Effect of stimulus level on the temporal response properties of the auditory nerve in cochlear implants

Abstract

Electrically evoked compound action potentials (ECAPs) have been used to examine temporal response patterns of the auditory nerve in cochlear implant (CI) recipients. ECAP responses to individual pulses in a pulse train vary across stimulation rates for individual CI users. For very slow rates, auditory neurons have ample time to discharge, recover, and respond to each pulse in the train. As the pulse rate increases, an alternating ECAP-amplitude pattern occurs. As the stimulation rate increases further, the alternating pattern eventually ceases and the overall ECAP amplitudes are diminished, yielding a relatively stochastic state that presumably reflects a combination of adaptation, desynchronization, and facilitation across fibers. Because CIs operate over a range of current levels in everyday use, it is important to understand auditory-nerve responses to pulse trains over a range of levels. The effect of stimulus level on ECAP temporal response patterns in human CI users has not been well studied. The first goal of this study was to examine the effect of stimulus level on various aspects of ECAP temporal responses to pulse-train stimuli. Because higher stimulus levels yield more synchronous responses and faster recovery, it was hypothesized that: (1) the maximum alternation would occur at slower rates for lower levels and faster rates at higher levels, (2) the alternation depth at its maximum would be smaller for lower levels, (3) the rate that produces a stochastic state (‘stochastic rate’) would decrease with level, (4) adaptation would be greater for lower levels as a result of slower recovery, and (5) refractory-recovery time constants would be longer (slower) for lower levels, consistent with earlier studies. The second goal of this study was to examine how refractory-recovery time constants relate specifically to maximum alternation and stochastic rate. Data were collected for 12 ears in 10 CI recipients. ECAPs were recorded in response to each of 13 pulses in an equal-amplitude pulse train ranging in rate from 900–3500 pps for three levels (low, medium, high). The results generally supported hypotheses 1–4; there were no significant effects of level on the refractory-recovery time constants (hypothesis 5). When data were pooled across level, there was a significant negative correlation between alternation depth and refractory recovery time. Understanding the effects of stimulus level on auditory-nerve responses may provide further insight into improving the use of objective measures for potentially optimizing speech-processing strategies.

Neural Adaptation of the Electrically Stimulated Auditory Nerve Is Not Affected by Advanced Age in Postlingually Deafened, Middle-aged, and Elderly Adult Cochlear Implant Users

“…In addition to acoustic stimulation, AN fibers adapt to continuous electrical stimulation (e.g., Wilson et al 1997;Haenggeli et al 1998;Matsuoka et al 2000aMatsuoka et al , 2000bLitvak et al 2001;Hay-McCutcheon et al 2005;Zhang et al 2007;Miller et al 2008;Heffer et al 2010;Hughes et al 2012Hughes et al , 2014He et al 2016;Hughes & Laurello 2017). Results of single-unit studies using animal models demonstrated that the discharge rate of electrically stimulated AN fibers to sustained pulse-train stimulation showed a rapid decline followed by a gradual decrease over the course of up to 200 ms (van den Honert & Stypulkowski 1987;Javel et al 1987;Litvak et al 2001;Zhang et al 2007).…”

“…Compared with results reported in animal models, data recorded in human CI users demonstrate a greater degree of alternation across a wider range of stimulation levels and pulse rates (Wilson et al 1994;Finley et al 1997;Matsuoka et al 2000a). This alternating response pattern disappears at higher pulse rates due to combined effects of refractory recovery, adaptation, and increased temporal jitter (Wilson et al 1997;Hay-McCutcheon et al 2005;Mino and Rubinstein 2006;Miller et al 2008;Hughes et al 2012Hughes et al , 2014McKay et al 2013;He et al 2016;Hughes & Laurello 2017). The rate at which the alternating pattern is no longer evident is defined as the stochastic rate.…”

“…In human CI users, the stochastic rate can range from 900 to 3500 pulses per second (pps) per channel (Hughes et al 2012). The amount of neural adaptation, as quantified by comparing amplitudes of the eCAPs elicited by pulses occurring later in the pulse train to eCAP amplitudes elicited by earlier pulses (Hay-McCutcheon et al 2005;Hughes et al 2012;He et al 2016), increases with pulse rate and stimulus duration (Wilson et al 1997;Haenggeli et al 1998;Matsuoka et al 2000aMatsuoka et al , 2000bHughes et al 2012Hughes et al , 2014He et al 2016), and decreases with stimulation level (Hughes & Laurello 2017). In this study, the term "adaptation" refers to a reduction in the eCAP amplitude for sustained pulse-train stimulation regardless of underlying mechanisms.…”

“…Several studies have used eCAPs evoked by pulse-train stimuli to assess neural adaptation of the AN in human CI users (e.g., Wilson et al 1997; Hay-McCutcheon et al 2005; Hughes et al 2012, 2014; He et al 2016; Hughes & Laurello 2017), as well as in animal models (e.g., Haenggeli et al 1998; Matsuoka et al 2000a, 2000b). In general, results recorded in human CI users are consistent with those reported for animal models.…”

Prognostics Factors of Cochlear Implant in Adults: How Can We Improve Poorer Performers?

“…Postoperative NRT testing may be indicated to assess neural recovery functions to gain information about beneficial stimulation rates. From their studies on the temporal characteristics of auditory nerve stimulation via CIs, [16] suggest that the programmed stimulation rate relates to the refractory period of the nerve. CI user performance may be addressed, in some cases, by reducing the stimulation rate.…”