European Annals of Otorhinolaryngology, Head and Neck diseases (2012) 129, 98—103

Available online at

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REVIEW OF THE LITERATURE

Understanding the deafened brain: Implications for

cochlear implant rehabilitation
D.S. Lazard a,b,∗, A.-L. Giraud a, D. Gnansia c, B. Meyer b,d, O. Sterkers b,e

a
Inserm U960, école normale supérieure, 45, rue d’Ulm, 75005 Paris, France
b
Service d’ORL et de chirurgie cervico-faciale, hôpital Beaujon, AP—HP, 100, boulevard du Général-Leclerc,
92118 Clichy cedex, France
c
MXM-Neurelec, 2720, chemin Saint-Bernard, 06224 Vallauris, France
d
Université Paris-6 Pierre-et-Marie-Curie, 15, rue de l’École-de-Médecine, 75006 Paris, France
e
UMR-S 867, Inserm, université Paris-7 Denis Diderot, 75018 Paris, France

KEYWORDS Summary The cochlear implant (CI), by enabling oral communication in severely to profoundly
Cross-modality; deaf subjects, is one of the major medical advances over the last fifty years. Despite the globally
Functional MRI; very satisfactory results, individual outcomes vary considerably. The objective of this review
PET; is to describe the various factors influencing the results of CI rehabilitation with particular
Phonology; emphasis on the better understanding of neurocognitive mechanisms provided by functional
Plasticity; brain imaging.
Rehabilitation; The following aspects will be discussed:
Pre/post-lingual; 1. Peripheral predictors such as the degree of preservation of nerve structures and the
Maturation; positioning of the electrode array.
Predictor; 2. The duration of auditory deprivation whose influence on brain reorganization is now
Performance becoming more clearly understood.
3. The age of initiation of hearing rehabilitation in subjects with pre-lingual deafness influ-
encing the possibility of physiological maturation of nerve structures.
4. The concepts of sensitive period, decoupling and cross-modality.
5. In post-lingually deaf adults, brain plasticity can allow adaptation to the disability induced
by deafness, subsequently potentiating CI rehabilitation, particularly as a result of audiovisual
interactions.
6. Several studies provide concordant evidence that implanted patients present different
phonological analysis and primary linguistic capacities.
The results of CI rehabilitation are dependent on factors situated between the cochlea
and cortical associative areas. The importance of higher cognitive influences on the func-
tional results of cochlear implantation justify adaptation of coding strategies, as well as global
cognitive management of deaf patients by utilising brain plasticity capacities.
© 2011 Published by Elsevier Masson SAS.

∗ Corresponding author. Tel.: +33 1 40 87 55 71; fax: +33 1 46 25 23 62.

E-mail address: dianelazard@yahoo.fr (D.S. Lazard).

1879-7296/$ – see front matter © 2011 Published by Elsevier Masson SAS.

doi:10.1016/j.anorl.2011.06.001
Understanding the deafened brain: Implications for cochlear implant rehabilitation
Introduction
Severe to profound bilateral deafness, especially when it
occurs in subjects previously able to hear, can cause social
isolation and severe distress. The cochlear implant (CI), by
enabling good quality oral communication in quiet [1,2],
represents one of the major medical advances over the last
fifty years. CI can be proposed in patients with congenital
deafness (pre-lingual deafness), ideally before the age of 2
years, or in patients in whom severe hearing loss occurred
after acquisition of language (post-lingual deafness). In
1995, there were 12,000 implanted subjects throughout the
world, with 120,000 in 2008, and 200,000 in 2010. Despite
the globally very satisfactory results, individual outcomes
vary considerably. For example, the median recognition of
disyllabic words is 70% 1 year after surgery (range: 100 to
0%) [1]. This variability is observed in both post-lingually
deaf adults and congenitally deaf children [2]. The propor-
tion of patients with word recognition scores less than 10% is
difficult to assess, but appears to be about 10% [3]. However,
patients with test scores less than 50% must be considered
to present oral communication difficulties.
This marked variability of outcomes can be partly
explained by peripheral predictors such as the degree of
preservation of spiral ganglion cells [4], or the position of
the electrode array [5,6]. The duration of auditory depriva-
tion is another major predictive factor due to its impact on
the peripheral [7] but especially the central nervous system.
Functional brain imaging has improved our understanding of
maturation of central auditory pathways in children, and the
cerebral changes induced by sensory deprivation in children
and in adults. The influence of cognitive factors appears to
be just as important if not more important than peripheral
structures in the performance of CI [8].
The objective of this review is to describe the var-
ious factors influencing the performance of CI hearing
rehabilitation, with particular emphasis on the better
understanding of neurocognitive mechanisms, provided by
functional brain imaging.
Possible causes of variable performance
Factors considered to have little or no influence
The older age of implantation of post-lingually deaf adults,
although resulting in lower performances, provides a high
gain in life quality to this sub-population [9]. There is there-
fore no upper age limit for cochlear implantation. The type
of implant or coding strategies at equivalent times has been
excluded so far as factors of variable performance [10,11].
Published results on meningitis as a cause of deafness are
contradictory. Some authors consider this aetiology to be
associated with poorer results due to more difficult and
therefore incomplete insertion of electrodes [12] or due
to central disorders (secondary hydrocephalus for example)
[9]. Other authors have reported similar performances to
those of patients implanted for congenital deafness, when
more progressive and higher stimulation thresholds (C and
T levels) and higher stimulation rates are applied during
fittings [13].
99
Certain peripheral factors have also been proposed to
explain the variable performance of CI.
Positioning of electrode array: angle, length, scalar
placement
The targets of electrical stimulation are the spiral ganglion
cells. There is a relationship between the distance to the
spiral ganglion and the quantity of energy that needs to
be delivered. Electrode placement as close as possible to
these structures is recommended by inserting the electrode
array in the scala tympani, while avoiding the scala vestibuli,
with the shortest possible distance to the modiolus [5,6].
Computed tomography methods have been developed to
evaluate: the distance of the electrode array to the modi-
olus; the percentage placement inside the cochlear canal
[14]; or the length or angle of insertion1 [6,15]. Excessively
deep insertion of electrode arrays not specifically designed
for long insertion appears to be associated with an increased
risk of cochlear damage (contortion, dislocation) and there-
fore poorer performance [5,6].
In order to limit these peripheral factors of variability,
‘‘soft surgery’’ introduction techniques [16] and the design
of electrode arrays have tried to decrease the distance
between the electrodes and spiral ganglion cells. A future
approach could consist of inserting the electrode array into
the modiolus [17] and/or promoting nerve growth by admin-
istration of neurotrophic factors. Finally, other types of
non-electrical (optic) stimulation are currently under inves-
tigation [18].
Duration of auditory deprivation
The aetiology most frequently proposed to explain the
variable performance in congenitally deaf children and post-
lingually deaf adults is the duration of auditory deprivation
[7,19,20]. However, many mechanisms are involved and
differ between pre- and post-lingually deaf populations.
Post mortem histological examination of the petrous tem-
poral bones of post-lingually deaf adults has concluded that
loss of inner hair cells induces retrograde neural degener-
ation [21]. The extent of this degeneration appears to be
correlated with the duration of deafness [4]. However, diver-
gent clinical and histological results are observed: patients
with few residual spiral ganglion cells can obtain good
results [11,22] and a long duration of deafness may not
always result in excessive degeneration. Another structure
influenced by auditory deprivation is the central nervous sys-
tem: even when all of the peripheral prerequisites for good
performances are present, functional cortical auditory net-
works and synergistic audiovisual cooperation are essential
to derive meaningful information from the distorted sound
provided by the CI [8]. Central processes therefore play an
essential role in understanding of the CI message.
1 The angle of insertion is more precise for evaluation of electrical
tonotopy, ensuring a better correspondence with the Greenwood’s
formula, relating cochlear place to characteristic frequency.
100
The auditory brain
Functional brain imaging (functional MRI (fMRI) or positron
emission tomography (PET)), evoked potentials, electroen-
cephalography or magnetoencephalography, have eluci-
dated the way in which brain structure is modified by the
presence or, on the contrary, the absence of auditory stimuli.
Maturation of multi-sensory and associative cortical
auditory areas in pre-lingually deaf children
Cortical responses generated by non-auditory stimuli (visual
[23] or somatosensory [24]) were studied by fMRI in pro-
foundly pre-lingually deaf adults using sign language. These
non-auditory stimuli, not related to sign language, gen-
erated activation in areas normally devoted to hearing
(temporal cortex) (Fig. 1). This mainly visual colonization
of the auditory cortex is secondary to the absence of audi-
tory stimulation and not to the practice of sign language
[25]. Normally functioning modalities deploy supplementary
resources and do not suffer from the sensory restriction.
Non-implanted profoundly deaf subjects therefore develop
better spatial attentional capacities [26].
These higher capacities compared to normal-hearing sub-
jects develop as a result of:
• potentiation of cortical areas that are already multimodal
[25,27]. Multimodal areas are defined as regions of the
brain able to process and integrate physiologically inputs
of various nature. An example of a multimodal area is the
associative auditory cortex, which integrates visual and
auditory inputs [28];
• modification of the intrinsic properties of the primary
auditory cortex. Colonization by other sensory modalities
of cortical areas not stimulated by their usual modality
Figure 1 Schematic surface representation of left auditory
and visual cortices in a setting of physiological sensory matura-
tion.
White: zones of activation responding to auditory input in the
primary and secondary auditory cortices and Wernicke’s area
(temporal lobe); black: zones of activation responding to visual
inputs in the primary and secondary visual cortices (occipi-
tal lobe). In the case of non-implanted profound congenital
deafness, visual or somatosensory inputs activate the primary
auditory cortex.
D.S. Lazard et al.
is called cross-modality. Non-implanted profoundly deaf
subjects therefore develop visual cross-modality of the
auditory cortex.
These modifications are now known to be influenced by
the duration of auditory deprivation. The study of cortical
auditory evoked potentials (latency and morphology of the
P12 wave) in children implanted at various ages has demon-
strated a sensitive period during which the auditory system is
particularly plastic and able to develop almost normal cen-
tral maturation. This maturation occurs as a result of the
auditory stimulation delivered by the CI [29]. The sensitive
period is situated before the age of 3.5 years. After the age
of 7 years, speech integration and comprehension become
much more difficult and the results of CI are much more
variable. Between these two extremes, there is an individual
variability of plastic capacities and therefore performances.
Part of this variability is independent of the duration of
auditory deprivation and may be explained by cross-modal
reorganization of the auditory cortex. This reorganization
seems to start during fetal life and to be irreversible despite
early cochlear implantation [30,31]. Some areas of the tem-
poral cortex may already be reused by modalities other than
hearing and may prevent physiological auditory maturation.
Inversely, other areas may remain devoid of any cognitive
use, allowing the possibility of good performance of CI if
maturation of these areas is triggered by the auditory inputs
provided by the CI, even at a relatively advanced age of
implantation [32]. The factors influencing these maturation
mappings have not been identified.
At the end of the sensitive period, in the absence of
auditory stimulation, primary and secondary auditory areas
become decoupled: these areas are no longer able to
develop interconnections, even when cochlear implantation
is performed [33]. Feedback loops and high-level cognitive
modulations controlling auditory processing fail to develop.
Auditory areas are then available for reorganizations involv-
ing aberrant connections and neo-couplings. Children who
are implanted at an older age may therefore present audi-
tory activation in visual and parieto-temporal areas with no
benefit in terms of speech comprehension [29].
Basic research has formally demonstrated the need for
early cochlear implantation in children. Although the sen-
sitive period for satisfactory afferentation and maturation
of the auditory cortex occurs very early in childhood, a cer-
tain amount of plasticity nevertheless remains possible at
all ages [34—36]. The brain of post-lingually deaf adults can
also undergo changes induced by auditory deprivation and
then by CI rehabilitation.
Plasticity and cross-modality in implanted
post-lingually deaf subjects
Despite progress in coding strategies, the auditory infor-
mation delivered by the CI remains coarse. In implanted
2 The P1 wave represents the sum of the activities of synapses
situated on auditory pathways from the thalamus to high-level cog-
nitive areas. It reflects associative auditory processing using neural
loops between primary and secondary auditory areas.
Understanding the deafened brain: Implications for cochlear implant rehabilitation
Figure 2 Word recognition learning curve during the first year
after cochlear implantation. Median results of a population
of 55 post-lingually deaf adults expressed as the percentage
recognition of dissyllabic words derived from Fournier lists and
presented at 65 dB in quiet.
post-lingually deaf subjects, progressive improvement of
performance during the first year demonstrates the capacity
of the brain to adapt to these deformed auditory inputs that
differ from those to which it is accustomed [8] (Fig. 2).
During the period of deafness, subjects maintain oral
comprehension by developing lip reading, the efficacy of
which varies from one subject to another. They use visual
clues to complete the limited auditory information avail-
able. It could be logical to assume that the use of lip
reading would decrease with restoration of hearing. How-
ever, in practice, the information transmitted by the CI is
too rudimentary and approximate (particularly in noise) to
be sufficient and requires the persistent use of the visual
clues provided by lip reading [37].
Over the months or even years following cochlear
implantation, activation of the associative auditory cortex
gradually increases for stimuli containing speech informa-
tion, but remains stable for noise. A central learning process
therefore occurs in implanted patients enabling them to dis-
tinguish information with a linguistic content from other
information [35]. This constitutes the intra-modal plastic-
ity of the auditory cortex. In parallel, the primary visual
cortex develops activation in response to auditory stimuli.
As in the auditory cortex, the rate of activation depends
on the speech information contained [35]. This modifica-
tion of the properties of the visual cortex corresponds to
cross-modal plasticity. A basic inter-modal audiovisual coop-
eration is present in all individuals, but due to the ambiguity
of the auditory signal of the CI, patients make greater use of
the visual component compared to normal-hearing subjects
and develop synergistic interactions [34,36,38]. In the case
of low performance with the CI (< 50% of word recognition),
due to insufficient auditory cues, a supplementary compen-
sation is created by the development of visual responses
within the auditory cortex [39]. This cross-modal reorgani-
zation of the auditory cortex can even become deleterious to
speech comprehension when it is over-developed, as it has
been shown that implanted subjects with poor performance
present deterioration of their word recognition scores in the
presence of visual stimuli (colour screens or moving points)
101
that compete with auditory recognition tasks. In contrast,
normal-hearing control subjects and cochlear-implanted
subjects with good performances are not bothered by visual
distractors [40]. Excessive visual reorganization of audi-
tory areas can therefore induce integration conflicts in the
case of incongruent audiovisual stimuli, even when they are
devoid of any linguistic content [40].
Reorganization of phonological processing
circuits: a possible key to the performance of
the cochlear implantees with post-lingual
deafness
Due to degradation of the auditory information delivered
by the CI, reconstitution of phonemic cues in cochlear-
implanted post-lingually deaf subjects, regardless of their
performance, is a cognitively more difficult task than
semantic processing [41]. Implanted subjects are also not
equivalent in terms of primary analysis of auditory infor-
mation. For example, some subjects with poor performance
perceive the auditory input, but do not activate the area
specific for recognition of the human voice, unlike normal-
hearing control subjects and implanted subjects with good
performance. Poor performance could be explained by a
defect of extraction of the human voice from the audi-
tory message [42]. Absence of recruitment has also been
demonstrated in the left inferior prefrontal cortex [43], a
multimodal region participating in phonological and seman-
tic processing of language.
The absence of recruitment of these regions could corre-
spond to:
• an inappropriate routing of auditory information due
to cross-modal reorganization of these regions. Audi-
tory information can no longer be analysed because the
dedicated neurons now process other sensory modalities
and/or;
• poor correspondence between the perceived sounds and
their internal phonemic representations.
Phonological decomposition is an initial auditory step
allowing the subsequent semantic analysis. Subjects with
poor performance would therefore lack linguistic analy-
sis and a valid correspondence between perceived and
memorized phonology, limiting extraction of speech com-
prehension. These difficulties of matching the sounds
provided by the CI and internal phonological representations
tend to worsen with the duration of auditory deprivation
[44]. Progressive deterioration of phonological memory and
its dorsal route (parieto-frontal) has been demonstrated
in post-lingually deaf subjects (Fig. 3). Subjects with the
longest duration of deafness use the ventral semantic route
(occipito-temporal) to palliate the insufficient elementary
phonological decomposition. This leads to difficulties in pro-
cessing the information delivered by the CI due to global
auditory analysis, resulting in erroneous segmentation of
the message. In contrast, subjects with maintained phono-
logical skills sustained by audiovisual interactions, present
good performances with their CI and generally present the
shortest durations of auditory deprivation [44].
The study of non-implanted pre-lingually deaf subjects
who have developed good reading skills shows that they
102 D.S. Lazard et al.

Figure 3 Functional MRI exploration phonological memory of post-lingually deaf adults, candidates for cochlear implantation (CI).
Surface representation of the left hemisphere.
The task consisted of phonological segmentation exercises by performing rhyme tests. The figure illustrates the correlation between
the neural networks used during the task and word recognition performances obtained prospectively after 6 months of implantation.
The physiological phonological network uses a dorsal network (superior) including fronto-parietal areas, while the ventral network
(inferior) extracts semantic information and uses inferior temporo-occipital, anterior temporal and inferior frontal areas. Deaf
subjects who use the dorsal phonological network will obtain good results with the CI. In contrast, subjects who use the ventral
semantic network (global analysis) to perform the rhyme task will obtain poorer performance with their CI. The use of the dorsal
network significantly decreases with increasing duration of auditory deprivation.

are able to successfully complete fine phonological anal-
ysis tasks (rhymes) despite the fact that they have never
received any auditory information [45,46]. Functional brain
imaging has demonstrated the existence of a dorsal net-
work, less well developed and less lateralised to the left
than in normal-hearing subjects, but nevertheless present.
It is based on more marked articulatory cues and internal
repetition [45,46]. Post-lingually deaf implanted subjects
with good performance may therefore also use articulatory
correspondences that have been maintained active by audio-
visual cooperation [44]. This audiovisual cooperation would
be less functional in subjects with poor performance, and
may even become deleterious when visual colonization of
auditory areas becomes predominant [40,47].
More extensive investigation of the auditory memory of
post-lingually deaf subjects has shown modifications of net-
works evoking environmental and non-speech sounds. These
reorganizations depend on the duration of deafness and are
designed to palliate the phonological deficit. In some cases,
they can be deleterious and associated with a poor prognosis
of cochlear implantation [44,48].
It would therefore be tempting to propose a cognitive
rehabilitation designed to promote internal phonological
segmentation and correspondences, and to preserve global
auditory memory. Studies are currently underway in this
field.
Conclusion
Auditory deprivation is clearly responsible for socioeco-
nomic disability, but also induces modifications of brain
organization in both pre-lingual and post-lingual deafness.
The results of CI rehabilitation are dependent on multiple
factors situated between the cochlea peripherally and high-
level central associative areas. The importance of higher
cognitive influences on the functional results of CI would
justify adaptation of transmission of the peripheral message
but also global cognitive management of deaf patients in
order to take maximum advantage of their brain plasticity
capacities.
Funding: this article was made possible by the financial
support of Neurelec (MXM, Vallauris, France) and the Asso-
ciation des anciens internes des hôpitaux de Paris, with no
conflict of interest.
Disclosure of interest
The authors declare that they have no conflicts of interest
concerning this article.
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