Cortical responses to promontorial stimulation in postlingual deafness
Introduction
Promontory testing is a crude electrical stimulation of the cochlea that pre-surgically evaluates the function of the auditory nerve and the temporal processing ability of cochlear implant candidates. The Nucleus Promontory Stimulator unit allows for subjective assessment of gap detection and duration discrimination (temporal difference limen, TDL) abilities, tasks which require temporal processing (Eddins and Green, 1995). Correlations between the results of pre-operative electrical stimulation and post-operative performance vary in previous studies. Of the two tests, the TDL has been demonstrated to be of greater predictive value (Black et al., 1987, Waltzman et al., 1990, Blamey et al., 1992, van Dijk et al., 1999).
In normal hearing, speech processing predominantly, but not completely, is left lateralized (Binder et al., 1997, Gjedde, 1999, Springer et al., 1999). In contrast, non-speech processing is known to be more right lateralized when the stimulus is tonal (Binder et al., 2000, Zatorre et al., 2002), whereas non-speech, in the form of pseudo-words or time-reversed sentences, is more bilaterally processed (Binder et al., 2000, Wong et al., 2002). A consistent finding in cochlear implant users listening to speech is the more extensive right temporal activity, i.e., the presence of more bilateral activity than characteristic of language processing in normal hearing (Wong et al., 1999, Giraud et al., 2000, Giraud et al., 2001). The reason for this difference is not known.
Tones commonly are used to study temporal processing, as processing of speech signals is held to be more complex and to involve analysis of other properties of speech. Imaging of this processing has yielded discrepant interpretations, however, including claims of both right-lateralized (Griffiths et al., 1999, Rao et al., 2001) and left-lateralized (Robin et al., 1990, Zatorre and Belin, 2001) activities. Both posterior temporal lobes are active during the temporal analysis of sounds in general (Griffiths et al., 1998), but the right posterior temporal lobe specifically is involved in duration discrimination tasks involving both auditory and tactile stimuli (Pardo et al., 1991, Belin et al., 2002).
Temporal coding is sufficient for speech comprehension (Shannon et al., 1995, Moller, 1999). Perception of phonemes primarily depends on the relative timing of acoustic events within the range of temporal differences of the order of tens of milliseconds (Ladefoged, 2000). Also, in some early studies, cochlear implantees showed a correlation between temporal resolution and the perception of consonants (Cazals et al., 1991, Muchnik et al., 1994). Recent animal studies suggest that plastic changes in temporal processing of central auditory neurons contribute to the variability of the outcome and the gradual improvement in speech recognition after implantation (Vollmer et al., 1999). Thus, we reason that knowledge of the ability to process temporal information before cochlear implantation is important to the evaluation of the outcome.
In a previous study, we combined promontory electrical stimulation with functional brain imaging by PET in normally hearing subjects (Mortensen et al., 2005). The test was chosen to assess brain function of normally hearing individuals during exposure to non-verbal temporal information presented in a manner similar to the stimulation applied to cochlear implant users. In that study we demonstrated that a right-lateralized fronto-temporal network of active neurons provides the neuronal basis for duration discrimination, irrespective of the subjective nature of the sensation, be it auditory or somatosensory. This study, as well as an earlier study showing the same right posterior temporal region to be involved in phoneme discrimination (Pedersen et al., 2000), led us to conclude that this region could be a major neuronal substrate of phoneme identification, a task which requires analysis of subtle temporal differences. We further suggested that gap detection is of little value in the assessment of cortical integration and rather appears to engage neuronal competence at a subcortical level (Mortensen et al., 2005).
On the basis of these results, we formulated the hypothesis that activity in the posterior right middle temporal gyrus and the right prefrontal cortex distinguish postlingually deaf subjects with the ability to discriminate smaller duration differences between two successive stimuli (100 ms or less) from subjects who need larger differences (more than 100 ms) to make the same judgment. We used positron emission tomography of promontory stimulation to test the hypothesis in candidates of cochlear implantation. We also tested whether gap detection provided additional information about cortical processing of temporal information in postlingually deaf subjects.
Section snippets
Subjects
Fourteen postlingually deaf adult CI-candidates were included in successive order after recommendation for cochlear implantation. They were stimulated in the ear chosen for implantation. The subjects formed two groups on the basis of the results of pre-operative promontory electrical stimulation. One group of six subjects (five men, one woman, with mean age of 53.5 years) had excellent sound duration discrimination (temporal difference limen, TDL ⩽ 100 ms) while another group of eight subjects
Results
In all subjects, regardless of side of stimulation and performance in the temporal tasks, the subtraction of baseline from electrical bursts resulted in a bilateral increase of activity at coordinates placed lateral and posterior to the primary auditory cortex, as anatomically defined by Rivier and Clarke (1997) from the distribution of cytochrome c oxidase density (Table 2 and Fig. 1).
A previous study of normally hearing subjects undergoing promontorial stimulation during PET scanning (
Discussion
The present study used PET to map auditory function in postlingually deaf adults. PET measurements are of two kinds, those that map a state, baseline or activation, and those that map a change or increment, caused by a perturbation of almost any kind and showing only those areas in which a significant change in brain activity has occurred. The former commonly provides a measure of metabolism of glucose, determined over a period of 45 min with a labeled glucose analog (FDG), or of oxygen,
Conclusion
This study shows that duration discrimination in postlingually deaf subjects depends on activity in specific regions of the cerebral cortex that include the right posterior temporal lobe in association with the right prefrontal cortex. The study confirms previous results of normal hearing and may provide a cortical basis for why, in some previous studies, TDL was observed to be a predictor of postimplantation speech perception performance (Waltzman et al., 1990, van Dijk et al., 1999). The
Acknowledgments
Supported by The National Association of Hearing Impaired in Denmark, Desirée & Niels Ydes Foundation, and The Danish National Research Foundation’s Center of Functionally Integrative Neuroscience. The MR Center, Skejby Sygehus, generously provided some MR-images.
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