Effects of long-term unilateral cochlear implant use on large-scale network synchronization in adolescents

Unilateral cochlear implantation (CI) limits deafness-related changes in the auditory pathways but promotes abnormal cortical preference for the stimulated ear and leaves the opposite ear with little protection from auditory deprivation. In the present study, time-frequency analyses of event-related potentials elicited from stimuli presented to each ear were used to determine effects of unilateral CI use on cortical synchrony. CI-elicited activity in 34 adolescents (15.4±1.9 years of age) who had listened with unilateral CIs for most of their lives prior to bilateral implantation were compared to responses elicited by a 500Hz tone-burst in normal hearing peers. Phase-locking values between 4 and 60Hz were calculated for 171 pairs of 19-cephalic recording electrodes. Ear specific results were found in the normal hearing group: higher synchronization in low frequency bands (theta and alpha) from left ear stimulation in the right hemisphere and more high frequency activity (gamma band) from right ear stimulation in the left hemisphere. In the CI group, increased phase synchronization in the theta and beta frequencies with bursts of gamma activity were elicited by the experienced-right CI between frontal, temporal and parietal cortical regions in both hemispheres, consistent with increased recruitment of cortical areas involved in attention and higher-order processes, potentially to support unilateral listening. By contrast, activity was globally desynchronized in response to initial stimulation of the naïve-left ear, suggesting decoupling of these pathways from the cortical hearing network. These data reveal asymmetric auditory development promoted by unilateral CI use, resulting in an abnormally mature neural network.