Brain voice processing with bilateral cochlear implants: a positron emission tomography study

OTOLOGY

Brain voice processing with bilateral cochlear implants: a positronemission tomography study

Arnaud Coez • Monica Zilbovicius • Evelyne Ferrary • Didier Bouccara •

Isabelle Mosnier • Emmanuele Ambert-Dahan • Eric Bizaguet •

Jean-Luc Martinot • Yves Samson • Olivier Sterkers

Received: 9 September 2013 / Accepted: 3 November 2013

� Springer-Verlag Berlin Heidelberg 2013

Abstract Most cochlear implantations are unilateral. To

explore the benefits of a binaural cochlear implant, we used

water-labelled oxygen-15 positron emission tomography.

Relative cerebral blood flow was measured in a binaural

implant group (n = 11), while the subjects were passively

listening to human voice sounds, environmental sounds

non-voice or silence. Binaural auditory stimulation in the

cochlear implant group bilaterally activated the temporal

voice areas, whereas monaural cochlear implant stimula-

tion only activated the left temporal voice area. Direct

comparison of the binaural and the monaural cochlear

implant stimulation condition revealed an additional right

temporal activation during voice processing in the binaural

condition and the activation of a right fronto-parietal cor-

tical network during sound processing that has been

implicated in attention. These findings provide evidence

that a bilateral cochlear implant stimulation enhanced the

spectral cues associated with sound perception and

improved brain processing of voice stimuli in the right

temporal region when compared to a monaural cochlear

implant stimulation. Moreover, the recruitment of sensory

attention resources in a right fronto-parietal network

allowed patients with bilateral cochlear implant stimulation

to enhance their sound discrimination, whereas the same

patients with only one cochlear implant stimulation had

more auditory perception difficulties.

Keywords Binaural hearing � Brain imaging �

Cochlear implant � Deafness � Positron emission

tomography � Temporal voice area

Introduction

Hearing loss is an auditory perception disorder that induces

deficits in oral communication due to an ability to perceive

A. Coez � M. Zilbovicius � J.-L. Martinot

CEA-Inserm U1000 Neuroimaging and Psychiatry, Service

Hospitalier Frederic Joliot, IFR49, 91401 Orsay, France

A. Coez � M. Zilbovicius � J.-L. Martinot � Y. Samson

CEA, DRM, DSV, Service Hospitalier Frederic-Joliot,

91401 Orsay, France

A. Coez (&) � E. Bizaguet

Laboratoire de Correction Auditive, Eric Bizaguet,

20, rue Therese, 75001 Paris, France

e-mail: [email protected]

E. Ferrary � D. Bouccara � I. Mosnier � O. Sterkers

UMR-S 867, Inserm, 75018 Paris, France

E. Ferrary � D. Bouccara � E. Ambert-Dahan � O. Sterkers

Service d’ORL et de Chirurgie Cervico-Faciale, AP-HP,

Hopital Beaujon, 92110 Clichy, France


Universite Paris, 7 Denis Diderot, Paris, France


Institut Federatif de Recherche Claude Bernard Physiologie et

Pathologie, IFR02, 75018 Paris, France

I. Mosnier � O. Sterkers

Service d’ORL et de Chirurgie Cervico-Faciale, AP-HP,

Hopital Louis Mourier, 92700 Colombes, France

Y. Samson

Service Urgences Cerebro-Vasculaires, AP-HP,

Hopital Pitie-Salpetriere, 75013 Paris, France

Y. Samson

Universite Paris, 6 Pierre et Marie Curie, Paris, France

123

Eur Arch Otorhinolaryngol

DOI 10.1007/s00405-013-2810-8

acoustical cues important for speech production and

understanding. Patients with hearing loss have difficulty in

distinguishing speech and voices from other sounds such as

environmental noises. Individuals with hearing loss may

benefit from cochlear implantation to improve voice and

speech cue transduction. Most current cochlear implants

(CI) are multichannel devices that provide intra-cochlear

stimulation, exploiting the tonotopic organisation of the

cochlea and the central auditory pathways. Psychophysical

experiments have demonstrated that stimulating different

cochlear electrodes elicits auditory perception of different

pitches and that the identification of consonants, vowels

and words significantly improved as the number of bands

increased [1]. The functional results ranged from the res-

toration of sound perception to full speech intelligibility

and voice recognition [2]. The outcome of implantation

depended on the implant signal, its coupling to the central

auditory system and the ability of the auditory system and

other related brain systems to learn how to most efficiently

obtain information from the signal [3].

Monaural or binaural cochlear implantation

Although binaural perception is important for normal

hearing, recent clinical studies have demonstrated that

bilateral perception improves speech intelligibility and

sound localisation in complex, noisy environments [4]. The

majority of the 120,000 patients [2] who have benefited

from cochlear implantation only have one cochlear implant.

Binaural information (interaural time and level differences)

and the spectral shaping of sounds by the pinna are used for

sound source localisation and to increase the ability to

distinguish background noise [5]. The overall increase in

sound quality is attributed to the head shadow effect, the

squelch effect and the diotic summation effect [6]. It is still

unknown whether two CI compared to one CI could

enhance voice and speech perception and whether their

response properties differ in the two brain hemispheres.

Cochlear implants and neuroimaging

Functional neuroimaging studies provide an insight into the

cortical changes that take place in patients with cochlear

implant (see review [7]), and especially in bilateral

cochlear implant users [8, 9]. Recent (H215O) positron

emission tomography (PET) activation studies [10, 11]

have suggested that PET is an effective method to explore

the benefit of cochlear implants and that improvements in

speech intelligibility can be linked to the activation of the

temporal voice area (TVA), which is located bilaterally

along the upper bank of the superior temporal sulcus (STS).

In adults, the cerebral processing of vocal sounds is known

to engage TVAs that are primarily located along the middle

and anterior parts of the STS. Functional magnetic reso-

nance imaging (fMRI) studies have shown increased

activity in the TVA in response to voices (speech and non-

speech vocalisations, such as laughs and coughs) when

compared to natural non-vocal sounds (environmental and

musical sounds) or to amplitude- or frequency-matched

acoustical control sounds [12]. A previous study [12]

examined how the activation of voice-sensitive areas and

the subjects’ performance on voice-perception tasks are

affected by modifying the spectral structure of the stimuli.

Sets of vocal and non-vocal sounds were presented during

scanning, and spectral filtering removed either the high or

low frequencies. The mean activity in the TVA was

enhanced by vocal stimuli in comparison to non-vocal

stimuli, but the activity was significantly decreased by

spectral filtering. A CI was used as one method of spectral

filtering [1]. To measure the benefit of two independent

sites of cochlear stimulation provided by a bilateral CI, we

used PET (H215O) to study TVA activation. We hypothe-

sised that an improvement in spectral cue transmission

by bilateral CI stimulation would produce stronger

TVA activation when compared to a unilateral implant

stimulation.

Materials and methods

Subjects

Eleven male patients with bilateral cochlear implants and

an average age of 56 years ± 9 (mean ± SD, n = 11)

were studied during binaural or monaural stimulation.

Written informed consent was obtained from all subjects.

The Xavier-Bichat Hospital Ethics Committee approved

the protocol. Patients had bilateral progressive (n = 8),

otosclerosis (n = 2), or meningitis (n = 1) post-lingual

deafness. They were bilaterally implanted between 2003

and 2006 with Opus 2 cochlear implants containing 12

active electrodes (Medel Inc, Innsbruck, Austria), and they

had 3 years ± 1 (mean ± SD, n = 11) of cochlear implant

experience. The CI was used more than 8 h a day. The

mean auditory threshold (average of auditory thresholds at

500 Hz, 1, 2 and 4 kHz) measured in the free field with

warble tones was 23 dB ± 7 (mean ± SD, n = 11). The

average intelligibility score on the Lafon monosyllabic task

at 65 dB in the free field of the binaural condition was

75 % ± 23, which was higher than in the monaural con-

dition (54 ± 28 %, p\ 0.05).

Task and stimuli

The subjects were scanned while passively listening to

voice sounds (30 % speech sounds, 70 % non-speech vocal


123

sounds) or to only non-voice stimuli (19 % nature, 24 %

animals, 47 % modern human environment, and 10 %

musical instruments). The same stimuli were used in the

original fMRI study [12]. Twelve PET (ECAT-EXACT-

HR?; Siemens AG, Erlangen, Germany) acquisitions after

an intravenous bolus of (H215O) (333 MBq per injection)

were obtained at 10-min intervals during passive listening:

four measurements occurred during passive listening to the

voice condition (two during a binaural stimulation, two

during a monaural stimulation), four occurred during pas-

sive listening to a non-voice condition (two during a bin-

aural stimulation, two during a monaural stimulation), and

four occurred during passive listening in silence. The lis-

tening blocks were presented to the patient in random order

at a mean sound pressure level of 65 dB through KOSS

electrostatic headphones. Patients were asked to listen

carefully to the sounds with their eyes closed and while

awake, which was systematically checked during the exam.

At the end of the PET exam, the patients were asked to

report what they had heard.

PET acquisition

The rCBF was determined from the distribution of radio-

activity measured with the PET (ECAT-EXACT-HR?,

Siemens AG, Erlangen, Germany) after intravenous H215O

bolus injections [13]. Listeners received 12 H215O injections

(333 MBq per injection) corresponding to the 12 rCBF

measurements that were performed at 10-min intervals.

The first scan corresponded to a silent condition. There was

a fixed period of 30 s between the bolus infusion and the

presentation of the stimuli. The attenuation-corrected data

were reconstructed into 63 axial slices (2.25 mm thick)

with a resulting resolution of 4.5 mm full width at half

maximum after reconstruction [14].

Data analyses

The rCBF images were analysed using statistical para-

metric mapping software (SPM99) that was used for image

realignment, transformation into standard stereotaxic ana-

tomical space [15], smoothing (12 mm) and statistical

analyses [16]. The state-dependent differences in global

flow were covaried using proportional scaling. Compari-

sons across conditions were made using a t test that was

subsequently transformed into normally distributed z sta-

tistics using a multi-study design. The resulting z map

threshold was at p\ 0.001.

Three statistical analyses of activation were performed

in the monaural and binaural conditions: a comparison of

activation for listening to voice and non-voice sounds

versus the silent condition (p = 0.001; corrected for mul-

tiple comparisons to p = 0.05) and a comparison between

voice stimuli and non-voice stimuli (p = 0.00005). These

analyses were then examined by a between-condition

comparison relative to the results obtained in the CI

monaural and binaural stimulation conditions for the voice

and non-voice stimuli (p = 0.001) and for the voice and

non-voice conditions compared to the silent condition

(p = 0.0001).

Results

Comparing voice to non-voice stimuli during monaural

and binaural conditions

Activation was observed bilaterally in the TVA in the

binaural CI stimulation condition. In contrast, in the

monaural condition, patients only showed left TVA acti-

vation without right TVA activation (Fig. 1, left upper

panel; Table 1).

When comparing the binaural condition to the monaural

condition, the CI showed a significantly greater right

activation along the upper bank of the right STS in the

former condition than in the latter one (Fig. 1, left lower

panel; Table 2). When comparing the monaural condition

to the binaural one, no activation was found.

Comparing the whole sound stimuli to silence

during the monaural and binaural conditions

When comparing the listening condition (pooled voice and

non-voice conditions) to the silence condition, binaural and

monaural stimulations by the CI led to a bilateral temporal

pattern of activation (Fig. 1, right upper panel; Table 3).

Activation peaks were similarly located in both right and

left STS, during the binaural and monaural stimulations.

Activation of a right fronto-parietal network was

observed in the binaural condition when compared to the

monaural one (Fig. 1, right lower panel; Table 4). No

additional temporal activation was found in the binaural

condition as compared to the monaural one.

Discussion

Bilateral cochlear implant and TVA activation

Listening to the voice stimuli compared to listening to non-

voice stimuli, a bilateral TVA activation was found during

bilateral CI stimulation. Only the left TVA was activated

during unilateral CI stimulation. When compared to mon-

aural stimulation, binaurally stimulated patients had an

additional right temporal activation with their CI. Patients

also had a better intelligibility score with two cochlear


123

implants. As shown in previous studies [10, 11], we found

that the subjects’ rCBF response to the stimuli paralleled

their intelligibility score performance. With a different

PET paradigm design, using word stimuli, binaural stim-

ulation through cochlear implants appeared also advanta-

geous when compared with the monaural at the

neurofunctional level because the pattern of brain activa-

tion was closer to the normal one [9]. The paradigm of the

present study allowed a direct comparison of a binaural

stimulation to a monaural one by cochlear implants.

Although, some studies suggested a dissociation in the

dynamic of functional recuperation of speech and voice

processing [17], binaural cochlear users had in this study an

immediate degradation of speech intelligibility when using

only one cochlear implant and they had concomitantly a

different pattern of brain networks when listening to voi-

ces. Moreover, in adults, the TVAs are sensitive to voices

and highly selective. The enhanced responses to voice

stimuli as compared to a range of control sounds, even after

spectral filtering of voice and non-voice stimuli [12],

allowed showing that the TVA’s preference is driven by

low-level acoustical parameters.

Bilateral cochlear implant and perception of spectral

acoustical cues

A weaker brain response with increased spectral filtering

was found in a group of normal hearing adults [12, 18]. In

vocoding, a process that mimics the effects of a cochlear

implant processor, global temporal information is pre-

served, while the fine spectral structure is degraded (1).

The difference between monaural and binaural CI stimu-

lation reflects the impact of a reduced number of inde-

pendent peripheral sites of stimulation in the cochlea

obtained with a single CI when compared to a strict bin-

aural effect with two cochlear implants. Actually, no more

than 4–8 independent sites are available in the speech-

processor context using the present electrode designs due

to substantial overlap in the electric fields from adjacent

electrodes [19]. The use of two CI allowed for an increase

in the number of independent ear stimulation sites and

improved the ability to discriminate the features of two

different sounds that could allow the patient to have a

stronger discrimination of voice sounds as compared to

other sounds.

Fig. 1 Localisation of activation peaks. Left upper panel voice versus

non-voice group analysis. The location of activation peaks to compare

‘voice’ versus ‘non-voice’ in each condition (binaural and monaural

condition with bilateral CI at p = 0.00005) shown in a lateral view of

both hemispheres. Right upper panel voice and non-voice versus

silence group analysis. The location of activation peaks comparing the

‘voice ? non-voice’ versus ‘silence’ conditions [binaural and mon-

aural conditions with bilateral CI at p\ 0.001 and then corrected for

multiple comparisons (p = 0.05)] are shown in a lateral view of both

hemispheres. Lower panel direct comparison of a monaural and a

binaural stimulation using a CI. The localisation of the activation

peaks are shown in a glass brain view. Left lower panel voice versus

non-voice (at p = 0.001). The location of activation peaks comparing

the ‘voice’ versus ‘non-voice’ in the binaural versus the monaural

stimulation (upper panel) is shown. Right lower panel voice and non-

voice versus silence (at p = 0.0001). The location of activation peaks

comparing the ‘voice ? non-voice’ versus ‘silence’ in the binaural

versus the monaural stimulation is shown. CI cochlear implant


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Specifically, several studies have examined the spectral

and temporal acoustical cues present in the stimuli, which

were shown to be important factors for determining the

recruitment of the left and/or right auditory cortex [20].

Many PET and fMRI experiments [21, 22] have shown an

enhanced sensitivity to temporal rate by the left auditory

cortex and to pitch by the right auditory cortex. In general,

damage to the right superior temporal cortex, but not to the

left primary auditory areas, affects a variety of other tonal

or spectral processing tasks [23, 24]. In this study, patients

had no cerebral lesions, and the supplementary right tem-

poral activation should reflect stronger bottom-up sound

perception from spectral cues when two cochlear implants

were functioning.

Bilateral cochlear implant and brain sound

discrimination networks

rCBF increases in the right temporal lobe have been pre-

viously correlated with subjects’ performance in a speaker

identification task [25] or with their ability to direct

attention to vocal identity [26, 27]. By comparing the

binaural to monaural conditions when listening to voice

and non-voice stimuli versus silence, we observed the

activation of a supplementary right fronto-parietal network

in the binaural CI stimulation condition. This right fronto-

parietal network activation has been found in other studies

on selective or sustained attention to sound intensity dis-

crimination [28] or to sound duration [29]. In these two

Table 1 Coordinates, size and Z score of areas activated by voice

compared to non-voice conditions in the CI group

Area Voice versus non-voice

x y z Z t Cluster

size

Binaural CI stimulation

STS, anterior (BA21) 66 -2 -6 4.38 4.48 27

STS, middle (BA22) 68 -14 4 4.06 4.14 15

STS, middle (BA21) -60 -10 -4 4.10 4.18 66

STS, posterior (BA22) -64 -22 4 4.17 4.25

Monaural CI stimulation

STS, middle (BA21) -58 -12 0 5.66 5.87 517

STS, posterior (BA22) -64 -22 2 4.98 5.12

Approximate Brodmann numbers (BA) associated with anatomical

regions of the superior temporal sulcus (STS) are given in paren-

theses. Coordinates (in standard stereotaxic space [15]) of voxels

correspond to local maxima of Z value, above Z = 4.0 (p = 0.00005)

within each focus of activation. x: distance (mm) to right (?) or left

(-) of the midsagittal line; y: distance anterior (?) or posterior (-) to

vertical plane through the anterior commissure; z: distance above (?)

or below (-) the intercommissural (AC-PC) line. The cluster size

refers to the number (k) of voxels in a given cluster (voxel size, in

mm: 2 9 2 9 2); for statistical parametric mapping, SPM(Z) maps

were thresholded at t = 3.96 (p\ 0.00005, uncorrected)

Table 2 Monaural and binaural CI stimulation comparison

Area Voice versus non-voice

x y z Z t Cluster

size

Binaural versus monaural CI stimulation

STS, middle (BA42) 72 -14 12 3.24 3.28 4

Monaural CI stimulation No significant differences

Coordinates, size and Z score of areas activated by voice compared to

non-voice conditions




correspond to local maxima of Z value, above Z = 3.0 (p = 0.001)







were thresholded at t = 3.13 (p = 0.001, uncorrected)

Table 3 Coordinates, size and Z score of areas activated by voice

and non-voice conditions compared to silent conditions in the CI

groups in the monaural and the binaural condition at p\ 0.001 cor-

rected for multiple comparison (p = 0.05)

Area Voice ? non-voice versus silence

x y z Z t Cluster

size

Binaural CI stimulation

STS, posterior (BA22) 62 -24 6 [10 16.76 5,455

STS anterior (BA21) 64 -6 -6 [10 14.50

STS posterior (BA 22) -60 -22 6 [10 11.48 3,280

STS posterior (BA42) -46 -24 6 [10 10.74

Monaural CI stimulation

STS, posterior (BA22) 66 -22 4 [10 18.12 4,811

STS, anterior (BA21) 62 -4 -4 [10 12.28

STS, posterior (BA22) -58 -30 8 [10 12.37 4,250

STS, middle (BA21) -48 -12 -4 [10 10.99




correspond to local maxima of Z value, above Z[ 10 (p\ 0.001)







were thresholded at t = 4.65 (p\ 0.001, uncorrected) and then cor-

rected for multiple comparisons (p = 0.05)

STS superior temporal sulcus


123

studies, comparable peaks (mean location: x, y, z) of acti-

vation [(48, 0, 48), (44, -48, 50) and (42, 28, 4)] were

found. This non-specific cortical network is associated with

sound discrimination ability. This neuro-functioning

observation supports the conclusion that with two CI,

patients have better sound discrimination abilities and they

have to pay less attention because of a lack of auditory

perception when compared to one CI.

We could speculate that while the involvement of

auditory areas reflected the processing of acoustic con-

tributors to voice sounds activity in frontal regions reflec-

ted the overall perceived attractiveness of sounds despite

their lack of linguistic content [30]. The results obtained

with two cochlear implants compared to one may suggest

the influence of hidden non-linguistic aspects of signals on

cerebral activity that needs further investigations.

It is currently important to determine the utility of

bilateral cochlear implants. The TVA PET activation

studies examined a group of patients to objectively dem-

onstrate the binaural advantages resulting from improve-

ments in the peripheral spectral representation of the

stimuli. The number of independent channels was an

important characteristic. We found an enhanced cortical

representation of the voice when using both CI, but the

activation of a right fronto-parietal attention network could

also facilitate spectral sound discrimination.

Acknowledgments We thank the Beaujon Hospital clinical team

for their assistance and the patients for their participation in this

study. This work was supported by the Institut National de la Sante et

de la Recherche Medicale, Inserm, France, and the Commissariat a

l’Energie Atomique, CEA, France. The authors declare that they have

no competing financial interests.

Conflict of interest No duality of interest to declare.

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Table 4 Monaural and binaural CI stimulation comparison

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CI stimulation

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Coordinates, size and Z score of areas activated by voice and non-

voice condition compared to silent condition


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Brain voice processing with bilateral cochlear implants: a positron emission tomography study

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