Does long-term unilateral deafness change auditory evoked potential asymmetries?

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Abstract

Objective

To investigate the long-term cortical changes in auditory evoked potential (AEP) asymmetries associated with profound unilateral deafness.

Methods

Electroencephalographic (EEG) recordings from 68 channels were used to measure auditory cortex responses to monaural stimulation from 7 unilaterally deaf patients and 7 audiogram-matched controls. Source localization of the AEP N100 response was carried out and regional source waveform amplitude and latency asymmetries were analysed for activity in the N100 latency range and for the middle latency response (MLR) range.

Results

Asymmetry indices (contralateral  ipsilateral)/(contralateral + ipsilateral) showed that matched control subjects, like normally hearing participants, produced activity in the N100 latency range that was more contralaterally dominant for left compared to right ear stimulation. Contrary to expectation, source waveforms and asymmetry indices in the MLR and N100 latency range were similar for unilaterally deaf patients, their matched controls and a group of normally hearing participants.

Conclusions

Regional source waveform analysis revealed no evidence of systematic cortical changes in hemispheric asymmetries associated with long-term unilateral deafness. It is possible that a reorganization of cortical asymmetries to a ‘normal’ pattern had taken place in the years between deafness and testing.

Significance

Electrophysiological measures of auditory hemispheric asymmetries do not suggest long-term cortical reorganisation as a result of profound unilateral deafness.

Introduction

The adult central auditory system is capable of changing in response to a profound hearing loss (Syka, 2002). Several studies have shown that experimentally induced unilateral deafness in adult animals alters the activity in the auditory pathway ipsilateral to the unaffected ear (Popelar et al., 1994, Moore et al., 1997). The findings from human studies, however, are far less consistent, possibly due to the variable nature of pathological as compared to experimentally induced hearing losses. Although interpretation of past research tends to conclude that unilateral deafness alters the normal pattern of cortical response asymmetries recorded to monaural stimulation, close examination of the studies reveals highly heterogeneous findings. The greatest contrast arises between functional magnetic resonance imaging (fMRI) studies, that consistently report altered response asymmetries as a result of unilateral deafness (Scheffler et al., 1998; Bilecen et al., 2000; Langers et al., 2005; Firszt et al., 2006), and magnetoencephalographic (MEG) studies that do not (Vasama et al., 1995, Vasama et al., 2001, Fujiki et al., 1998). Moreover, a recent study from our laboratory (Hine and Debener, 2007) revealed that the extent of auditory evoked potential asymmetries in normally hearing participants depends on the ear and hemisphere examined. With the aim of furthering and extending our knowledge on the long-term cortical changes associated with profound unilateral deafness to include middle latency AEPs, we applied the same EEG source analysis techniques to recordings taken while unilaterally deaf participants and their matched controls were presented with monaural sounds.

Late auditory evoked potentials (AEPs) such as the N100 are important clinical tools for the assessment of functional hearing loss (Hyde, 1997). Furthermore, the N100 and its MEG equivalent, the N100m, as well as fMRI have been used to investigate whether experience-related changes in auditory cortex function are reflected in altered hemispheric asymmetries. One AEP study (Ponton et al., 2001) and several fMRI studies (Scheffler et al., 1998; Bilecen et al., 2000; Langers et al., 2005; Firszt et al., 2006) have concluded that profound unilateral deafness tends to shift the cortical activation pattern to one that is more symmetric. In contrast, MEG studies (Vasama et al., 1995, Vasama et al., 2001, Fujiki et al., 1998) have failed to find any long-term effect of unilateral deafness acquired as adults on the normal pattern of larger N100m dipole moments in the contralateral compared to the ipsilateral hemisphere. Whether long-term unilateral deafness affects hemispheric asymmetries of the auditory evoked middle latency response (MLR) is unknown since, as far as the authors are aware, no previous research has examined this issue.

Across studies, the cause of the patients’ unilateral deafness may be a confounding factor. Whereas some studies recruited their patients with profound unilateral deafness simply according to their audiogram, irrespective of etiology (Fujiki et al., 1998; Scheffler et al., 1998; Ponton et al., 2001; Langers et al., 2005), a few required unilateral deafness to be the result of a common cause (Vasama et al., 1995, Vasama et al., 2001). In the present study, we adopted the latter approach in order to reduce inter-subject variability. Patients who have undergone translabyrinthine surgery to remove a unilateral acoustic neuroma offer a unique, and declining, opportunity to study the effects of abrupt, profound unilateral deafness on auditory processing. The translabyrinthine surgical approach results in complete destruction of the inner ear on the side of the tumour. While still used in selected cases, it is now one of a range of management options. The patients in the current study had all undergone the same surgical procedure under the care of one consultant surgeon. In addition, special attention was paid to match each patient to a control subject whose bilateral audiogram was the same as that of the patient’s intact ear, since it is known that the N100 is affected by loudness level (Beauducel et al., 2000).

As in our recent study using normally hearing participants (Hine and Debener, 2007), we employed regional source waveform analysis to measure the degree of hemispheric asymmetry produced in the N100 latency range in response to monaural stimulation. Irrespective of the side of deafness, we predicted reduced hemispheric asymmetry in unilaterally deaf patients compared to their matched controls. Since previous studies that have shown effects of long-term unilateral deafness on hemispheric asymmetry are inconsistent as to whether the side of deafness differentially affects the results (Scheffler et al., 1998; Ponton et al., 2001; Khosla et al., 2003; Langers et al., 2005), no specific prediction was made regarding this point. Similarly, since no previous research has examined the effect of long-term unilateral deafness on middle latency AEPs, no specific prediction was made with regard to MLR asymmetries.

Section snippets

Participants

Seven unilaterally deaf patients (3 women and 4 men, mean age 57 ± 7 years, 5 left deaf, 2 right deaf) who had undergone surgery to remove a unilateral acoustic neuroma (between the last 5 and 11 years) took part in the study after giving written informed consent. The translabyrinthine surgical procedure experienced by all patients results in the complete destruction of the inner ear on the side of the tumour. Paired to each patient, a control participant was found whose bilateral audiogram

AEP source localization

Single subject dipole source localization revealed a very good fit between the reference location in auditory cortex (Talairach coordinates [x, y, z] = ± 49.5, −17, 9) and the modelled location. This is illustrated in Fig. 1, showing the single subject localizations in two-dimensional views and in a three-dimensional view plotted on a standardized brain. As can be seen, source locations for patients and their matched controls largely overlapped. For control subjects, the mean location was at [x, y, z] =

Effect of long-term unilateral deafness on late AEP source waveform asymmetries

The results for the matched controls in this study confirmed our previous findings in normally hearing participants (Hine and Debener, 2007) that activity in the N100 latency range is more contralaterally dominant for left compared to right ear stimulation. This finding has recently been corroborated in a MEG study as well (Yu et al., 2007). Contrary to our prediction, however, was the finding that unilaterally deaf patients showed no sign of abnormal response activity. In agreement with the

Acknowledgement

We thank Angela Barks for assistance with recording the data.

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