Electrical Excitation of the Acoustically Sensitiv

Authors: Charles A Miller Paul J Abbas Barbara K Robinson Kirill V Nourski Fawen Zhang FuhCherng Jeng

Publish Date: 2006/05/16

Volume: 7, Issue: 3, Pages: 195-210

PDF Link

Abstract

Nearly all studies on auditorynerve responses to electric stimuli have been conducted using chemically deafened animals so as to more realistically model the implanted human ear that has typically been profoundly deaf However clinical criteria for implantation have recently been relaxed Ears with “residual” acoustic sensitivity are now being implanted calling for the systematic evaluation of auditorynerve responses to electric stimuli as well as combined electric and acoustic stimuli in acoustically sensitive ears This article presents a systematic investigation of singlefiber responses to electric stimuli in acoustically sensitive ears Responses to 250 pulse/s electric pulse trains were collected from 18 cats Properties such as threshold dynamic range and jitter were found to differ from those of deaf ears Other types of fiber activity observed in acoustically sensitive ears ie spontaneous activity and electrophonic responses were found to alter the temporal coding of electric stimuli The electrophonic response which was shown to greatly change the information encoded by spike intervals also exhibited fast adaptation relative to that observed in the “direct” response to electric stimuli More complex responses such as “buildup” increased responsiveness to successive pulses and “bursting” alternating periods of responsiveness and unresponsiveness were observed Our findings suggest that bursting is a response unique to sustained electric stimulation in ears with functional hair cellsThe criteria for cochlearimplant candidacy have recently been expanded to include individuals with significant “residual” lowfrequency hearing with promising results von Ilberg et al 1999 Gantz and Turner 2003 Animal models show that hair cells apical to implanted electrode arrays can survive over chronic periods Ni et al 1992 Xu et al 1997 and human studies indicate that acoustic sensitivity can be preserved after implantation Kiefer et al 1998 The standard animal model for cochlear implant research has long used a deaf cochlea to isolate the direct electrical depolarization of auditory nerve fibers ie the “α” response of Moxon 1971 However a new animal model is needed to study how electric stimulus coding is modified by viable hair cells which may occur through several possible mechanismsMoxon 1971 not only described the α response but a β response in response to electric stimulation of hearing ears It is attributed to electrically induced contraction of outer hair cells OHCs production of a traveling wave and normal excitation of nerve fibers by inner hair cell IHC activity Brownell et al 1985 Nuttall and Ren 1995 As β responses can occur coincidently with α responses van den Honert and Stypulkowski 1984 they could result in relatively complex temporal responsesModification of electric responses may not require activation of hair cells but simply the existence of spontaneous activity Such activity could modify α responses by placing fibers in states of partial refractoriness thereby altering their responses cf Miller et al 2001aEfferent effects could involve the medial olivocochlear MOC or the lateral olivocochlear LOC systems which project primarily to OHCs and peripheral axons of afferents respectively Warr and Guinan 1979 Although deafness would wipe out MOC functionality LOC effects may persist if peripheral terminals remain Thus the normal cochlea may be influenced by both systems whereas LOC effects may occur in deafened ears with peripheral processesIHCs may be excited through direct depolarization of their membranes which presumably leads to the δ response an infrequent response described by van den Honert and Stypulkowski 1984 IHC depolarization may also modulate spontaneous spike activityThese mechanisms could conceivably improve electric stimulus coding or interfere with it We recognize that electric hearing in acoustically sensitive ears may involve peripheral and central mechanisms however a clear understanding of effects at the level of the auditory nerve will not only elucidate peripheral mechanisms but also improve the ability to interpret central measuresIn addition to the singlefiber studies mentioned above von Ilberg et al 1999 examined auditory nerve fiber responses to acoustic and electric stimuli focusing primarily on the nerves capacity to respond independently to both In contrast our study addresses how acoustic sensitivity alters fiber responses to electric stimuli paralleling to some degree our earlier work that examined the electrically evoked compound action potential ECAP Hu et al 2003 Nourski et al 2005 This study developed an acute animal model using a minimally invasive intracochlear electrode to preserve as much hearing as possible We therefore sought not to model a human implant candidate with residual hearing but to maximize the contrasts between deaf and hearing ears Prior to addressing these goals we characterized our animal preparations in terms of their ability to model acoustically sensitive ears so that limitations could be identified A moderaterate 250 pulse/s electric pulse train was used to examine a stimulus relevant to auditory prostheses while providing for the ability to examine both the α and β responses Another effort to be reported in a subsequent article will address how combined acoustic and electric stimuli modify singlefiber responses evoked by electric stimuli

Keywords: