitivity and ineffective gaze movements.

Keywords: binaural hearing; children and adolescents; hearing loss and cochlear implants; sound localization; unrestricted head and eye movements.

Figure 1.

Preimplant unaided PTA (dB HL) is negatively associated with age at implantation with higher hearing thresholds being associated with earlier implantation (p < .001) for children with bilateral cochlear implants provided simultaneously and sequentially.

Figure 2.

Postimplant speech perception scores were collected from age-appropriate word tests in children with BCIs implanted sequentially or simultaneously. Postimplant speech perception scores (RAU) collected in unilateral presentations in quiet were comparable between left and right ear presentations with no significant difference between the two sides (p = .05).

Figure 3.

Spondee-word recognition thresholds (SRTs; dB) of target words presented at 0° azimuth amid speech-weighted noise presented at 45 dB HL in children with typical hearing (control, n = 26) and children with bilateral cochlear implants (BCIs, n = 31). (A) SRTs (dB) were higher in the BCI group (p < .001) and highest when speech and noise were colocated rather than spatially separated (p < .001). (B) Spatial release from masking (SRM; colocated − separated conditions) was larger for left than right positions of noise (p < .001) with no significant differences between groups (p = .52), indicating a right ear bias across groups. (C) Ear bias (asymmetry) in SRM is plotted for each group with a dashed line demarcating side of ear advantage. Most children had a right ear bias (n = 24 [77.4%] BCI and n = 23 [88%] control) and this asymmetry was not significantly different between groups (p > .05).

Figure 4.

Reported hearing challenges in 27 children with bilateral cochlear implants (BCI) (M_SSQ [SD] = 7.0 [1.6]) measured by the Speech, Spatial and Qualities of Hearing Scale (SSQ) and 11 age-matched peers with typical hearing (controls; M_SSQ [SD] = 9.5 [0.4]). BCI users had significantly lower self-reported hearing scores compared to controls across subtests (p < .001).

Figure 5.

Responses to presentation of stationary white noise. (A) Response position plotted against stationary stimulus location (regression lines for each child) reveals greater variability in the BCI than control group. Coefficient of determination (R²) values of responses from each child were significantly lower in the BCI than control group (p < .001). (B) Root-mean-square error (RMSE; °) by side (hemifield) of stationary sound presentation (bars are mean [±1 SE] and circles are individual data] show higher RMSE values in BCI than controls (p < .001). There was no significant effect of hemifield (p = .10). (C) Response times increased with RMSE at a faster rate in BCI users than controls (p < .001).

Figure 6.

Responses to presentation of moving white noise. (A) Perception of direction of sound movement modeled by logistic regression curves for each child shows reduced sensitivity in the BCI group compared to the control group. (B) Logistic regression slope values were significantly reduced in BCI than controls (p < .001). (C) RMSE of the response change (°) relative to the stimulus change condition (L1 − L2) shows increased RMSE in BCI than controls (p < .001) and largest RMSE for larger sound movement conditions (p < .001). (D) Response times (s) to moving sound increase with RMSE at a faster rate in BCI than controls (p < .05) and for conditions with more sound movement (p < .001).

Figure 7.

Comparison of auditory localization of 1-kHz pure tone with 40-Hz amplitude modulation (AM) compared to bandpass-filtered white noise (WN) during stationary (A) and moving presentation (B) in 26 children with BCIs and 10 with typical hearing. There was no significant effect of auditory stimulus for stationary auditory localization accuracy (p = .2), However, there was an improvement of perception of direction of sound movement for listening to the AM stimulus compared to the WN stimulus (p < .01).

Figure 8.

Responses to lateralization of binaural cues with interaural level differences (ILDs) and interaural timing differences (ITDs). (A) Individual logistic regression curves of “right” responses to ILD conditions reveal similar sensitivity to ILDs between BCI (n = 21) and controls (n = 10). (C) Extracted regression slopes for the ILD lateralization task (bars = mean [1 ± SE], symbols = individual data) are not significantly different between groups (p = .98). (B) Individual logistic regression curves of “right” responses to ITD conditions show reduced sensitivity to ITDs between BCI and controls. Extracted regression slopes for the ITD lateralization task in D (bars = mean [±1 SE], symbols = individual data) are significantly different between groups (p < .05).

Figure 9.

Top row: Slopes of ILD lateralization did not significantly affect localization of a 1-kHz pure tone with 40-Hz amplitude modulation (AM) stimuli in either stationary (A) or moving (B) conditions nor was associated with aural preference measured by asymmetric SRM benefits (dB) (C). Bottom row: ITD lateralization slopes were significantly associated with reduced stationary localization error (D) and improved direction perception acuity (E). Poorer ITD sensitivity was significantly associated with increased preference for one ear measured by SRM asymmetries (F).

Figure 10.

(A) Gaze displacement (summated head and eye movements) is shown from onset of stationary sound presentation to 5 s (stationary sound offset occurs at 3 s) in bins of 10°. Horizontal blue bands indicate sound source location (L1). (B) Gaze displacement to stationary sounds measured as area under the waveform curve (AUC) reveal less movement in children with BCIs than controls (p < .001). (C) The proportion of gaze that was in the stationary stimulus hemifield was greater than 50% chance (shown by blue line) for positions outside of the shaded ranges. (D) Gaze displacement from onset of moving sound presentation to 10 s from onset. Blue lines indicate terminal sound location (L2). (E) Gaze displacement during moving sound presentation measured as AUC reveal less movement in children with BCIs than controls during large movements of 40° (p < .001). (F) Proportion of time gaze was in the same direction as sound movement and was significantly better than chance (50% shown by blue line) for all movement conditions >0° in both groups. The gaze proportions were significantly lower in the BCI group compared to controls (p < .01).