Rehabilitation plasticity: Influence of hearing aid fitting on frequency discrimination performance near the hearing-loss cut-off

Abstract

Several studies have already demonstrated that patients with steeply sloping hearing loss of cochlear origin exhibit an improvement in frequency discrimination performance at or around the cut-off frequency. This enhancement cannot be explained in terms of peripheral mechanisms and should rather be interpreted in terms of central reorganization: i.e., injury-induced cortical plasticity. However, the reversibility and time course of such reorganization has not yet been described. The main goal of the present study was therefore to investigate the occurrence of rehabilitation plasticity associated with hearing-aid fitting in human subjects. Nine subjects with steeply sloping hearing loss and who were candidates for auditory rehabilitation were tested. Discrimination-limen-for-frequency (DLF) enhancement was investigated at the frequency with the best DLF (bDLF) for each individual subject before and during auditory rehabilitation (at 1 month, 3 months and 6 months). From 1 month on, frequency discrimination performance decreased significantly at the bDLF frequency, while remaining stable at other frequencies. This normalization may reflect a new central reorganization reversing the initial injury-induced changes in the cortical map. A correlation between subject’s age and alteration in DLF at 1 month was also found, suggesting that plasticity operates faster in younger patients.

Introduction

Changes in primary cortex functional organization with sensory deprivation are beginning to be extensively analysed in each sensory modality. In the somatosensory modality, animal models have provided some well-described examples of such plasticity: following amputation, primary sensory cortex areas initially responding to the deafferented body become responsive to input from adjacent body parts. (Kelahan et al., 1981, Merzenich et al., 1983, Pons et al., 1991). Similar results have been observed recently in human amputees, with the region previously encoding the amputated segment beginning to encode neighbouring muscles (Roricht et al., 1999).

The reversibility of this reorganization has also been studied – in monkeys, with neuronal changes following a nerve crush reversed after regeneration (Wall et al., 1983), and in one human subject who received a double hand graft (Giraux et al., 2001). The latter study, performed with MRI measurements, revealed that a only few months were necessary to reverse the prior amputation-induced reorganization.

Cortical reorganization following auditory deprivation has also been a matter of research, leading to the conclusion that plasticity can also be observed in this modality. Several authors have studied the effect of a mechanically generated cochlear lesion resulting in severe high-frequency hearing loss, in various animal species (guinea pigs: Robertson and Irvine, 1989; cats: Rajan et al., 1993; macaques: Schwaber et al., 1993). Electrophysiological recordings showed that the primary auditory cortex reorganized so that cortical regions previously encoding high-frequency tones subsequently encoded frequencies at the edge of the hearing loss; this presumably results in an enlarged representation of these unimpaired frequencies. A similar reorganization was also observed in animals with natural progressive loss of high-frequency hearing. Willott et al. (1993) observed enlarged cortical representation of middle frequencies in aged C57 mice (a breed which suffers high-frequency hearing loss at of the age of 3 months).

Several pieces of evidence have also been given in humans for reorganization of the cortex in case of auditory deprivation. Some studies of unilaterally deaf adults have used imaging methods to observe bilateral activation of the auditory cortices under monaural stimulation, whereas in normal-hearing subjects only a strong contralateral activation of auditory cortex is recordable (Bilecen et al., 2000, Fujiki et al., 1998, Ponton et al., 2001, Scheffler et al., 1998). Another branch of studies has focused on plasticity caused by high-frequency cochlear hearing-loss. As this plasticity certainly occurs in a wide range of animal species, it can reasonably be expected to be observed in humans. Thus, Dietrich et al. (2001) noted an increase in the amplitude of the N1m wave (a prominent wave, reflecting auditory cortex response and peaking approximately 100 ms after stimulus onset) at the hearing-loss cut-off frequency. Another way of studying neuronal change in humans is based on the assumption that cortical reorganization should involve some difference in perceptual performance in hearing-impaired subjects. Despite the wide range of tasks used, Buss et al. (1998) failed to find any significant effect at the hearing-loss cut-off frequency. Nevertheless, perceptual changes in frequency discrimination have been observed at the lesion-edge frequency (McDermott et al., 1998) of a steep hearing loss, the slope of the loss being a determining factor in the cortical reorganization (Thai-Van et al., 2002). Although these results are not direct proof of cortical plasticity, no peripheral phenomenon, such as loudness cues or spontaneous otoacoustic emissions, has been found to explain them (Thai-Van et al., 2003).

In the auditory modality, the reversal of such deprivation-induced plasticity, a phenomenon that may be termed rehabilitation plasticity, has yet to be investigated – although the situation is readily available for study in humans in the form of auditory amplification due to hearing aid (HA) fitting. The perceptual recovery provided by the HA may induce neuronal changes in the auditory cortex. Since the work of Gatehouse (1989), HA effects on the perceptual capacity of hearing-impaired subjects have been clearly demonstrated (e.g., Robinson and Gatehouse, 1995, Olsen, 1999, Philibert et al., 2002), suggesting a form of functional plasticity. Further light, however, needs to be thrown on the possible functional rearrangement induced by HA use.

Consequently, one of the goals of the present study was to investigate further the perceptual changes in frequency discrimination induced by auditory deprivation followed by rehabilitation. The time course of the changes was also studied. We made the hypothesis that the local frequency discrimination enhancement observed around the lesion-edge frequency of patients with steeply sloping hearing losses may be renormalized with respect to other frequencies in the same patients undergoing auditory rehabilitation, indicating rehabilitation plasticity in the auditory pathway.