Temporal Properties of Chronic Cochlear Electrical Stimulation Determine Temporal Resolution of Neurons in Cat Inferior Colliculus

Abstract

As cochlear implants have become increasingly successful in the rehabilitation of adults with profound hearing impairment, the number of pediatric implant subjects has increased. We have developed an animal model of congenital deafness and investigated the effect of electrical stimulus frequency on the temporal resolution of central neurons in the developing auditory system of deaf cats. Maximum following frequencies (Fmax) and response latencies of isolated single neurons to intracochlear electrical pulse trains (charge balanced, constant current biphasic pulses) were recorded in the contralateral inferior colliculus (IC) of two groups of neonatally deafened, barbiturate-anesthetized cats: animals chronically stimulated with low-frequency signals (< or = 80 Hz) and animals receiving chronic high-frequency stimulation (> or = 300 pps). The results were compared with data from unstimulated, acutely deafened and implanted adult cats with previously normal hearing (controls). Characteristic differences were seen between the temporal response properties of neurons in the external nucleus (ICX; approximately 16% of the recordings) and neurons in the central nucleus (ICC; approximately 81% of all recordings) of the IC: 1) in all three experimental groups, neurons in the ICX had significantly lower Fmax and longer response latencies than those in the ICC. 2) Chronic electrical stimulation in neonatally deafened cats altered the temporal resolution of neurons exclusively in the ICC but not in the ICX. The magnitude of this effect was dependent on the frequency of the chronic stimulation. Specifically, low-frequency signals (30 pps, 80 pps) maintained the temporal resolution of ICC neurons, whereas higher-frequency stimuli significantly improved temporal resolution of ICC neurons (i.e., higher Fmax and shorter response latencies) compared with neurons in control cats. Furthermore, Fmax and latencies to electrical stimuli were not correlated with the tonotopic gradient of the ICC, and changes in temporal resolution following chronic electrical stimulation occurred uniformly throughout the entire ICC. In all three experimental groups, increasing Fmax was correlated with shorter response latencies. The results indicate that the temporal features of the chronically applied electrical signals critically influence temporal processing of neurons in the cochleotopically organized ICC. We suggest that such plastic changes in temporal processing of central auditory neurons may contribute to the intersubject variability and gradual improvements in speech recognition performance observed in clinical studies of deaf children using cochlear implants.

Congenital and Prolonged Adult-Onset Deafness Cause Distinct Degradations in Neural ITD Coding with Bilateral Cochlear Implants

“…The exact pulse rate limit varies across neurons and is also affected by neonatal deafening and chronic stimulation (Snyder et al 1995;Vollmer et al 1999;Vollmer et al 2005), but there are no published data for long-term, adult-deafened cats. We compared the range of pulse rates over which neurons show pulse-locked responses in the three deafness models and looked for possible correlation with ITD coding.…”

Topography of Auditory Nerve Projections to the Cochlear Nucleus in Cats after Neonatal Deafness and Electrical Stimulation by a Cochlear Implant

“…Neural response thresholds were plotted as a function of depth along the cochleotopic gradient of the IC to obtain STC functions, as reported previously (Snyder et al 1990(Snyder et al , 1991Vollmer et al 1999;Leake et al 2000Leake et al , 2007Leake and Rebscher 2004). In the present study, extent of activation of the IC was measured at the maximum electrical signal intensities of the amplitude modulated pulse trains (or analogue signal in K154) used for the electrical stimulation delivered to each implant channel in that particular subject.…”

“…All animals received electrical stimulation with signals considered to be "temporally challenging" to the central auditory system (see Leake and Rebscher 2004;Vollmer et al 1999). Stimulation periods were 4 h/day, 5 days/week for at least 6 months, except in one subject (K163) that was studied earlier due to device failure (Table 1).…”

“…Respiratory rate, heart rate, and body temperature were monitored throughout all procedures, and body temperature was maintained using a warm water recirculating blanket. The electrophysiological recording methods have been described in detail in several previous publications (Snyder et al 1990Leake et al 2000;Leake and Rebscher 2004;Vollmer et al 1999Vollmer et al , 2005. Briefly, tungsten microelectrodes were used to record responses of multi-neuronal clusters and single neurons in several penetrations through the IC that were made along a standardized trajectory orthogonal to the tonotopic gradient of the IC.…”

“…At birth, the cat auditory system is so immature that it is essentially non-functional. Behavioral thresholds are extremely high (Foss and Flottorp 1974;Clements and Kelly 1978;Ehret and Romand 1981), and spontaneous activity cannot be recorded reliably in auditory nerve fibers until several days postnatal (Romand 1984;Walsh and McGee 1986;Jones et al 2007). Auditory nerve fibers thresholds remain high, tuning is broad, and spontaneous discharge rates are very low (mean G10 spikes/s) until at least P8 to P10 (Romand 1984;Dolan et al 1985;McGee 1986, 1990;Walsh and Romand 1992).…”