Simultaneous bilateral cochlear implants: Developmental advances do not yet achieve normal cortical processing

Abstract

Background: Simultaneous bilateral cochlear implantation promotes symmetric development of bilateral auditory pathways but binaural hearing remains abnormal. To evaluate whether bilateral cortical processing remains impaired in such children, cortical activity to unilateral and bilateral stimuli was assessed in a unique cohort of 16 children who received bilateral cochlear implants (CIs) simultaneously at 1.97 ± 0.86 years of age and had ~4 years of CI experience, providing the first opportunity to assess electrically driven cortical development in the absence of reorganized asymmetries from sequential implantation.

Methods: Cortical activity to unilateral and bilateral stimuli was measured using multichannel electro-encephalography. Cortical processing in children with bilateral CIs was compared with click-elicited activity in 13 normal hearing children matched for time-in-sound. Source activity was localized using the Time Restricted, Artefact and Coherence source Suppression (TRACS) beamformer method.

Results: Consistent with dominant crossed auditory pathways, normal P1 activity (~100 ms) was weaker to ipsilateral stimuli relative to contralateral and bilateral stimuli and both auditory cortices preferentially responded to the contralateral ear. Right hemisphere dominance was evident overall. Children with bilateral CIs maintained the expected right dominance but differences from normal included: (i) minimal changes between ipsilateral, contralateral and bilateral stimuli, (ii) weaker than normal contralateral stimulus preference, (iii) symmetric activity to bilateral stimuli, and (iv) increased occipital lobe recruitment during bilateral relative to unilateral stimulation. Between-group contrasts demonstrated lower than normal activity in the inferior parieto-occipital lobe (suggesting deficits in sensory integration) and greater than normal left frontal lobe activity (suggesting increased attention), even during passive listening.

Conclusions: Together, findings suggest that early simultaneous bilateral cochlear implantation promotes normal-like auditory symmetry but that abnormalities in cortical processing consequent to deafness and/or electrical stimulation through two independent speech processors persist.

Keywords: auditory brain; beamformer; bilateral cochlear implant; children; cortical aural preference; cortical lateralization; development; electro‐encephalogram; hearing loss; speech perception.

Figure 1

illustrates similar distribution of children's time‐in‐sound (in years) between groups at the time of data collection

Figure 2

Grand average Cz waveforms and global field power (GFP) in normal hearing children (a, b) and children with bilateral CIs (c, d) to unilateral and bilateral conditions demonstrate immature responses in both groups. (e, f) display average topographic maps at response peaks for P1/Pci and N2 in children with normal hearing and bilateral CIs, respectively. The change between conditions at P1 in children with normal hearing (e) was more distinct than in children with CI (Pci; f). Distribution of EEG activity at N2 was similar in both groups

Figure 3

Mean pseudo‐Z maps (only axial images shown) in children with normal hearing (a) demonstrate contralateral cortical activity to unilateral stimulation and bilateral cortical activity to bilateral stimulation during the response peak P1. Mean pseudo‐Z maps in children with bilateral CIs (b) illustrate more bilateral activity during unilateral stimulation. Peak dipole moment (mean in black and individual in gray) to ipsilateral stimulation was lower in left and right hemispheres in children with normal hearing (c), but not in children with bilateral CIs (d). * indicates a significant difference. Peak latencies for ipsilateral stimulation were longer relative to contralateral and bilateral stimulation in both groups (e, f). Error bars represent standard error (SE). Abbreviations L Unil and R Unil represent left‐unilateral and right‐unilateral conditions, respectively

Figure 4

Mean pseudo‐Z maps (axial images) in children with normal hearing (a) and bilateral CIs (b) display similar predominant contralateral activated cortical regions during unilateral stimulation. Peak dipole moment (c, d, mean in black and individual in gray) and peak latency (e, f) illustrate a similar pattern of lower dipole moment and longer latencies for ipsilateral relative to contralateral and bilateral stimulation in both groups. Error bars represent SE. Abbreviations L Unil and R Unil represent left‐unilateral and right‐unilateral conditions, respectively

Figure 5

(a, b) display mean (black) and individual (gray) cortical lateralization indices (%) for response peaks P1/Pci and N2, respectively. A significant (indicated by *) progressive increase in cortical lateralization toward the right hemisphere going from right to left unilateral stimulation is evident only in children with normal hearing during P1. Cortical lateralization patterns in N2 resemble that of P1 and are similar between the two groups. Error bars represent SE

Figure 6

(a) Individual (gray) and group mean (black) aural preference in children with normal hearing and bilateral CIs indicate contralateral aural preference in both groups however significantly lower scores in bilateral CI users (* indicates a significant main effect of group, when averaged across both hemispheres). Error bars represent SE. (b) illustrates the symmetry in aural preference of the left and right hemisphere with greater variability in bilateral CI users. (c) illustrates the positive correlation between the right and left CI speech scores

Figure 7

(a and b) plot the voxels showing significant differences in dipole moment between unilateral conditions, and bilateral and unilateral conditions evaluated within each group for each response peak (P1/Pci, N2) using 10000 permutations (corrected for multiple comparisons using a Bonferroni correction; p = .05/62 = 0.0008; Jiwani et al., 2016). Only axial images are shown. Hotter colors indicate greater activity in the left‐unilateral condition in (a) and in the bilateral condition in (b). Children with bilateral CIs show fewer differences than children with normal hearing (a, b) and greater activity in the occipital lobe when bilateral conditions are contrasted with unilateral conditions (b). (c) illustrates between‐group differences; hotter colors in the left frontal lobe indicate significantly higher dipole moment in the CI group and cooler colors in the inferior parieto‐occipital regions indicate significantly higher dipole moment in the normal hearing group