Electrical Excitation of the Acoustically Sensitive Auditory Nerve: Single-Fiber Responses to Electric Pulse Trains

Abstract

Nearly all studies on auditory-nerve 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 Bresidualâ coustic sensitivity are now being implanted, calling for the systematic evaluation of auditory-nerve responses to electric stimuli as well as combined electric and acoustic stimuli in acoustically sensitive ears. This article presents a systematic investigation of single-fiber 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 (i.e., 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 Bdirect^response to electric stimuli. More complex responses, such as Bbuildup^(increased responsiveness to successive pulses) and Bbursting^(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 cells.

Effects of Hearing Preservation on Psychophysical Responses to Cochlear Implant Stimulation

“…In the absence of hair cells, the auditory nerve is normally silent, but when hair cells are present, there is spontaneous activity, which can affect the responses of the nerve to electrical stimulation (Wilson 1997;Haenggeli et al 1998;Hu et al 2003;Miller et al 2006). In our study, the presence or absence of spontaneous activity in the auditory nerve was assessed by recording ensemble activity (Dolan et al 1990;Searchfield et al 2004) from the cochlear implant electrodes in all group I animals and in four group II animals.…”

“…However, it is probable that surviving hair cells and related cochlear elements also directly affect electrical hearing. Cochlear implant function in hearing versus deaf ears has been studied in some detail at the neurophysiological level (Moxon 1971;van den Honert and Stypulkowski 1984;Shepherd and Javel 1997;Miller et al 2006), but we know less about the effects of preserved acoustic hearing on the responses to electrical stimulation at the psychophysical perceptual level. Thus, studies exploring the effects of preserving acoustic hearing on the perception of cochlear implant electrical stimulation are needed.…”

“…There are several possible mechanisms by which this might occur. Electrical stimulation can result in basilar membrane motion by several mechanisms, including electrically induced contraction of outer hair cells (OHCs), resulting in mechanical stimulation of inner hair cells (IHCs) and electrophonic hearing (Stevens and Jones 1939;Moxon 1971;van den Honert and Stypulkowski 1984;McAnally et al 1993;Nuttall and Ren 1995;Le Prell et al 2006;Miller et al 2006). It is also possible that the radial component of the electrical current results in direct excitation of the peripheral process and/or the IHC (van den Honert and Stypulkowski 1984).…”

Tonotopic Distribution of Short-Term Adaptation Properties in the Cochlear Nerve of Normal and Acoustically Overexposed Chicks

“…In spite of this, the rate of vesicle fusion decreases on a time scale similar to that of short-term adaptation (Moser and Beutner 2000;Spassova et al 2004), and refilling of the emptied vesicle pool is kinetically similar to recovery from this adaptation ). Adaptation resulting from direct electrical stimulation of the auditory nerve (i.e., bypassing the hair cell) contrasts with acoustically evoked adaptation in that it is mild and seen only under certain conditions (Parkins 1989;Javel 1996;Miller et al 2006). Miller et al (2006) also note that adaptation to electric stimuli can be reduced by increasing the level of stimulation, a phenomenon not seen with acoustic stimulation.…”

“…Adaptation resulting from direct electrical stimulation of the auditory nerve (i.e., bypassing the hair cell) contrasts with acoustically evoked adaptation in that it is mild and seen only under certain conditions (Parkins 1989;Javel 1996;Miller et al 2006). Miller et al (2006) also note that adaptation to electric stimuli can be reduced by increasing the level of stimulation, a phenomenon not seen with acoustic stimulation. Furthermore, the insensitivity of chick short-term adaptation kinetics to temperature change is an argument against a role for neural refractoriness or receptor desensitization in adaptation (Crumling and Saunders 2005).…”