Michael D. Waring

Maturation of human cortical auditory function : Differences between normal-hearing children and children with cochlear implants

Objective: We investigated maturation of cortical auditory function in normal‐hearing children and in children who receive stimulation of their auditory system through a cochlear implant. Design: As a measure of cortical auditory function, auditory evoked responses(AERs) were recorded from normal‐hearing children and adults as well as from children and adults fitted with a cochlear implant. Morphological and latency changes for evoked responses recorded at electrode Cz are reported. Results: For normal‐hearing children, there is a gradual evolution of AER features that extends through adolescence, with P1 latency becoming adult‐like in the late teens. Latency changes for P1 occur at the same rate for implanted children, but the overall maturation sequence is delayed. By extrapolation from the existing data, the age at which P1 latency becomes adult‐like is delayed by approximately 5 yr for the implanted population. Other typical features of the AER, namely N1 and P2, are either delayed in developing or absent in the implanted children. Conclusions: These preliminary findings suggest both similarities and differences in cortical auditory maturation for normal‐hearing and implanted children. For implanted children, the 5 yr delay for maturation of P1 latency roughly corresponds to the average 4.5 yr interval between the onset of deafness and the time of implantation. These findings suggest that during the period of deafness, maturation of cortical auditory function does not progress. However, some, if not all, maturational processes resume after stimulation is reintroduced.

Auditory system plasticity in children after long periods of complete deafness

DEAF children fitted with a cochlear implant provide a unique opportunity to examine the effects of auditory deprivation on the maturation of the human auditory system. We compared cortical evoked potentials recorded in implanted and normal-hearing children and found that age-dependent latency changes for the P1component, fitted to a decaying exponential curve, showed the same rate of maturation. For implanted children, however, maturational delays for P1 latency approximated the period of auditory deprivation prior to implantation. This indicates the auditory system does not mature without stimulation. Nonetheless, the auditory system retains its plasticity during the period of deafness since the re-introduction of stimulation by the cochlear implant resumes the normal maturational sequence.

Maturational Delays in Cortical Evoked Potentials in Cochlear Implant Users

We studied the effects of prolonged auditory deprivation in children in whom auditory stimulation was restored by a cochlear implant. The latency of the P1 component of the late cortical potential was used as the indicator of auditory system maturation. For normal-hearing children there is a gradual evolution of evoked potential features that extends through adolescence with P1 latency becoming adult-like at about age 15. It appears that maturation of P1 latency in normal and implanted children occurs at the same rate, but the time to maturity in implanted subjects is delayed by an amount approximately equal to the duration of deafness.

Auditory brain-stem responses evoked by electrical stimulation of the cochlear nucleus in human subjects.

When auditory nerve function is lost due to surgical removal of bilateral acoustic tumors, a sense of hearing may be restored by means of an auditory brain-stem implant (ABI), which electrically stimulates the auditory pathway at the level of the cochlear nucleus. Placement of the stimulating electrodes during surgical implantation may be aided by electrically evoked auditory brain-stem responses (EABRs) recorded intra-operatively. To establish preliminary standards for human EABRs evoked by electrical stimulation of the cochlear nucleus, short-latency evoked potentials were recorded from 6 ABI patients who were either already implanted or undergoing implantation surgery. Neural responses were distinguished from stimulus artifact and equipment artifact by their properties during stimulus polarity reversal and amplitude variation. Other properties contributed to further identification of the evoked potentials as auditory responses (EABRs). The response waveforms generally had 2 or 3 waves. The peak latencies of these waves (approximately 0.3, 1.3, and 2.2 msec) and the brain-stem localization of the region from which they could be elicited are consistent with auditory brain-stem origin.

Spatio-temporal source modeling of evoked potentials to acoustic and cochlear implant stimulation

Spatio-temporal source modeling (STSM) of event-related potentials was used to estimate the loci and characteristics of cortical activity evoked by acoustic stimulation in normal hearing subjects and by electrical stimulation in cochlear implant (CI) subjects. In both groups of subjects, source solutions obtained for the N1/P2 complex were located in the superior half of the temporal lobe in the head model. Results indicate that it may be possible to determine whether stimulation of different implant channels activates different regions of cochleotopically organized auditory cortex. Auditory system activation can be assessed further by examining the characteristics of the source wave forms. For example, subjects whose cochlear implants provided auditory sensations and normal hearing subjects had similar source activity. In contrast, a subject in whom implant activation evoked eyelid movements exhibited different source wave forms. STSM analysis may provide an electrophysiological technique for guiding rehabilitation programs based on the capabilities of the individual implant user and for disentangling the complex response patterns to electrical stimulation of the brain.

Electrically evoked auditory brainstem response monitoring of auditory brainstem implant integrity during facial nerve tumor surgery

Evoked potentials identified as electrically evoked auditory brainstem responses (EABRs) have been recorded from a patient in response to electrical stimulation of the cochlear nucleus via an auditory brainstem implant. Recording such EABRs during surgery for removal of an ipsilateral facial nerve tumor provided a means to monitor the integrity of the implant. The presence of stable EABRs similar to those obtained before surgery indicated that the lead wires had not been severed and that the implanted electrodes had not been dislodged. EABR recording may also be useful for assisting with positioning the stimulating electrodes during initial implantation surgery, by verifying that stimulation can activate the auditory system.

Refractory properties of auditory brain-stem responses evoked by electrical stimulation of human cochlear nucleus: evidence of neural generators

In this study of electrically-evoked auditory brain-stem responses (EABRs) elicited by cochlear nucleus stimulation, 3 waves were identified after the initial wave that is directly initiated by the electric stimulus. Varying the rate of periodic stimulation or the interval between pairs of stimuli revealed that the shorter the latency of a wave, the faster it recovered from activation (i.e. shorter refractory period). The slow recovery of the third wave and an accompanying contribution to the second wave could be accounted for by postsynaptic generation in the two medial superior olivary nuclei (MSO); the faster recovery of another contribution to the second wave by generation in an axonal tract bending around the contralateral MSO; and the fastest recovery of the first wave by another axonal pathway having larger axons. Comparison with the relative latencies and spatial distribution of an acoustically-evoked auditory brain-stem response (AABR) indicated that the third wave corresponds to wave V, the second to wave IV (called IVb), and the first to a wave that precedes wave IV (called IVa). The anatomical interpretations for the two later waves of the EABR are consistent with most of the extant data on the neural generators of AABR waves IV and V. Thus, the present data and analysis strengthen the identification of the electrically evoked responses as EABRs and provide a firmer foundation for intra-operative EABR monitoring to assist auditory brain-stem implant placement.

Activating separate ascending auditory pathways produces different human thalamic/cortical responses

When auditory nerve function is lost due to surgical removal of bilateral acoustic tumors in cases of neurofibromatosis type 2, a sense of hearing may be restored by means of an auditory brainstem implant (ABI), which electrically stimulates the cochlear nucleus. Electrically evoked auditory brainstem responses recorded from ABI subjects exhibit a variety of waveforms due to the presence or absence of different components. Evidently, ABI stimulation activates different ascending auditory pathways in different individuals. This study examined whether such differences at the brainstem level are associated with corresponding differences at higher levels. Multichannel recordings of electrically evoked middle-latency and late auditory responses were obtained from two ABI subjects whose very different electrically evoked auditory brainstem responses represent distinct categories of waveform morphology. The waveforms of both types of response were qualitatively similar in that for each condition tested there were corresponding main peaks and troughs. Quantitatively, however, there were differences in the scalp distributions and magnitudes of all components present. One subject had distributions suggesting bilateral activation and an N1-P2 complex of large amplitude, whereas the other subject had distributions suggesting unilateral activation contralateral to the side of stimulation and an N1-P2 complex of small amplitude. The differences suggest that activation of different ascending pathways in the auditory system results in different spatial and temporal patterns of neural activity in the thalamic and/or cortical auditory areas.

Neurophysiological and psychophysical measures of duration discrimination in normal‐hearing adults and adults with cochlear implants

The ability to discriminate duration contrasts (a first approximation of voice onset time differences) was evaluated in adult cochlear implant users and normal‐hearing adults using a neurophysiological response (the mismatch negativity—MMN). The MMN is an evoked response generated by a deviant stimulus when embedded in a series of standard homogeneous stimuli. Magnitude of the MMN correlates with psychophysical discrimination thresholds indicating that the MMN provides a measure of perceived acoustic change [Kraus et al. (1996)]. The MMN thus provides a neurophysiological correlate of acoustic discrimination. The present study compared an objective statistical measure of MMN magnitude to psychophysical measures in response to duration differences of brief auditory stimuli. A ten‐click train was paired with shorter trains to create an oddball sequence. The selected duration differences were similar to voice onset time differences that distinguish voiced from voiceless speech phonemes. The MMN magnitude was measured at four scalp‐electrode locations. The relationship between neurophysiological and psychophysical thresholds was determined and comparisons were made between the normal‐hearing adults and adults with cochlear implants. While some similarities were found, the results suggest that the sensitivity to duration differences differs between normal‐hearing and cochlear implant subjects.

Human auditory system maturation: A neurophysiological comparison between normal‐hearing children and children who use a cochlear implant

Auditory‐evoked responses provide detailed, objective measures of maturational change in the central auditory system from the level of the brainstem to the cortex. Auditory‐evoked responses can reflect activity originating from three pathways: the lemniscal and nonlemniscal pathways as well as from a modality nonspecific pathway originating in the reticular activating system (RAS) and its associated thalamic nuclei. Maturational time courses for these pathways were derived from evoked response data recorded from 156 normal‐hearing subjects ranging from 5–20 years of age. Analyses of these data indicate that each pathway may have a unique developmental sequence. For normal‐hearing children, the lemniscal pathway appears to follow a longer developmental time course than either the nonlemniscal or RAS pathways. For children with implants, the developmental sequences for these pathways are differentially affected depending on onset and duration of deafness. Specifically, maturation of the lemniscal pathway is...