Brain Advance Access originally published online on July 7, 2003
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Brain, Vol. 126, No. 10, 2235-2245,
October 2003
© 2003 Guarantors of Brain
doi: 10.1093/brain/awg228
Enhanced frequency discrimination near the hearing loss cut-off: a consequence of central auditory plasticity induced by cochlear damage?
1 Unité CNRS UMR 5020 Laboratoire ‘Neurosciences et Systèmes Sensoriels’, CNRS GDR 2213 ‘Prothèses auditives’, Université Claude Bernard Lyon I, Lyon, 2 Service d’Audiologie et d’Explorations Orofaciales, Hôpital Edouard Herriot, Lyon, France and 3 Department of Experimental Psychology, University of Cambridge, Cambridge, UK
Correspondence to: Dr Hung Thai-Van, Service d’Audiologie et d’Explorations Orofaciales, Pavillon U, CHU Edouard Herriot, Place d’Arsonval, 69437 Lyon Cedex 03, France E-mail: hung.thaivan{at}chu-lyon.fr
Received November 8, 2002. Revised April 29, 2003. Accepted May 1, 2003.
 |
Summary |
|---|
 Top Summary Special noteIntroductionMethodsResultsDiscussionReferences |
|---|
Patients with steeply sloping hearing losses of cochlear origin may exhibit enhanced difference limens for frequency (DLFs) near the cut-off frequency (Fc) of their hearing loss. This effect has been related to observations in deafened animals of an over-representation of Fc in the primary auditory cortex. However, alternative interpretations in terms of peripheral mechanisms have not been eliminated. In the present study, we assessed the possible role of two peripheral mechanisms [loudness cues and spontaneous otoacoustic emissions (SOAEs)] in a group of patients with high-frequency hearing loss. We tested first whether the DLF enhancement effect was still observed under conditions where subjects could not rely on loudness cues to perform the frequency discrimination task. To achieve this, we adjusted the nominal level of each stimulus so that it fell on an equal loudness contour measured at very fine (1/8 octave) frequency intervals, and we roved the level of each stimulus over a large range (12 dB). Under these conditions, the DLF enhancement was still observed in all patients; this demonstrates that the effect cannot be explained simply by loudness cues. We then screened the patients for SOAEs to test whether the DLF enhancement effect could be explained by the presence of such emissions in the vicinity of the Fc. None of the patients exhibited SOAEs. Finally, we tested whether the patients had cochlear dead regions, i.e. regions lacking functional inner hair cells and/or auditory nerve fibres. Using a refined version of a non-invasive clinical test for the identification of dead regions, we assessed the presence of such regions in fine frequency steps (1/4 octave) up to very high frequencies. All of the patients had cochlear dead regions. The first two findings support the hypothesis that DLF enhancement is due to injury-induced central reorganization in the auditory system. The last one is consistent with neurophysiological data in animals, which suggest that complete deprivation from auditory input at certain cochlear sites may be a necessary condition for the occurrence of injury-induced cortical reorganization.
Keywords: frequency discrimination; loudness cues; spontaneous otoacoustic emissions; cochlear dead region; neural plasticity
Abbreviations: DLF= frequency limen difference; ELC = equal loudness contour; ERB = equivalent rectangular bandwidth; Fc = cut-off frequency; HL = hearing loss; SOAE = spontaneous otoacoustic emission; SPL = sound pressure level; TEN = threshold-equalizing noise; TOAE = transiently evoked otoacoustic emission
|
Special note |
|---|
|
TopSummarySpecial noteIntroductionMethodsResultsDiscussionReferences |
|---|
In the context of this article, the expression dB ‘HL’ refers to stimulus levels expressed relative to hearing thresholds measured in a population of 20 young subjects who had beforehand been found to have normal hearing (i.e. hearing thresholds were between –10 and 10 dB ‘HL’) using standard (Telephonics TDH 49) headphones and a standard (InterAcoustics AC30) audiometer. These reference hearing thresholds were measured using exactly the same testing material and headphones as used with the subjects of the experiments. Test frequencies ranged between 125 and 8000 Hz in 1/2 octave intervals; the reference values for intermediate frequencies were derived using linear interpolation.
|
Introduction |
|---|
|
TopSummarySpecial noteIntroductionMethodsResultsDiscussionReferences |
|---|
A crucial feature of sensory systems is that receptor surfaces are represented topographically (‘mapped’) in the CNS. Over the last two decades, increasing numbers of experimental studies have demonstrated that the organization of these sensory maps is not fixed after development, but retains a large degree of plasticity, even in adulthood. Dramatic alterations in sensory maps at the cortical and subcortical levels have been observed following peripheral lesions that affected restricted portions of sensory receptor surfaces: rather than becoming silent, neurons deprived of peripheral input become responsive to stimuli applied to peri-lesion regions of the receptor surface, to which they formerly did not respond. A striking illustration of this phenomenon is provided by results of Jones and Pons (1998
) showing that, after upper limb amputation in monkeys, neurons in the somatosensory cortex that initially responded specifically to the severed limb were activated by stimuli applied to the face. Since the face is represented next to the upper arm in the somatosensory cortex, this observation can be explained by re-routing of neural inputs between neighbouring cortical regions; it can also be described, metaphorically, as the ‘invasion’ of one cortical territory by another. Analogous neural reorganization phenomena have been observed in the primary visual cortex following focal retinal lesions: units deprived of peripheral input start responding to stimulation of neighbouring retinal sites (Kaas et al., 1990; Kaas, 1991; Gilbert and Wiesel, 1992). Similarly, in the auditory modality, cochlear lesions affecting a restricted portion of the cochlea have been shown to affect dramatically the tonotopic functional organization of the primary auditory cortex: in general, auditory neurons that are deprived of direct cochlear inputs due to the lesion all become responsive to cochlear sites at which significant input is still present (Robertson and Irvine, 1989; Rajan et al., 1993; Schwaber et al., 1993; Irvine and Rajan, 1995).
An important question relates to the perceptual consequences, if any, of injury-related neural plasticity. Since neural sensory maps are assumed to play an important role in the processing of sensory information, changes in these maps should induce changes at the perceptual level. One possible effect is a distortion, leading to illusory sensations or perceptions. This can be understood by considering that, whilst neurons in primary sensory cortices adapt to peripheral lesions by deriving their inputs from adjacent regions of the receptor surface, these neurons may continue to represent the original peripheral region for other parts of the cortex. In other words, neurons located in non-primary cortical areas, to which the reorganized primary sensory cortex neurons send information, may not be ‘aware’ that the information which they receive is in fact derived from a peripheral region different from the case before the lesion. Therefore, stimuli applied to intact parts of the receptor surface may be mistakenly attributed to stimulation of the lesioned region. Clinical data in human amputees spectacularly support this hypothesis. It has indeed been known for more than a century that amputees often experience vivid sensations that originate, apparently, in their severed limb (Ramachandran et al., 1992; Ramachandran, 1993; Flor et al., 1995; Knecht et al., 1996, 1998). These sensations are known as ‘phantom limb’ sensations. Furthermore, it has been shown that stimulation of the amputation stump, or even the face, can elicit sensations that are perceptually referred to the amputated limb (Ramachandran, 1992). These perceptual phenomena can be explained in the light of results like those of Jones and Pons (1998), which indicate that, after amputation of the upper limb, neurons in the primary somatosensory cortex that formerly responded specifically to this limb start to respond to stimuli applied to the face. Similarly, in the visual modality, neural plasticity induced by restricted retinal lesions might explain the perceptual filling-in of visual scotomas (Gilbert, 1998). In the auditory modality, analogous injury-induced reorganization might sometimes be responsible for the occurrence of phantom auditory sensations, known as tinnitus (Norena et al., 2002).
Besides illusory or distorted sensations, another possible perceptual consequence of the injury-induced reorganization of sensory maps relates to the fact that this reorganization results in the over-representation of certain portions of the receptor surface. This fact has been strikingly demonstrated in the primary auditory cortex, where, following mechanical lesions of the basal turn of the cochlea, most of the neurons deprived of their usual peripheral inputs had best frequencies corresponding to the hearing loss (HL) cut-off or ‘edge’ frequency. As a result, the HL cut-off frequency (Fc) was over-represented at the cortical level; in some cases, half or more of the whole surface of the primary auditory cortex was occupied by neurons having a best frequency corresponding to this frequency.
The results of electrophysiological and behavioural studies conducted by Recanzone et al. (1992a, b, c, 1993) in monkeys indicate that the ability to discriminate stimuli exciting a restricted portion of a sensory receptor surface is related to the size of the primary cortical area devoted to the representation of that portion. For instance, Recanzone et al. (1993) found that thresholds for the discrimination of two successive sounds differing slightly in frequency were correlated to the size of the area devoted to the representation of these frequencies in the primary auditory cortex. They showed that animals who had repeatedly practised the frequency discrimination task around a specific nominal frequency exhibited an enlarged cortical representation of the trained frequency region, as compared with that of untrained frequencies. Although the learning-induced plasticity found by Recanzone et al. and the above-described injury-induced plasticity phenomena may involve different neurophysiological mechanisms (Irvine and Rajan, 1995), the observation that both forms of auditory plasticity result in an over-representation of a narrow frequency range at the cortical level suggests the possibility that cochlear lesions may, paradoxically, result in enhanced frequency discrimination performance near the HL Fc.
Three previous studies have examined, in detail, whether discrimination abilities were enhanced near the HL edge in patients with HL of cochlear origin (Buss et al., 1998; McDermott et al., 1998; Thai-Van et al., 2002). In the latter two studies, difference limens for frequency (DLFs) were found to be significantly enhanced at or near the HL Fc in patients with steeply sloping, high-frequency HL. Although this finding is consistent with an interpretation in terms of injury-induced plasticity, it can be explained more parsimoniously in terms of peripheral mechanisms. For instance, the finding of enhanced DLFs in patients with steeply sloping loss, but not in patients with more gradual loss, might be explained by the fact that, in the former, a given increase in stimulus frequency above the HL cut-off produced a larger difference in loudness than in the latter. The authors of the cited studies took certain methodological precautions to control for this. In particular, they measured equal loudness contours (ELCs) in each of their subjects prior to the frequency discrimination task and adjusted the nominal level of the tones used in this task, so that their average loudness would remain approximately constant. Furthermore, they randomized the actual levels of the tones over a certain range around their adjusted nominal level. These two precautions were intended to prevent subjects from relying on loudness cues in the frequency discrimination task. However, as acknowledged by the authors themselves, the relative coarseness of the ELC measures (which were performed in 1/2 octave steps), and the relatively small level randomization range (±3 dB) prevented them from confidently ruling out loudness cues. Consequently, no conclusive evidence could be provided against the hypothesis that the DLF enhancement near the HL edge is due to the use of loudness cues.
Another possible peripheral mechanism for local improvements in DLFs around the HL cut-off involves spontaneous otoacoustic emissions (SOAEs). SOAEs, which are generated inside the cochlea (Kemp, 1978), may interact with external tones of neighbouring frequencies and provide additional cues for frequency discrimination. Recent experimental results indicate that, in normal-hearing subjects, DLFs can be locally enhanced in the vicinity of SOAEs (Norena et al., 2002). Although SOAEs presumably originate in the spontaneous activity of the cochlear outer hair cells (OHCs), which are in general adversely affected by cochlear damage (Moulin et al., 1991), they may be generated in regions of the cochlea where functional OHCs are bordered by lesioned OHCs (Powers et al., 1995).
The aim of the present study was to test further for the possible role of the two types of auditory mechanisms of peripheral origin described above (i.e. loudness cues and SOAEs) in the local enhancement of DLFs observed near the audiogram edge in patients with steeply sloping HL of cochlear origin. First, more stringent methodological constraints were employed in this study than in previous studies, to ensure that the patients would not rely on loudness cues in the frequency discrimination task; specifically, ELCs were measured using much finer frequency steps (1/8 octave) than in previous studies (1/2 octave), and stimulus level was randomized over a larger range (±6 dB, instead of ±3 dB). We reasoned that, if enhanced DLFs were still observed near the HL cut-off with such stringent methodological constraints, we could safely conclude that the effect is not explained by loudness cues. Secondly, the patients were screened for SOAEs. Finally, we also assessed the presence of cochlear dead regions in all the patients. Cochlear dead regions are defined as regions of the cochlea where there are no functioning inner hair cells (IHCs) and/or primary afferent auditory nerve fibres, so that no information can be transmitted to higher auditory structures. Cochlear dead regions cannot be identified reliably on the basis of audiometric thresholds, but can be assessed non-invasively in human patients using a specific perceptual test devised by Moore et al. (2000): the threshold-equalizing noise (TEN) test. The rationale for applying this test to the patients of the present study is that the presence of such dead regions is, according to the results of certain neurophysiological studies (Rajan and Irvine, 1998), a necessary condition for the occurrence of injury-induced plasticity in the central auditory system. Previous studies of the enhancement of DLFs near the HL edge have not used any test to confirm the presence of dead regions.
|
Methods |
|---|
|
TopSummarySpecial noteIntroductionMethodsResultsDiscussionReferences |
|---|
Subjects
We studied five patients with steeply sloping, high-frequency HLs of cochlear origin. All patients gave written consent, in accordance with the Declaration of Helsinki. The study was approved by the local ethics committee (Hospices Civils de Lyon, France). The patients’ ages and audiological characteristics (aetiology of deafness, HL Fc and HL slope in the test ear) are summarized in Table 1. Following Thai-Van et al. (2002
), subjects were tested in the ear in which the HL slope was steeper, even if only slightly. Also, the HL Fc was estimated for each patient as the highest test frequency above the audiogram edge (identified by visual inspection) at which the measured absolute threshold was within 5 dB of the best absolute threshold. Fc varied between 595 and 2181 Hz across patients. The HL slope, measured as the difference in absolute threshold at Fc and one octave above Fc, varied between 32 and 68 dB/octave.
|
Psychophysical procedures
Subjects were tested individually in a double-walled sound-attenuating booth. All stimuli were delivered monaurally via Sennheiser HD 545 headphones and consisted of pulsed pure tones with a 20 ms rise/fall time and a 350 ms plateau. Customized software, running on an IBM-compatible computer, was used to control the stimuli and to collect each subject’s responses. We used a Turtle Beach Systems Pro Series Digital Audio sound card (version 1.0.10), with a sampling rate of 44.1 kHz. Subjects were tested during three sessions with an overall duration of
12 h, including rest periods. The three sessions took place within the same week.
Absolute hearing threshold measurement
The first phase of the experiment involved measurement of absolute hearing thresholds. The stimulus frequencies ranged from 250 to 8000 Hz in 1/2 octave steps. Frequency steps were reduced to 1/8 octave near the beginning of the audiogram slope, so that the Fc could be estimated more precisely. At least 13 frequencies, spaced at intervals of 1/8 octave, were tested in the vicinity of the Fc, the lowest being set 5/8 or 1/2 octave below the Fc and the highest 7/8 or one octave above. Absolute thresholds were measured using a one-interval, ‘yes/no’ procedure in which the subject’s task was to indicate whether he/she had perceived a tone. Threshold estimates obtained using this quick ‘yes/no’ procedure, which also forms the basis of routine audiometric tests, are affected by the subject’s decision criterion. However, we reasoned that the criterion would be consistent across frequencies within a given subject, and would not have any major effect on the form of the absolute threshold curve. Following a one-down one-up adaptive tracking rule, the stimulus level, initially set at 50 dB ‘HL’, was decreased after a ‘yes’ response and increased after a ‘no’ response. With this rule, thresholds correspond to the 50% correct response point on the psychometric function (Levitt, 1971). The level was varied in 6 dB steps until the fourth reversal in level variation, and in 2 dB steps thereafter. The procedure stopped after a total of eight reversals. The absolute threshold was computed as the arithmetic mean of the levels at the last four reversals. Two threshold estimates were obtained for each frequency; the absolute thresholds shown in the Results correspond to the average of these two estimates. The various frequencies were tested in random order. It took 1.5 h to measure the absolute thresholds for 20 different frequencies in each subject.
ELC measurement
The second phase of the experiment involved measurement of the ELC. The ELC was measured using as a reference a 500 Hz tone 30 dB above the hearing threshold of the subject (30 dB sensory level, SL), i.e. at a comfortable level. Each subject had to determine the level of various comparison tones which created the same loudness sensation as did the reference tone. Comparison tones were distributed between 500 and 8000 Hz. In order to take into account the rapid changes in loudness with frequency that may occur, comparison tones were spaced at intervals of 1/8 octave in the vicinity of the Fc. Loudness matches were performed using an adaptive two-interval, two-alternative procedure with a two-down two-up tracking rule. On each trial, two successive observation intervals were presented, separated by a 300 ms silent gap. One interval contained a 500 Hz reference tone with a fixed 30 dB SL level, and the other contained a comparison tone of variable level. The two tones were presented in random order, with an equal probability of either one coming first. The subject was asked to indicate in which interval the tone was louder. The level of the comparison tone, which initially was set at random 10 dB below or 10 dB above that of the reference tone, was decreased when it was judged louder than the reference on two consecutive trials, and increased when it was judged less loud on two consecutive trials. Five dB steps were used until the second level reversal, and 1 dB steps thereafter. The arithmetic mean of the levels at the last four reversals was computed. The order of testing was determined by random selection from among the set of frequencies spaced 1/8 octave apart in the audiogram. For each tested frequency, the result was the average of two runs. The overall ELC measurement took 3.5 h to complete per subject.
Frequency discrimination procedure
Finally, DLFs for pure tones were measured. All frequencies for which absolute threshold and equal loudness values had been determined previously were tested. Methodological precautions were taken to prevent subjects basing their judgements in the DLF task on frequency-related changes in loudness rather than on changes in pitch. First, stimuli were delivered at a constant loudness level independently of frequency, using each subject’s previously obtained ELC. Levels for frequencies between those tested in the loudness matching procedure were calculated by linear interpolation. Secondly, to prevent subjects from exploiting any residual loudness differences as the frequency changed in the DLF procedure, the level of each and every stimulus was varied by a random value selected from a uniform distribution ranging between –6 and +6 dB. Each subject performed pre-test DLF training with a small number of runs, with feedback provided at the end of each trial in the form of a green light coming on after each correct response and a red light after each incorrect response; responses were not collected from these training runs. The DLFs were measured using a three-interval, two-alternative forced-choice procedure with a two-down one-up decision rule. On each trial, two of three successive observation intervals contained pure tones at a reference frequency; the remaining interval, which had a 50% chance of coming second and a 50% chance of coming third, contained a pure tone of variable frequency which was always higher than the reference. The intervals were separated by 300 ms silent gaps. The subject’s task was to identify the interval that contained the higher tone. The difference between the reference and the variable frequencies was initially set to 20% of the reference. After two consecutive correct responses, the difference in frequency was decreased; it was increased after each incorrect response. Ten reversals were obtained in each run. The frequency difference was varied by a factor of 2 until the fourth reversal occurred and by a factor of 1.41 thereafter. After each run, the geometric mean frequency at the last six reversals was computed. The order of testing was determined by random selection from among the set of frequencies spaced 1/8 octave apart, for which the absolute hearing threshold and the ELC had been measured previously. Three runs were collected at each of these test frequencies. The overall mean was taken as the geometric mean of these three. The overall DLF task lasted 4 h per subject.
Cochlear dead regions
Cochlear dead regions were assessed using the TEN test devised by Moore et al. (2000). This requires the measurement of detection thresholds for pure tones in quiet and in the presence of a TEN masker designed, as indicated by its name, so as to produce constant masked thresholds across frequency in normal-hearing listeners. The absolute and masked thresholds were measured from 250 to 11 314 Hz, in 1/4 octave intervals. If the absolute threshold at the test frequency was <50 dB sound pressure level (SPL), the level of the noise was set to 50 dB SPL/ERB, where ERB stands for the equivalent rectangular bandwidth of the auditory filter. If the threshold was larger, the noise level was increased to 60, 70 or 80 dB SPL/ERB, so that the noise was always audible, unless the absolute threshold was >80 dB SPL, in which case the TEN test was no longer applicable, and the result inconclusive. Following Moore et al. (2000), frequencies at which the masked threshold was at least 10 dB above both the absolute threshold and the TEN level per ERB were taken as corresponding to dead regions.
Otoacoustic emission recordings
Otoacoustic emissions were recorded in a soundproof room using the Otodynamics ILO88 system. The probe, comprising a transmitter and a microphone, was fitted to the external auditory meatus with a foam rubber tip. Long latency transiently evoked otoacoustic emissions (TOAEs) were elicited by 80 µs clicks of 57 ± 3 dB SPLpe (peak equivalent SPL). Stimulus artefact was eliminated by excluding the first 2.5 ms of the response. The click rate was 12.5 Hz, and the post-stimulus analysis time was 80 ms, divided into four equal bins. Averaging was over 200 responses, with a 500–6000 Hz pass-band. The response spectrum was analysed with a 50 Hz resolution. Each ear was tested twice in order to demonstrate reproducibility of any given peak identified in the measured spectra.
The SOAEs were assessed using the SOAE search facility of the ILO88 software. The procedure took advantage of the possibility of recording long-latency TOAEs synchronized to the stimulus. SOAEs were defined as present when synchronized TOAEs were present >60 ms after the click stimulus, and were at least 3 dB above the noise floor. The equivalence between long-latency TOAEs and SOAEs has been shown previously (Wable and Collet, 1994). Further details about SOAE recording and processing methods may be found in Moulin (2000a, b).
|
Results |
|---|
|
TopSummarySpecial noteIntroductionMethodsResultsDiscussionReferences |
|---|
Figure 1 shows the absolute thresholds (filled squares), ELCs (open squares) and DLFs (filled circles) for each patient. In all five, DLFs were found to reach a minimum at or near (i.e. no more than 1/4 octave away from) the Fc. In some of the patients, in addition to the absolute minimum in DLFs at or around the Fc, local minima in the DLF curves were observed above the Fc. Such minima were observed at Fc + 3/8 and Fc + 5/8 octave for patient J.M.O., at Fc + 3/4 octave for patient M.F.E. and at Fc + 1/2 octave for patient L.P.A. One-way ANOVA (analysis of variance) and Student–Newman–Keuls pairwise comparisons were used to test for the significance of local DLF improvements. Statistically significant differences are summarized in Table 2. In all patients, a significant local improvement in DLFs was observed at or near (–1/8 to +1/4 octave) the Fc. In three of the patients, a second local DLF improvement was found well above (+1/2, +3/4 or +5/8 octave) the Fc.
|
|
Table 3 summarizes the results of otoacoustic emission recordings. Reproducible TOAEs could be obtained in three out of the five patients. The TOAE spectra are shown in Fig. 2. It can be seen that most of the components in these spectra ranged from 500 to 3000 Hz. None of the subjects tested had SOAEs above the measurement-noise floor.
|
|
Figure 3 shows the results of the TEN test. Absolute thresholds are represented by open circles and masked thresholds by filled triangles. The asterisks show the level of the TEN used at each test frequency, specified as level per ERB. The hatched bars correspond to frequencies at which the masked threshold was at least 10 dB above the absolute threshold and above the level of the TEN; these are the two criteria used to define the presence of a dead region (Moore et al., 2000
). As can be seen, dead cochlear regions were identified in all patients. For three of the patients, the dead regions occupied frequency regions situated well above (i.e. at least one octave) the Fc. For the other two patients, dead regions were found fairly close to the Fc (i.e. 5/8 octave above it in patient L.P.A. and 1/2 octave above it in patient B.G.O.). For these two patients, DLFs were available for some of the frequencies corresponding to dead regions (as shown by the hatched areas in Fig. 3). It was found that, at frequencies corresponding to dead regions, DLFs were substantially elevated (values up to 8%) as compared with those measured at frequencies where no dead regions were present. This effect is noteworthy: in the three patients who had no dead region in the frequency range over which frequency discrimination performance was measured, DLFs remained lower than 2–3% at all the tested frequencies (even though the HL measured at some of those frequencies was comparable with that at which elevated DLFs were observed in the patients with dead regions close to the Fc).
|
|
Discussion |
|---|
|
TopSummarySpecial noteIntroductionMethodsResultsDiscussionReferences |
|---|
The results obtained, showing that DLFs are locally enhanced in the vicinity of the Fc in patients with sensorineural HL, are in general agreement with the findings of McDermott et al. (1998
) and the more recent results of Thai-Van et al. (2002). One important advantage of the present study over previous ones is that, owing to the use of finer frequency steps for the assessment of ELCs (i.e. 1/8 octave instead of 1/2 octave in earlier studies) and the larger range of level randomization for the measurement of DLFs (12 instead of 6 dB in earlier studies), it provides convincing evidence against an explanation of the effect in terms of loudness cues. The present results demonstrate that the DLF enhancement effect is robust and occurs when subjects cannot reliably exploit differences in loudness between the test tones in order to perform the discrimination task. Indeed, even assuming an HL slope of 70 dB/octave, which is larger than the largest slope measured in this study (68 dB/octave), the difference in absolute threshold between two tones separated by 1% (the largest best DLF measured in this study) was 1 dB, well below the 12 dB range of level roving used here. Therefore, it can safely be concluded that the enhanced DLFs measured near the Fc in the present study cannot be accounted for by differences in loudness between the test tones.
As mentioned in the Introduction, another possible aspect of cochlear functioning that might explain the enhanced DLFs near the Fc relates to the existence of SOAEs, which may interact (beat) with external tones, and provide additional cues for their discrimination. This hypothesis is made more plausible by recent results showing that DLFs can be significantly enhanced in the vicinity of SOAEs, at least in subjects with normal hearing (Norena et al., 2002). The present results, showing that none of the patients had SOAEs, indicate that the local enhancement in DLF observed in these subjects is not due to an interaction between external tones and SOAEs.
By ruling out both an interpretation in terms of both loudness cues and SOAEs, the present results do not support explanations of the DLF enhancement effect in terms of peripheral mechanisms. On the other hand, they are consistent with the hypothesis that the DLF enhancement effect is related to injury-induced neural plasticity in the central auditory system. Experimental studies in animals indicate that, for injury-induced central auditory plasticity to occur, there must be ‘a cochlear region in which damage is so comprehensive that there is no neural outflow from this region’ (Rajan and Irvine, 1998). The present results, which indicate that all the patients who took part in this study had cochlear dead regions, are consistent with the idea that in humans, as in animals, total deprivation of peripheral input may be a necessary condition for injury-induced central reorganization to occur. It is interesting to note that the dead regions were not necessarily close to the Fc and to the frequency at which DLFs were found to be enhanced: in some cases, as in patients P.D.U. and M.F.E., the dead regions were located several octaves above the Fc. This lack of a systematic relationship between the location of the dead regions and that at which DLFs were enhanced may, at first sight, appear as an argument against a linkage between the two phenomena. However, the results of some of the animal studies cited above indicate that, when the region of complete damage is adjacent to a region where damage is more gradual, the frequency that is over-represented at the central level is not one at which the damage is profound, but rather one at which absolute thresholds are only slightly elevated (Rajan and Irvine, 1998). This observation in animals is consistent with our observation in humans, of enhanced DLFs near the Fc, at frequencies for which absolute thresholds were only slightly elevated, even though dead regions were, in some cases, found only at much higher frequencies.
Another interesting aspect of the present results is that, for three patients, local minima in the DLFs were observed not only near the Fc, but also at frequencies where absolute thresholds changed rapidly. This observation suggests that, when there is more than one breakpoint in the audiogram, there can be more than one frequency that becomes over-represented centrally in the auditory system. This effect needs replication and further study before its significance can be assessed. It should be pointed out that there are some data in the neurophysiological literature to suggest that injury-induced reorganization can occur even in cases of progressive HL, where the elevation in thresholds at high frequencies remains limited (Willott et al., 1993). The results of Thai-Van et al. (2002) suggest that, in human subjects, relatively steep HLs are a necessary condition for the occurrence of significant enhancement of DLFs near the Fc.
It is important to point out that the present psychophysical results cannot be used to determine whether the local improvement in DLFs near the Fc is caused by long-term plastic changes induced by cochlear lesions, or by changes in cortical auditory function following almost immediately from cochlear lesions. One such quasi-instantaneous consequence of restricted cochlear lesions is the unmasking of latent inputs, from cochlear regions corresponding to the HL edge, to the cortical region now deprived of direct inputs. This unmasking of latent connections related to loss of surround inhibition may, just like the cortical plastic changes described above, result in a spatially expanded cortical representation of HL edge frequencies. The exact relationship, if any, between this unmasking phenomenon and injury-induced plastic changes remains unclear at present. While data in the literature suggest that removal of inhibition can lead to reorganization in the somatosensory or motor cortex (Calford and Tweedale, 1988; Jacobs and Donoghue, 1991), other data indicate that surround inhibition loss may occur without any plastic changes in the frequency map of the primary auditory cortex (Rajan, 1998). To be effective, an enlarged cortical representation of the lesion edge frequencies must be associated with normal threshold sensitivity as assessed by intracortical microelectrode mapping (Robertson and Irvine, 1989; Rajan et al., 1993). On the contrary, an increase in neural response thresholds at these frequencies would only reflect the residue of pre-existing inputs (Rajan and Irvine, 1998). Since no intracortical electrophysiological measurements were available in the present study, this last hypothesis cannot be definitely ruled out.
Finally, another important question that must be mentioned here is that of the functional consequences, if any, of the DLF enhancement effect for auditory perception in everyday life. For one thing, an improvement in DLFs as localized as that observed here is unlikely to have a significant beneficial influence, per se, on speech or music perception: the cues for speech recognition or musical tone identification are, in general, scattered across a large frequency range and very unlikely to coincide systematically with the HL edge. From this point of view, it appears that the psychophysical effect demonstrated here simply represents a side-effect of neurophysiological mechanisms that, at least in the auditory modality, have no major perceptual consequences.
In conclusion, the results obtained in this study indicate that the enhancement of DLFs observed near the audiogram edge frequency (Fc) in patients with HL cannot be explained by the use of loudness cues or by SOAEs interacting with the test tones for frequencies near the Fc. Overall, this rules out two of the main possible interpretations of the DLF enhancement effect in terms of peripheral mechanisms. On the other hand, the present results are consistent with an interpretation in terms of injury-induced reorganization of tonotopic maps in the central nervous auditory system, leading to an over-representation of Fc. The finding of cochlear dead regions in all five patients in this study, in all of whom DLFs were also found to be significantly enhanced near the Fc, is consistent with earlier data in animals indicating that complete removal of peripheral output from certain cochlear sites is necessary for the occurrence of injury-induced central auditory reorganization.
|
Acknowledgements |
|---|
The authors wish to thank Kamel Adjout and Jean-François Vesson (Laboratoire Voir and Entendre, Grande Pharmacie Lyonnaise, Lyon, France) for their help in testing cochlear dead regions. This work was supported by research grants from CNRS, CCA Groupe, Entendre, Oticon, Phonak and Siemens Audiologie.
|
References |
|---|
|
TopSummarySpecial noteIntroductionMethodsResultsDiscussionReferences |
|---|
Buss E, Hall JW 3rd, Grose JH, Hatch DR. Perceptual consequences of peripheral hearing loss: do edge effects exist for abrupt cochlear lesions? Hear Res 1998; 125: 98–108.[CrossRef][Web of Science][Medline]
Calford MB, Tweedale R. Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation. Nature 1988; 332: 446–8.[CrossRef][Medline]
Flor H, Elbert T, Knecht S, Wienbruch C, Pantev C, Birbaumer N, et al. Phantom limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 1995; 375: 482–4.[CrossRef][Medline]
Gilbert CD. Adult cortical dynamics. Physiol Rev 1998; 78: 467–85.
Gilbert CD, Wiesel TN. Receptive field dynamics in adult primary visual cortex. Nature 1992; 356: 150–2.[CrossRef][Medline]
Hughson W, Westlake H. Manual for program outline for rehabilitation of aural casualties both military and civilian. Trans Am Acad Ophthalmol Otolaryngol Suppl 1944; 48: 1–15.
Irvine DRF, Rajan R. Plasticity in the mature auditory system. In: Manley GA, Klump GM, Köppl C, Fastl C, Oeckinghaus H, editors. Advances in hearing research. Singapore: World Scientific; 1995. p. 3–23.
Jacobs KM, Donoghue JP. Reshaping the cortical motor map by unmasking latent intracortical connections. Science 1991; 251: 944–7.
Jones EG, Pons TP. Thalamic and brainstem contributions to large-scale plasticity of primate somatosensory cortex. Science 1998; 282: 1121–5.
Kaas JH. Plasticity of sensory and motor maps in adult mammals. Annu Rev Neurosci 1991; 14: 137–67.[CrossRef][Web of Science][Medline]
Kaas JH, Krubitzer LA, Chino YM, Langston AL, Polley EH, Blair N. Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 1990; 248: 229–31.
Kemp DT. Stimulated acoustic emissions from within the human auditory system. J Acoust Soc Am 1978; 64: 1386–91.[CrossRef][Web of Science][Medline]
Knecht S, Henningsen H, Elbert T, Flor H, Höhling C, Pantev C, et al. Reorganizational and perceptional changes after amputation. Brain 1996; 119: 1213–9.
Knecht S, Henningsen H, Höhling C, Elbert T, Flor H, Pantev C, et al. Plasticity of plasticity? Changes in the pattern of perceptual correlates of reorganization after amputation. Brain 1998; 121, 717–24.
Levitt H. Transformed up-down methods in psychoacoustics. J Acoust Soc Am 1971; 49 Suppl 2: 467–77.
McDermott HJ, Lech M, Kornblum MS, Irvine DRF. Loudness perception and frequency discrimination in subjects with steeply sloping hearing loss: possible correlates of neural plasticity. J Acoust Soc Am 1998; 104: 2314–25.[CrossRef][Web of Science][Medline]
Moore BCJ, Huss M, Vickers DA, Glasberg BR, Alcantara JI. A test for the diagnosis of dead regions in the cochlea. Br J Audiol 2000; 34: 205–24.[Web of Science][Medline]
Moulin A. Influence of primary frequencies ratio on distortion product otoacoustic emissions amplitude. I. Intersubject variability and consequences on the DPOAE-gram. J Acoust Soc Am 2000a; 107: 1460–70.[CrossRef][Web of Science][Medline]
Moulin A. Influence of primary frequencies ratio on distortion product otoacoustic emissions amplitude. II. Interrelations between multicomponent DPOAEs, tone-burst-evoked OAEs, and spontaneous OAEs. J Acoust Soc Am 2000b; 107: 1471–86.[CrossRef][Web of Science][Medline]
Moulin A, Collet L, Delli D, Morgon A. Spontaneous otoacoustic emissions and sensori-neural hearing loss. Acta Otolaryngol 1991; 111: 835–41.[Medline]
Norena A, Micheyl C, Durrant JD, Chery-Croze S, Collet L. Perceptual correlates of neural plasticity related to spontaneous otoacoustic emissions? Hear Res 2002; 171: 66–71.[CrossRef][Web of Science][Medline]
Powers NL, Salvi RJ, Wang J, Spongr V, Qiu CX. Elevation of auditory thresholds by spontaneous cochlear oscillations. Nature 1995; 375: 585–7.[CrossRef][Medline]
Rajan R. Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nat Neurosci 1998; 1: 138–43.[CrossRef][Web of Science][Medline]
Rajan R, Irvine DRF. Neuronal responses across cortical field A1 in plasticity induced by peripheral auditory organ damage. Audiol Neurootol 1998; 3: 123–44.[CrossRef][Medline]
Rajan R, Irvine DRF, Wise LZ, Heil P. Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex. J Comp Neurol 1993; 338: 17–49.[CrossRef][Web of Science][Medline]
Ramachandran VS. Behavioral and magnetoencephalographic correlates of plasticity in the adult human brain. [Review]. Proc Natl Acad Sci USA 1993; 90: 10413–20.
Ramachandran VS, Rogers-Ramachandran D, Stewart M. Perceptual correlates of massive cortical reorganization. Science 1992; 258: 1159–60.
Recanzone GH, Merzenich MM, Jenkins WM. Frequency discrimination training engaging a restricted skin surface results in an emergence of a cutaneous response zone in cortical area 3a. J Neurophysiol 1992a; 67: 1057–70.
Recanzone GH, Merzenich MM, Schreiner CE. Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. J Neurophysiol 1992b; 67: 1071–91.
Recanzone GH, Merzenich MM, Jenkins WM, Grajski KA, Dinse HR. Topographic reorganization of the hand representation in cortical area 3b of owl monkeys trained in a frequency-discrimination task. J Neurophysiol 1992c; 67: 1031–56.
Recanzone GH, Schreiner CE, Merzenich MM. Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci 1993; 13: 87–103.[Abstract]
Robertson D, Irvine DRF. Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J Comp Neurol 1989; 282: 456–71.[CrossRef][Web of Science][Medline]
Schwaber MK, Garraghty PE, Kaas JH. Neuroplasticity of the adult primate auditory cortex following cochlear hearing loss. Am J Otol 1993; 14: 252–8.[Web of Science][Medline]
Thai-Van H, Micheyl C, Norena A, Collet L. Local improvement in auditory frequency discrimination is associated with hearing-loss slope in subjects with cochlear damage. Brain 2002; 125: 524–37.
Wable J, Collet L. Can synchronized otoacoustic emissions really be attributed to SOAEs? Hear Res 1994; 80: 141–5.[CrossRef][Web of Science][Medline]
Willott JF, Aitkin LM, McFadden SL. Plasticity of auditory cortex associated with sensorineural hearing loss in adult C57BL/6J mice. J Comp Neurol 1993; 329: 402–11.[CrossRef][Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  B. C. J. Moore and S. N. Vinay Enhanced discrimination of low-frequency sounds for subjects with high-frequency dead regions Brain, February 1, 2009; 132(2): 524 - 536. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Weisz, C. Wienbruch, K. Dohrmann, and T. Elbert Neuromagnetic indicators of auditory cortical reorganization of tinnitus Brain, November 1, 2005; 128(11): 2722 - 2731. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||