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Journal of Medical and Biological Engineering, 30(4): 215-219 215 Activation of the Auditory Cortex in Subjects with Unilateral Sensorineural Hearing Impairment in Response to Hearing Their Own Names Jen-Fang Yu 1,2 Chin-Kuo Chen 2,3 Sheng-Ru Wang 1,2 Che-Ming Wu 3 Shu-hang Ng 4,5,6 Leslie Ying 7 Ying-Zu Huang 8 Jiun-Jie Wang 4,5,* 1 Graduate Institute of Medical Mechatronics, Chang Gung University, Tao-Yuan 333, Taiwan, ROC 2 Taiouan Interdisciplinary Otolaryngology Laboratory, Chang Gung University, Tao-Yuan 333, Taiwan, ROC 3 Department of Otolaryngology, Chang Gung Memorial Hospital, Taipei 105, Taiwan, ROC 4 Department of Diagnostic Radiology, Chang Gung Memorial Hospital, Taipei 105, Taiwan, ROC 5 Department of Medical Imaging and Radiological Sciences, Chang Gung University, Tao-Yuan 333, Taiwan, ROC 6 Molecular Imaging Center, Chang Gung Memorial Hospital, Taipei 105, Taiwan, ROC 7 Department of Electrical Engineering and Computer Science, University of Wisconsin, Milwaukee, WI 53706, USA 8 Department of Neurology, Chang Gung Memorial Hospital, Taipei 105, Taiwan, ROC Received 20 Jan 2010; Accepted 18 Jun 2010 Abstract This study investigated the differences in activation of the auditory cortex between subjects with right and left unilateral sensorineural hearing loss (SNHL) when hearing their own names spoken by an unknown voice. All experiments were performed in the Chang Gung Memorial Hospital. Magnetic resonance imaging was acquired using a 3-Tesla Siemens scanner. Ten subjects with unilateral SNHL were recruited (3 male and 7 female, aged 30 ± 14.9 years, with 14 ± 6.29 hearing-impaired years). The activation pattern in the contralateral auditory cortex was wider than in the ipsilateral auditory cortex for all unilateral SNHL subjects. The auditory cortex of subjects with left SNHL hearing their own names spoken by an unknown voice was more active than it was in subjects with right SNHL. Despite this difference, however, subjects with unilateral SNHL in different ears were still generally treated with the same management strategies. The activation of the subjects’ auditory cortex in response to hearing their own names spoken by an unknown voice was different between the two groups. Therefore, it indicates that the ability of residual hearing of subjects to recognize their own name spoken by an unknown voice varies depending on the side of their SNHL. Keywords: Unilateral sensorineural hearing loss, Auditory cortical activation, Naming, Functional magnetic resonance imaging (fMRI) 1. Introduction A subject who has normal hearing (NH) in one ear and sensorineural hearing loss in the other ear is considered to be unilateral sensorineural hearing impaired. Previous studies have shown that unilateral sensorineural hearing loss (SNHL) presents a particular model for the investigation of functional auditory plasticity mechanisms in humans. In addition, the hearing ability of subjects with unilateral SNHL varies from person to person because each subject will have a differing degree of hearing impairment [1,2]. Despite this, the same * Corresponding author: Jiun-Jie Wang Tel: +886-961-179139; Fax: +886-3-3275798 E-mail: [email protected] management strategies are still used for subjects with unilateral SNHL, regardless of which ear is affected. The auditory pathway of humans with normal hearing has been extensively studied. In normal-hearing subjects, auditory cortical activation in response to speech stimuli is stronger than it is in response to pure tone and white noise, especially at the left side of the superior temporal sulcus (STS) [3,4]. Speech stimuli produce cortical activation predominantly at the superior temporal gyrus (STG) bilaterally [5-7], whilst the areas of the auditory cortex activated by environmental sound are the supramarginal gyri, thalamus, insula, and right medial frontal gyrus [5,6]. Generally, in subjects with normal hearing, the auditory cortex in the left cerebral hemisphere is more active than the right in responding to speech stimuli [8,9]. However, the cortical activation pattern is characterized by neurophysiological responses over the hemisphere contralateral
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Page 1: Activation of the Auditory Cortex in Subjects with Unilateral Sensorineural Hearing ... · 2010-11-10 · impaired hearing in the other [26]. This research has, however, ignored the

Journal of Medical and Biological Engineering, 30(4): 215-219

215

Activation of the Auditory Cortex in Subjects with Unilateral

Sensorineural Hearing Impairment in Response to Hearing

Their Own Names

Jen-Fang Yu1,2 Chin-Kuo Chen2,3 Sheng-Ru Wang1,2 Che-Ming Wu3

Shu-hang Ng4,5,6 Leslie Ying7 Ying-Zu Huang8 Jiun-Jie Wang4,5,*

1Graduate Institute of Medical Mechatronics, Chang Gung University, Tao-Yuan 333, Taiwan, ROC 2Taiouan Interdisciplinary Otolaryngology Laboratory, Chang Gung University, Tao-Yuan 333, Taiwan, ROC

3Department of Otolaryngology, Chang Gung Memorial Hospital, Taipei 105, Taiwan, ROC 4Department of Diagnostic Radiology, Chang Gung Memorial Hospital, Taipei 105, Taiwan, ROC

5Department of Medical Imaging and Radiological Sciences, Chang Gung University, Tao-Yuan 333, Taiwan, ROC 6Molecular Imaging Center, Chang Gung Memorial Hospital, Taipei 105, Taiwan, ROC

7Department of Electrical Engineering and Computer Science, University of Wisconsin, Milwaukee, WI 53706, USA 8Department of Neurology, Chang Gung Memorial Hospital, Taipei 105, Taiwan, ROC

Received 20 Jan 2010; Accepted 18 Jun 2010

Abstract

This study investigated the differences in activation of the auditory cortex between subjects with right and left

unilateral sensorineural hearing loss (SNHL) when hearing their own names spoken by an unknown voice. All

experiments were performed in the Chang Gung Memorial Hospital. Magnetic resonance imaging was acquired using a

3-Tesla Siemens scanner. Ten subjects with unilateral SNHL were recruited (3 male and 7 female, aged 30 ± 14.9 years,

with 14 ± 6.29 hearing-impaired years). The activation pattern in the contralateral auditory cortex was wider than in the

ipsilateral auditory cortex for all unilateral SNHL subjects. The auditory cortex of subjects with left SNHL hearing

their own names spoken by an unknown voice was more active than it was in subjects with right SNHL. Despite this

difference, however, subjects with unilateral SNHL in different ears were still generally treated with the same

management strategies. The activation of the subjects’ auditory cortex in response to hearing their own names spoken

by an unknown voice was different between the two groups. Therefore, it indicates that the ability of residual hearing

of subjects to recognize their own name spoken by an unknown voice varies depending on the side of their SNHL.

Keywords: Unilateral sensorineural hearing loss, Auditory cortical activation, Naming, Functional magnetic resonance

imaging (fMRI)

1. Introduction

A subject who has normal hearing (NH) in one ear and

sensorineural hearing loss in the other ear is considered to be

unilateral sensorineural hearing impaired. Previous studies have

shown that unilateral sensorineural hearing loss (SNHL)

presents a particular model for the investigation of functional

auditory plasticity mechanisms in humans. In addition, the

hearing ability of subjects with unilateral SNHL varies from

person to person because each subject will have a differing

degree of hearing impairment [1,2]. Despite this, the same

* Corresponding author: Jiun-Jie Wang

Tel: +886-961-179139; Fax: +886-3-3275798

E-mail: [email protected]

management strategies are still used for subjects with unilateral

SNHL, regardless of which ear is affected.

The auditory pathway of humans with normal hearing has

been extensively studied. In normal-hearing subjects, auditory

cortical activation in response to speech stimuli is stronger than

it is in response to pure tone and white noise, especially at the

left side of the superior temporal sulcus (STS) [3,4]. Speech

stimuli produce cortical activation predominantly at the

superior temporal gyrus (STG) bilaterally [5-7], whilst the

areas of the auditory cortex activated by environmental sound

are the supramarginal gyri, thalamus, insula, and right medial

frontal gyrus [5,6]. Generally, in subjects with normal hearing,

the auditory cortex in the left cerebral hemisphere is more

active than the right in responding to speech stimuli [8,9].

However, the cortical activation pattern is characterized by

neurophysiological responses over the hemisphere contralateral

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J. Med. Biol. Eng., Vol. 30. No. 4 2010

216

to the stimulated ear [10-12]. This activation pattern is based on

the contralateral dominance of the auditory pathway. Because

the contralateral auditory pathway contains a greater number of

nerve fibers than the ipsilateral pathway, this route results in a

more direct activation of the contralateral cortex [13-15].

The subject’s own name (SON) is known to be a

significant stimulus to capture attention and generate a cognitive

response [16,17]. Hearing one's own name automatically elicits

a robust response [18-21], and a specific response to hearing the

SON has been obtained even in conditions of reduced

consciousness [20,22-24]. In addition, a familiar voice uttering

the SON might activate additional cerebral regions related to

higher cognitive processes [25]. In order to eliminate the

potential additional cerebral activation caused by a familiar

voice, the stimulus adopted in this study was the subject’s name

spoken by an unknown voice. A recent study into rapid auditory

perception and its role in speech processing, using functional

magnetic resonance imaging (fMRI), has recently helped in the

understanding of this area [9].

Although there have been studies related to the activation

of the auditory cortex in unilateral SNHL patients, this topic is

still underrepresented in the literature. At present, research on

cortical responses in unilateral sensorineural hearing loss

generally uses patients with healthy hearing in one ear and

impaired hearing in the other [26]. This research has, however,

ignored the impact impaired hearing can exert on hearing

perception. The left and right cortical regions of the brain are

differentially activated depending on the types of sound

stimulus [5,6]; even impaired hearing can exert an influence

on the cortical response. In order to eliminate this effect, all

participants recruited for this study had complete sensorineural

hearing loss in one ear and healthy hearing in the other.

This study looked at the activation of the auditory cortex

in subjects with unilateral SNHL in different ears when

hearing their own names spoken by an unknown voice. We

looked at the differences in activation between the right and

left auditory cortices, as well as at the differences in the

activation of the auditory cortex for subjects with right versus

left SNHL.

2. Materials and methods

2.1 Subjects

All experiments were performed at Chang Gung Memorial

Hospital. Magnetic resonance imaging was acquired using a

3-Tesla scanner (Trio a TIM system, Siemens). Ten patients

(three male and seven female) with unilateral SNHL were

recruited. Of these subjects, five had left hearing impairment

(aged 28 ± 14.9 years, with 10 ± 2.29 hearing-impaired years)

and the remaining five had right hearing impairment (aged

32 ± 12.6 years, with 11 ± 3.36 hearing-impaired years). All

subjects were right-handed. Pure tone audiometry was

performed on each subject in order to confirm the degree of

unilateral sensorineural hearing loss. The pure tone audiogram

demonstrated that for all patients, threshold levels were less

than 25 dB HL for the ear with normal hearing and over 110 dB

HL for the ear with hearing impairment. Tympanometry was

also performed to exclude any subjects with middle- ears

abnormalities. This study was approved by the Institutional

Review Board of Chang Gung Memorial Hospital, and

informed consent was obtained from all participants. The

experiment was conducted in accordance with the Declaration

of Helsinki.

BOLD fMRI was performed using a single-shot

T2*-weighted Echo Planar Imaging sequence. Sixty-nine slices

were acquired, with a thickness of 3 mm, covering the whole

brain down to the cerebellum. Other imaging parameters were

TR/TE/flip angle = 3000 ms/ 35 ms/ 90°, matrix size = 64 × 64,

and FOV = 192 mm, giving an in-plane resolution of

3 mm × 3 mm.

T1-weighted images were acquired for reference using an

MPRAGE sequence. The imaging parameters were TR/TE/flip

angle = 9 ms/ 4.2 ms/ 9°. One hundred and eighty sagittal slices

covering the whole brain were acquired in 10 minutes, with a

spatial resolution of 0.86 mm × 0.86 mm × 1.0 mm.

2.2 Paradigm design

The experiment consisted of 3 sessions of event-related

design paradigms, with each session consisting of 21 events.

Stimuli were conducted to both of the subject’s ears

simultaneously via Siemens air-conduction headphones.

Before the experiment, the procedure was explained to each

subject for approximately 30 minutes. The experiment would

be processed after confirming that the subject pushed the

trigger on time.

The sequence of acoustic stimuli consisted of a mixture of

pure tone and the subject’s name spoken by an unknown voice.

The pure tone stimulus shown in Figure 1(c) was a short pulse

(duration 100 msec) at a single frequency (1000 Hz), which

was produced by Audition 2.0. The subject’s name was

recorded by microphone; its waveform is shown in Figure 1(b).

The average root mean square (RMS) power for the pure tone

stimuli was -26.88 dBFS (decibels below full scale). The

average RMS power for subjects’ names was -18.07 dBFS. The

subjects’ names were introduced at random in the stimuli

sequence, as shown in Figure 1(d), and the subject was

requested to press a trigger upon hearing his (or her) name. The

total duration of the experiment was 15 minutes.

Figure 1(a) shows the noise spectrum obtained at the

5-gauss line measured during the BOLD fMRI experiment. The

peak frequency of the noise was 1475 Hz, and the peak

intensity was 88 dBSPL. The stimulus frequency of 1000 Hz

was thus not influenced by noise during the fMRI scan;

additionally, the subject was able to hear the stimuli at less than

88 dBSPL because of noise deduction by the air-conduction

headphones.

2.3 fMRI data analysis

The fMRI data were analyzed using SPM5 software

(Wellcome Trust Functional Imaging Laboratory, London, UK)

in MATLAB 7.0 (MathWorks, Inc., Natick, MA, USA). The

first two scans of the EPI series were excluded to minimize T1

relaxation artifacts.

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Sensorineural Hearing Loss - fMRI

217

(a) (b)

(c) (d)

Figure 1. (a) The spectrum of noise by EPI-fMRI (units for x, y axes are Hz and dBSPL, respectively). (b) The sound wave of one of subjects’

names spoken by an unknown voice. (c) The sound wave of pure tone. (d) Sequence of the stimuli.

The functional images were first corrected for each

participant’s motion, and the realigned images were then

normalized into the standard SPM/MNI template of a standard

stereotaxic space. The images were then interpolated to a

resolution of 2 × 2 × 2 mm3. The data was filtered using a

Gaussian spatial filter of 10-mm and a high-pass filter with a

cut-off period of 128 s. The hemodynamic response function

was used to identify the significantly activated voxels. The

subject-level statistical analysis was performed using a general

linear model. Linear contrasts of interest were constructed to

obtain subject-specific estimates of event-related activity for

the following main effects: (1) activation of the auditory

cortex of subjects with right SNHL in response to SON spoken

by an unknown voice; (2) activation of the auditory cortex of

subjects with left SNHL in response to SON spoken by an

unknown voice; and (3) a comparison of the activation of the

auditory cortex in subjects with left versus right SNHL. In

order to be able to make broader inferences about the general

population from which the subjects were drawn, these

estimates for contrasts were entered into a standard SPM

second-level analysis with the subject treated as a random

effect, using a one-sample t test. The expected mean

difference value for the t tests was set to zero. The threshold

(p < 0.05) was corrected for a false discovery rate (FDR) at

voxel level. The extent threshold for the activated regions was

set to 10 voxels. All significantly activated areas were

transformed into Talairach space. Anatomical labels (lobes

and gyri) and the Brodmann area (BA) of the local maxima of

the activated clusters were determined using a 3-D electronic

brain atlas.

3. Results

The anatomical region of auditory cortical activation of

the five subjects with right sensorineural hearing loss in

response to the SON spoken by an unknown voice is shown in

Figure 2. The region of auditory cortical activation is mainly

distributed at the superior temporal gyrus. The T value of the

voxel-level for the right hemisphere was 4.69. The coordinates

of the activation location were X = 58, Y = -44 and Z = 11

(p < 0.05). The T value of the voxel-level for the left brain was

3.82. The coordinates of the activation location shown in

Table 1 were X = -60, Y = -18 and Z = 5 (p < 0.05). These

findings show that the right auditory cortex was more active

than the left for the five subjects with right SNHL.

Figure 2. The anatomical region of auditory cortical activation of

subjects with right sensorineural hearing impairment. The T

value of the voxel-level was 4.69 in the right hemisphere and

3.82 in the left hemisphere (p < 0.05). L: left hemisphere, R:

right hemisphere.

The anatomical region of auditory cortical activation of

the five subjects with left sensorineural hearing loss in

response to the SON spoken by an unknown voice is shown in

Figure 3. The region of auditory cortical activation is again

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J. Med. Biol. Eng., Vol. 30. No. 4 2010

218

mainly distributed at the superior temporal gyrus. The T value

of the voxel-level for the right hemisphere was 6.16. The

coordinates of the activation location were X = 56, Y = -7 and

Z = 6 (p < 0.05). The T value of the voxel-level for the left

hemisphere was 7.55. The coordinates of the activation

location shown in Table 1 are X = -60, Y = -14 and Z = 3

(p < 0.05). These findings show that the left auditory cortex

was more active than the right for the five subjects with left

SNHL.

Table 1. The anatomical region of activation of subjects with unilateral

sensorineural hearing loss (p < 0.05).

Subject Hemisphere T value Anatomical region

Subjects with right

hearing impairment

Right 4.69 Superior temporal gyrus

Left 3.82 Superior temporal gyrus

Subjects with left

hearing impairment

Right 6.16 Superior temporal gyrus

Left 7.55 Superior temporal gyrus

Figure 3. The anatomical region of auditory cortical activation of

subjects with left sensorineural hearing impairment. The T

value of the voxel-level was 6.16 in the right hemisphere and

7.55 in the left hemisphere (p < 0.05). L: left hemisphere, R:

right hemisphere.

Table 2 shows the response time to pressing the trigger.

The mean response time to pressing the trigger for the five

subjects with right SNHL was 1.3 ± 0.32 seconds, and the

mean response time for the five subjects with left SNHL was

1.33 ± 0.12 seconds. There was no significant difference

between these two groups as demonstrated by independent

t test (p = 0.84).

Table 2. The response time of subjects with unilateral sensorineural

hearing impairment to press the trigger.

Subjects Response time (second)

p value Mean Standard deviation

Hearing impairment in right ear 1.3 0.32 0.84

Hearing impairment in left ear 1.33 0.12

The two groups were analyzed by two-sample t-test. The

comparison of the activation of the auditory cortex between

subjects with left SNHL and those with right SNHL is shown in

Figure 4. Based on the results, the region of auditory cortical

activation in all ten subjects was mainly distributed at the

superior temporal gyrus. The T value of the voxel-level for the

right hemisphere was 6.63. The coordinates of the activation

location were X = 52, Y = -17 and Z = 14 (p < 0.05). The T

value of the voxel-level for the left hemisphere was 8.45, which

is higher than that for the right hemisphere. The coordinates of

the activation location was X = -54, Y = -37 and Z = 10

(p < 0.05), as shown in Table 3. The auditory cortex in subjects

with left SNHL was thus demonstrably more active than that in

subjects with right SNHL.

Figure 4. The difference in activation of the auditory cortex between

subjects with left sensorineural hearing impairment and those

with right sensorineural hearing impairment. The T value of

the voxel-level was 6.63 in the right hemisphere and 8.45 in

the left hemisphere (p < 0.05). L: left hemisphere, R: right

hemisphere.

Table 3. The difference in the activation of the auditory cortex of 10

subjects with unilateral sensorineural hearing loss in either the

left or right ear (p < 0.05).

Difference Hemisphere T value Anatomical region

Unilateral SNHL in left

ear versus right ear

Right 6.63 Superior temporal gyrus

Left 8.45 Superior temporal gyrus

4. Discussion

This study found that the right auditory cortex was more

active than the left for subjects with right SNHL who heard

their own names spoken by an unknown voice. The opposite

was true for the subjects with left SNHL, with the left auditory

cortex being more active than the right. Even though the

subjects had suffered from unilateral hearing impairment for

14 ± 6.29 years, the contralateral activation pattern is still

wider than the activation in the ipsilateral auditory cortex. We

deduce from this that the crossing system of the auditory

pathway is not affected by the duration of the subjects’ hearing

impairment. It is possible that the nerve fibers involved in the

contralateral auditory pathway could be healthy and functional

in patients with unilateral SNHL, and the condition of these

nerve fibers could potentially be examined and tracked.

The activation of the auditory cortex in response to the

subjects’ own names spoken by an unknown voice was

different between the two groups, with the auditory cortex of

subjects with left SNHL being more active than that of the

subjects with right SNHL. There was no variation between the

groups in the hearing condition of either the impaired or

normal ears (which had pure tone audiometry-assessed

thresholds of over 110 dB HL and less than 25 dB HL,

respectively). This result indicates, therefore, that the ability of

subjects to recognize their own name spoken by an unknown

voice varies depending on the side of their SNHL. Because the

stimulus for this study was a speech stimulus (the subject’s

own name), and because speech signals are mostly lateralized

to the left hemisphere [3,4], the auditory cortex for the subject

with left SNHL should be more active than in a subject with

right SNHL.

5. Conclusions

Currently, subjects with unilateral SNHL are treated using

the same management strategies for hearing aid selection,

regardless of which ear is affected. Even if the subjects were

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Sensorineural Hearing Loss - fMRI

219

not treated, due to having another normal hearing ear, the

listening ability of these unilateral SNHL subjects might be

affected. Furthermore, based on pattern changes, it is possible

to compare the influence of different sound stimuli on the

auditory cortex of subjects with unilateral SNHL. Because the

stimulus for this study was a speech stimulus (the subject’s

own name), and because speech signals are mostly lateralized

to the left hemisphere, the auditory cortex for the subject with

left SNHL should be more active than in a subject with right

SNHL. Therefore, it indicates that the ability of residual

hearing of subjects to recognize their own name spoken by an

unknown voice varies depending on the side of their SNHL.

Acknowledgments

This project was supported by National Science Council

and Chang Gung Memorial Hospital (CMRPG371021).

Facilities were provided by the Biomedical Engineering Center

at Chang Gung University.

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