The pattern of auditory brainstem response wave V maturation in cochlear-implanted children

OBJECTIVE Maturation of acoustically evoked brainstem responses (ABR) in hearing children is not complete at birth but rather continues over the first two years of life. In particular, it has been established that the decrease in ABR wave V latency can be modeled as the sum of two decaying exponential functions with respective time-constants of 4 and 50 weeks [Eggermont, J.J., Salamy, A., 1988a. Maturational time-course for the ABR in preterm and full term infants. Hear Res 33, 35-47; Eggermont, J.J., Salamy, A., 1988b. Development of ABR parameters in a preterm and a term born population. Ear Hear 9, 283-9]. Here, we investigated the maturation of electrically evoked auditory brainstem responses (EABR) in 55 deaf children who recovered hearing after cochlear implantation, and proposed a predictive model of EABR maturation depending on the onset of deafness. The pattern of EABR maturation over the first 2 years of cochlear implant use was compared with the normal pattern of ABR maturation in hearing children. METHODS Changes in EABR wave V latency over the 2 years following cochlear implant connection were analyzed in two groups of children. The first group (n=41) consisted of children with early-onset of deafness (mostly congenital), and the second (n=14) of children who had become profoundly deaf after 1 year of age. The modeling of changes in EABR wave V latency with time was based on the mean values from each of the two groups, allowing comparison of the rates of EABR maturation between groups. Differences between EABRs elicited at the basal and apical ends of the implant electrode array were also tested. RESULTS There was no influence of age at implantation on the rate of wave V latency change. The main factor for EABR changes was the time in sound. Indeed, significant maturation was observed over the first 2 years of implant use only in the group with early-onset deafness. In this group maturation of wave V progressed as in the ABR model of [Eggermont, J.J., Salamy, A., 1988a. Maturational time-course for the ABR in preterm and full term infants. Hear Res 33, 35-47; Eggermont, J.J., Salamy, A., 1988b. Development of ABR parameters in a preterm and a term born population. Ear Hear 9, 283-9] of normal hearing children: a sum of two decaying exponential functions, one showing an early rapid decrease in latency and the other a slower decrease. Remarkably, the time-constants fell well within the ranges described by Eggermont and Salamy (i.e., 3.9 and 68 weeks), consistent with the time-course of the neurophysiological mechanisms presumably involved in auditory pathway maturation during the first 2 years of life: i.e., myelination and increased synaptic efficacy. In contrast, relatively little change in wave V was evident in children with late-onset deafness. In agreement with the notion that EABR maturation follows an apex-to-base gradient as described for ABR, we observed that wave V latencies were longer for the basal than the apical end of the implant electrode array and remained so throughout the study period, whatever the time of onset of deafness. CONCLUSIONS The findings in the early-onset of deafness group support the theory that auditory pathways remain "frozen" during the period of sensory deprivation until cochlear implant rehabilitation restores the normal chronology of maturational processes. In children with late-onset deafness, however, some maturational processes may occur before the onset of deafness, and thus less additional maturation is required during the first two years of implant use resulting in no significant EABR latency changes being observed in this period. The results suggest that the rehabilitation-induced plasticity of the auditory pathways is, in case of late auditory deprivation, unlikely to result in neurophysiological outcomes similar to those observed in children with early auditory deprivation. SIGNIFICANCE Changes in EABR wave V latency over the first 2 years of cochlear implant use were found to be well fitted by the sum of two decaying exponential functions in children with early-onset deafness. This is in line with the maturation of ABR wave V latency in normal-hearing children over the first two years of life. Further studies are needed to assess whether the differences observed in terms of auditory pathways maturation are associated with consistent differences in terms of language development.

[1]  R. Illing Activity-Dependent Plasticity in the Adult Auditory Brainstem , 2001, Audiology and Neurotology.

[2]  L. Collet,et al.  Effect of stimulus intensity variation on brain-stem auditory evoked potentials: comparison between neonates and adults. , 1987, Electroencephalography and clinical neurophysiology.

[3]  A. Starr,et al.  Development of auditory function in newborn infants revealed by auditory brainstem potentials. , 1977, Pediatrics.

[4]  Charles A. Miller,et al.  Electrically evoked auditory brainstem response to stimulation of different sites in the cochlea , 1993, Hearing Research.

[5]  E. Truy,et al.  Electrophysiological Findings in Two Bilateral Cochlear Implant Cases: Does the Duration of Deafness Affect Electrically Evoked Auditory Brain Stem Responses? , 2002, The Annals of otology, rhinology, and laryngology.

[6]  B. Papsin,et al.  Effects of cochlear implant use on the electrically evoked middle latency response in children , 2005, Hearing Research.

[7]  Jos J. Eggermont,et al.  Maturational time course for the ABR in preterm and full term infants , 1988, Hearing Research.

[8]  C W Ponton,et al.  Prolonged deafness limits auditory system developmental plasticity: evidence from an evoked potentials study in children with cochlear implants. , 1999, Scandinavian audiology. Supplementum.

[9]  Cheng Ak,et al.  Meta-analysis of pediatric cochlear implant literature. , 1999 .

[10]  J. Niparko,et al.  Restoration of Auditory Nerve Synapses in Cats by Cochlear Implants , 2005, Science.

[11]  Myelination of the Human Auditory Nerve: Different Time Courses for Schwann Celland Glial Myelin , 2001, The Annals of otology, rhinology, and laryngology.

[12]  P. Stypulkowski,et al.  Characterization of the electrically evoked auditory brainstem response (ABR) in cats and humans , 1986, Hearing Research.

[13]  Eric Truy,et al.  Modeling the relationship between psychophysical perception and electrically evoked compound action potential threshold in young cochlear implant recipients: clinical implications for implant fitting , 2004, Clinical Neurophysiology.

[14]  B. Papsin,et al.  Auditory Brain Stem and Midbrain Development after Cochlear Implantation in Children , 2002, The Annals of otology, rhinology & laryngology. Supplement.

[15]  M. Dorman,et al.  A Sensitive Period for the Development of the Central Auditory System in Children with Cochlear Implants: Implications for Age of Implantation , 2002, Ear and hearing.

[16]  J. Eggermont On the rate of maturation of sensory evoked potentials. , 1988, Electroencephalography and clinical neurophysiology.

[17]  H. Kinney,et al.  Sequence of Central Nervous System Myelination in Human Infancy. II. Patterns of Myelination in Autopsied Infants , 1988, Journal of neuropathology and experimental neurology.

[18]  W. Doyle,et al.  Maturation of the auditory brain stem response (ABR): additional perspectives. , 1984, Ear and hearing.

[19]  B. Papsin,et al.  An Evoked Potential Study of the Developmental Time Course of the Auditory Nerve and Brainstem in Children Using Cochlear Implants , 2006, Audiology and Neurotology.

[20]  Nina Kraus,et al.  Neurophysiology of Cochlear Implant Users I: Effects of Stimulus Current Level and Electrode Site on the Electrical ABR, MLR, and N1-P2 Response , 2002, Ear and hearing.

[21]  A. Beiter,et al.  Electrically evoked auditory brain stem responses (EABR) and middle latency responses (EMLR) obtained from patients with the nucleus multichannel cochlear implant. , 1990, Ear and hearing.

[22]  B. Papsin,et al.  Activity-Dependent Developmental Plasticity of the Auditory Brain Stem in Children Who Use Cochlear Implants , 2003, Ear and hearing.

[23]  A. Starr,et al.  Brain Stem Potentials Evoked by Electrical Stimulation of the Cochlea in Human Subjects , 1979, The Annals of otology, rhinology, and laryngology.

[24]  B. Ryals,et al.  Development of the place principle: acoustic trauma. , 1983, Science.

[25]  S. Trehub,et al.  Auditory Development in Infancy , 1985 .

[26]  J. Eggermont,et al.  Development of ABR parameters in a preterm and a term born population. , 1988, Ear and hearing.

[27]  A. J. Klein,et al.  An analysis of auditory brainstem responses in infants , 1982, Hearing Research.

[28]  Donald K. Eddington,et al.  Cochlear Implants in Adults and Children , 1995 .

[29]  E. Truy,et al.  EABRs and surface potentials with a transcutaneous multielectrode cochlear implant. , 1997, Acta oto-laryngologica.

[30]  J. Kronenberg,et al.  Electrical Stimulation Levels and Electrode Impedance Values in Children Using the Med-El Combi 40+ Cochlear Implant: A One Year Follow-Up , 2005, Journal of basic and clinical physiology and pharmacology.

[31]  L. Collet,et al.  Effect of brainstem auditory evoked potential stimulus intensity variations in neonates of small for gestational age , 1988, Brain and Development.

[32]  J. Eggermont,et al.  Maturational delays in cortical evoked potentials in cochlear implant users. , 1997, Acta oto-laryngologica.

[33]  J. Eggermont Mathematical models for developmental changes. , 1985, Acta oto-laryngologica. Supplementum.

[34]  G. Woodworth,et al.  Results of multichannel cochlear implants in congenital and acquired prelingual deafness in children: five-year follow-up. , 1994, The American journal of otology.

[35]  Kenzo Takeshita,et al.  Functional and morphometrical maturation of the brainstem auditory pathway , 1987, Brain and Development.

[36]  R. Galamboš,et al.  Brain stem auditory evoked responses in human infants and adults. , 1974, Archives of otolaryngology.

[37]  Nina Kraus,et al.  Auditory training improves neural timing in the human brainstem , 2005, Behavioural Brain Research.

[38]  B Frachet,et al.  Cochlear implant performance and electrically-evoked auditory brain-stem response characteristics. , 1998, Electroencephalography and clinical neurophysiology.

[39]  C. Micheyl,et al.  Loudness growth functions and EABR characteristics in Digisonic cochlear implantees. , 1999, Acta oto-laryngologica.

[40]  Jean K. Moore,et al.  Time course of axonal myelination in the human brainstem auditory pathway , 1995, Hearing Research.

[41]  M. Dorman,et al.  The influence of a sensitive period on central auditory development in children with unilateral and bilateral cochlear implants , 2005, Hearing Research.

[42]  C W Ponton,et al.  Auditory Brain Stem Response Generation by Parallel Pathways: Differential Maturation of Axonal Conduction Time and Synaptic Transmission , 1996, Ear and hearing.

[43]  Yael Henkin,et al.  Changes over time in electrical stimulation levels and electrode impedance values in children using the Nucleus 24M cochlear implant. , 2003, International Journal of Pediatric Otorhinolaryngology.

[44]  J. Eggermont Development of auditory evoked potentials. , 1992, Acta oto-laryngologica.

[45]  J. Eggermont,et al.  Of Kittens and Kids: Altered Cortical Maturation following Profound Deafness and Cochlear Implant Use , 2001, Audiology and Neurotology.

[46]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[47]  A. Krumholz,et al.  Maturation of the brain-stem auditory evoked potential in premature infants. , 1985, Electroencephalography and clinical neurophysiology.

[48]  Maike Vollmer,et al.  The effects of chronic intracochlear electrical stimulation on inferior colliculus spatial representation in adult deafened cats , 2002, Hearing Research.

[49]  Jos J. Eggermont,et al.  Auditory-evoked Potential Studies of Cortical Maturation in Normal Hearing and Implanted Children: Correlations with Changes in Structure and Speech Perception , 2003, Acta oto-laryngologica.

[50]  M. Dorman,et al.  Rapid development of cortical auditory evoked potentials after early cochlear implantation , 2002, Neuroreport.

[51]  J. Eggermont,et al.  Maturation of Human Cortical Auditory Function: Differences Between Normal‐Hearing Children and Children with Cochlear Implants , 1996, Ear and hearing.

[52]  J. Eggermont,et al.  Auditory system plasticity in children after long periods of complete deafness , 1996, Neuroreport.

[53]  J. Eggermont Physiology of the Developing Auditory System , 1985 .

[54]  E. Truy,et al.  Relationship between NRT measurements and behavioral levels in children with the Nucleus 24 cochlear implant may change over time: preliminary report. , 2001, International journal of pediatric otorhinolaryngology.

[55]  Perinatal Maturation of the Auditory Brain Stem Response: Changes in Path Length and Conduction Velocity , 1996, Ear and hearing.