Elsevier

Hearing Research

Volume 315, September 2014, Pages 1-9
Hearing Research

Research paper
Effects of deafness and cochlear implant use on temporal response characteristics in cat primary auditory cortex

https://doi.org/10.1016/j.heares.2014.06.001Get rights and content

Highlights

  • Cortical temporal processing in neonatally profoundly deafened unstimulated cats was near-normal after 7–13 months.

  • High-rate intracochlear electrical stimulation had significant, but diverse, effects on temporal processing.

  • Temporal processing in cats receiving low-rate electrical stimulation did not differ from that in controls.

Abstract

We have previously shown that neonatal deafness of 7–13 months duration leads to loss of cochleotopy in the primary auditory cortex (AI) that can be reversed by cochlear implant use. Here we describe the effects of a similar duration of deafness and cochlear implant use on temporal processing. Specifically, we compared the temporal resolution of neurons in AI of young adult normal-hearing cats that were acutely deafened and implanted immediately prior to recording with that in three groups of neonatally deafened cats. One group of neonatally deafened cats received no chronic stimulation. The other two groups received up to 8 months of either low- or high-rate (50 or 500 pulses per second per electrode, respectively) stimulation from a clinical cochlear implant, initiated at 10 weeks of age. Deafness of 7–13 months duration had no effect on the duration of post-onset response suppression, latency, latency jitter, or the stimulus repetition rate at which units responded maximally (best repetition rate), but resulted in a statistically significant reduction in the ability of units to respond to every stimulus in a train (maximum following rate). None of the temporal response characteristics of the low-rate group differed from those in acutely deafened controls. In contrast, high-rate stimulation had diverse effects: it resulted in decreased suppression duration, longer latency and greater jitter relative to all other groups, and an increase in best repetition rate and cut-off rate relative to acutely deafened controls. The minimal effects of moderate-duration deafness on temporal processing in the present study are in contrast to its previously-reported pronounced effects on cochleotopy. Much longer periods of deafness have been reported to result in significant changes in temporal processing, in accord with the fact that duration of deafness is a major factor influencing outcome in human cochlear implantees.

Introduction

Cochlear implants are highly successful sensory prostheses, providing hearing and good levels of speech perception to more than 300,000 individuals with profound/severe sensorineural hearing loss. A congenital or neonatal hearing loss of this sort has effects on the morphology and function of neurons along the auditory pathway, which influence the effectiveness of a subsequently introduced cochlear implant (for reviews see Shepherd and Hardie, 2001, Fallon et al., 2014a). At the cortical level, a period of 7–13 months of deafness in neonatally deafened cats results in complete loss of cochleotopy in the primary auditory cortex (AI) (Fallon et al., 2009, Fallon et al., 2014b), though cochleotopy can be maintained (Fallon et al., 2009) or re-established (Fallon et al., 2014b) by 6–8 months of cochlear implant use.

The perception of speech and of other complex acoustic signals involves the processing of both spectral and temporal information (e.g. Rosen, 1992, Shannon et al., 1995, Moore, 2008), and temporal information plays a critically important role when spectral information is degraded, as is the case with a cochlear implant. These considerations have prompted a number of studies in animal models examining the way in which central auditory neurons process temporal information provided by intra-cochlear electrical stimulation (ICES), and of the effects of deafness and of experience with chronic ICES on temporal resolution in the auditory system. As elaborated below, the term “temporal resolution” is used here to refer to two aspects of processing of temporal information by the central auditory system. The first is the latency of the responses evoked by ICES and the variability of that latency (viz. latency “jitter”). The second is the precision with which trains of stimuli are represented in the neuronal discharge, which is quantified by measuring the stimulus repetition rate at which the maximum response is evoked and/or the highest rate at which the response can follow the stimulus (e.g. Eggermont, 1991, Eggermont, 1992).

Most studies of the effects of deafness and of chronic ICES on temporal resolution in the central auditory system have been carried out on neurons in the inferior colliculus (IC, e.g. Snyder et al., 1991, Snyder et al., 1995, Shepherd et al., 1999, Vollmer et al., 1999, Vollmer et al., 2005). The general findings are of degraded temporal processing with deafness that is reversed with chronic intracochlear electrical stimulation. At the cortical level, Vollmer and Beitel (2011) reported that very long periods of deafness in two neonatally deafened cats (38 and 78 months, respectively) resulted in degradation in temporal following capacity and spike-timing precision. Vollmer and Beitel (2011) also reported that passive chronic ICES combined with training to detect ICES (but not passive ICES alone) over a period of 4–8 months after many years of deafness partially restored temporal resolution.

The primary aim of the present study was to investigate whether deafness of moderate duration (less than 14 months), known to effect cochleotopy, results in degradation of temporal resolution, and whether any such effects are offset by cochlear implant use that provides chronic ICES related to the acoustic environment. A secondary aim was to determine whether the effects of chronic ICES depend on stimulus rate. Preliminary findings have been presented in abstract form (Fallon et al., 2007a, Fallon et al., 2007b).

Section snippets

Experimental subjects

Seventeen healthy cats with otoscopically normal tympanic membranes were used in the present study. Data on the cochleotopic organization of the AI obtained from some of these cats were presented in Fallon et al. (2009), and the basic methods were as described in that paper. Those methods will therefore be described only briefly here. All procedures were in accordance with Australian Code of Practice for the Care and Use of Animals for Scientific Purposes and with the Guidelines laid down by

Duration of deafness

As there is ongoing degeneration of spiral ganglion neurons following a profound hearing loss, it is important to ensure that all groups had a similar duration of deafness. The duration of deafness for the DU, HR-ES and LR-ES groups of animals is equivalent to their age at acute study (Table 1; mean ages 9.6, 8.0, and 10.2 months, respectively), and there was no significant difference in age between the groups (one-way ANOVA, F2,14 = 2.2, P = 0.16). However, given that duration of stimulation

Discussion

We have examined the effects of neonatal deafness and cochlear implant use on temporal resolution in the AI of young adult cats. The only effect of profound deafness of moderate (7–13 months) duration, known to result in a complete loss of cochleotopic organisation (Fallon et al., 2009, Fallon et al., 2014b), was a decrease in the ability to respond to every stimulus in a pulse train (MFR). Chronic low-rate (50 pps) stimulation from a cochlear implant resulted in an increase in MFR compared to

Conflict of interest

None of the authors have any known or potential.

Acknowledgments

We are grateful for funding support from the National Institutes of Health NIDCD (NO1-DC-3-1005 & HHS-N-263-2007-00053-C), the National Health and Medical Research Council of Australia, and the Victorian State Government through their Operational Infrastructure Support scheme.

We thank Rodney Millard, Anne Coco, Stephanie Epp, Lauren Donnelly and Alison Neil for technical assistance, Helen Feng and Jin Xu for electrode manufacture and implantation, Sue Pierce for veterinary advice and Elisa Borg

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