Cortical imbalance following delayed restoration of bilateral hearing in deaf adolescents

Abstract

Unilateral auditory deprivation in early childhood can lead to cortical strengthening of inputs from the stimulated side, yet the impact of this on bilateral processing when inputs are later restored beyond an early sensitive period is unknown. To address this, we conducted a longitudinal study with 13 bilaterally profoundly deaf adolescents who received unilateral access to sound via a cochlear implant (CI) in their right ear in early childhood before receiving bilateral access to sound a decade later via a second CI in their left ear. Auditory-evoked cortical responses to unilateral and bilateral stimulation were measured repeatedly using electroencephalogram from 1 week to 14 months after activation of their second CI. Early cortical responses from the newly implanted ear and bilateral stimulation were atypically lateralized to the left ipsilateral auditory cortex. Duration of unilateral deafness predicted an unexpectedly stronger representation of inputs from the newly implanted, compared to the first implanted ear, in left auditory cortex. Significant initial reductions in responses were observed, yet a left-hemisphere bias and unequal weighting of inputs favoring the long-term deaf ear did not converge to a balanced state observed in the binaurally developed system. Bilateral response enhancement was significantly reduced in left auditory cortex suggesting deficits in ipsilateral response inhibition of new, dominant, inputs during bilateral processing. These findings paradoxically demonstrate the adaptive capacity of the adolescent auditory system beyond an early sensitive period for bilateral input, as well as restrictions on its potential to fully reverse cortical imbalances driven by long-term unilateral deafness.

Keywords: auditory development; bilateral processing; binaural; cortical plasticity; deafness; electroencephalography; hemispheric asymmetry; longitudinal; pediatric; sequential cochlear implantation.

FIGURE 1

Timeline of EEG recordings for each participant. Participants completed multiple EEG recording sessions over the first year of bilateral CI use. All participants had a “baseline” recording at 1–2 weeks following initial activation of their second CI, and at least one “follow‐up” recording spanning from 1 to 14 months of bilateral CI use. The four categorical time groupings used in subsequent analyses are indicated by shaded boxes and labels. Points are color‐coded and labeled by participant number that are ordered by age at CI‐1. Note that for Participant #3, only their Month 3 data were included in analyses where time was treated as a categorical factor. Both Months 3 and 4 data were included in supplementary modeling when time was treated as a continuous factor

FIGURE 2

Evoked potentials with increased bilateral CI use. (a) Global field power (GFP) and (b) group mean surface potentials at the vertex recording channel (Cz) are shown for unilateral and bilateral stimulation, paneled by duration of bilateral CI use. Solid line indicates mean and shaded region ± SE. (c) Topographic distributions of mean activity across the surface of the head at the peak latency of the first identifiable component in the GFP. For each child, surface activity was averaged across a 5‐ms time window centered on the peak latency of the first component. Mean peak latency is indicated for each stimulation condition at each time point. (d) Axial view of mean evoked source activity in ~64,000 voxels evaluated using the TRACs beamformer (higher signal‐to‐noise ratio, omnibus‐corrected pseudo‐Z, in red). The highest level of activation is consistently seen in the left auditory cortex regardless of the stimulation condition or time point

FIGURE 3

Changes in amplitude of auditory cortical activity with increased bilateral CI use. Amplitude of cortical activation (omnibus‐corrected pseudo‐Z) plotted for each child, with estimated marginal means from the linear mixed‐effect regression model (white‐filled points) and bars representing ±1 SE

FIGURE 4

Cortical lateralization and bilateral speech perception. (a) Cortical lateralization (%) with increased bilateral CI use plotted for each child, with estimated marginal means from the linear mixed‐effect regression model (white‐filled points) and bars representing ±1 SE. (b) Stronger atypical left‐hemispheric lateralization at baseline is associated with poorer bilateral speech perception ability in the future (mean ± SD = 17.2 ± 18.6 months post‐CI‐2)

FIGURE 5

Asymmetrical cortical representation of auditory inputs and duration of unilateral deprivation. (a) Cortical representation (%) of new and established inputs in the auditory cortices, illustrating dominance of the left newly implanted ear in both auditory cortices. Values are plotted for each child as a function of increased bilateral CI use with estimated marginal means from the linear mixed‐effect regression model (white‐filled points) and bars representing ±1 SE. (b) Greater asymmetrical cortical representation of new inputs from the left ear at initial CI‐2 use is predicted by a longer duration of unilateral deprivation/stimulation

FIGURE 6

Bilateral response enhancement and bilateral speech perception benefit. (a) Bilateral enhancement (omnibus‐corrected pseudo‐Z) in the left and right auditory cortex over time. Grey lines indicate significant post hoc Tukey HSD comparisons (*p < .005, **p < .001). (b) Amount of improvement in speech perception provided by each ear in bilateral conditions (improvement in speech perception that each ear provided in bilateral listening conditions, compared to when listening with the opposite ear only) as a proportion of possible improvement. Grey lines indicate significant paired t test comparisons (*p < .05). (c) Associations between bilateral response enhancement in the left and right auditory cortex and bilateral speech perception benefit obtained by the ipsilateral ear