Vision, central 385
Reduced visual discrimination in cochlear implant users
Christine Turgeona,b, Franc¸ois Champouxa,b,d, Franco Leporea
and Dave Ellemberga,c
The aim of the study was to investigate low-level visual
function in cochlear implant users. Spatial frequency
discrimination was assessed in 16 adults with normal
hearing and 18 adults with profound deafness who had
a cochlear implant. Thresholds were measured with
sinusoidal gratings using a two-alternative temporal
forced-choice procedure combined with an adaptive
staircase. Cochlear implant users had significantly
poorer spatial frequency discrimination compared with
normal hearing participants. Therefore, auditory privation
leads to substantial changes in this particular visual
function and these changes remain even after the
restoration of hearing with a cochlear
Introduction
Sensory deprivation induces extensive brain reorganization, and deprivation of a sensory modality can alter the
neuronal responses in the remaining modalities. For example, event-related potentials show enhanced activation
of the anterior temporal areas in deaf individuals compared with hearing individuals [1,2]. Further, MRI demonstrates activation in the auditory cortex of congenitally
deaf individuals in response to visual stimuli such as moving dot patterns and moving sinusoidal gratings [3,4].
Several authors suggest that brain reorganization induced
by sensory deprivation leads to behavioral changes in
numerous visual tasks. In the case of early auditory deprivation, there is some debate over whether profound deafness results in visual deficits or an enhancement in visual
performance [5]. Some studies have documented improved visual processing in the peripheral visual field of
deaf individuals. Compared with hearing individuals, they
are faster and more accurate in detecting the direction of
moving visual stimuli [1,6], they are better at detecting
an increment in luminance [7], and they have enhanced
visual attention in the peripheral visual field [3,8,9]. In
contrast, other studies suggest that deafness leads to
a deterioration of some visual functions. For example,
higher visual temporal thresholds [10] and poorer visual
resolution [11,12] have been reported in deaf individuals.
These findings suggest that auditory stimulation during
development may play a role in the development and
maturation of certain visual functions, and that the lack of
auditory input may ultimately lead to an enhancement
in higher level functions such as visual attention and deterioration in low-level visual functions.
It is now possible to partially restore hearing in deaf individuals through the insertion of a cochlear implant. This
c 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins
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c 2012 Wolters Kluwer
implant. NeuroReport 23:385–389 !
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NeuroReport 2012, 23:385–389
Keywords: cochlear implant, deafness, frequency discrimination, vision
a
Neuropsychology and Cognition Research Center, bSchool of Speech
Pathology and Audiology, cDepartment of Kinesiology, University of Montreal and
d
Raymond-Dewar Institute, Montre´al, Que´bec, Canada
Correspondence to Dave Ellemberg, PhD, Department of Kinesiology, University
of Montreal, 2100 Edouard-Montpetit, Montre´al, Quebec, Canada H3T 1C5
Tel: + 1 514 343 7458; fax: + 1 514 343 2115;
e-mail: [email protected]
Received 4 January 2012 accepted 7 February 2012
device bypasses the missing or damaged hair cells in the
cochlea by directly stimulating the neurons of the auditory nerve and converts auditory signals into electrical
impulses. Only a few studies have investigated visual functions in deaf individuals with a cochlear implant, and those
that did were mainly interested in higher-level visual
attention. In contrast to what is reported for higher-level
visual tasks in deaf individuals, children with cochlear implants perform more poorly on tasks of visual attention
compared with normally hearing participants [13,14]. Further, using a change blindness paradigm, Bottari et al. [15]
found that deaf individuals with a cochlear implant were
less sensitive to visual changes compared with deaf participants who did not have a cochlear implant. To date, nothing is known about the development of lower-level visual
functions in deaf individuals with a cochlear implant.
The aim of the present study was to investigate low-level
visual functions in deaf individuals with a cochlear implant. Spatial frequency discrimination is known to represent a fundamental building block of visual perception
and it is essential for the analysis of fine details in a visual
scene [16]. Therefore, we compared spatial frequency
discrimination in normal hearing participants and in
individuals with a cochlear implant.
Materials and methods
Participants
Sixteen adults with normal hearing (mean age = 26 years)
and 18 adults with profound deafness and a cochlear implant (mean age = 36 years) participated in the study. For
inclusion in the study, normal hearing participants were
required to pass an audiometric test. Pure-tone detection
thresholds were assessed using an adaptive method at
250, 500, 1000, 2000, and 4000 Hz. They were assessed
DOI: 10.1097/WNR.0b013e3283525af4
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386 NeuroReport 2012, Vol 23 No 6
independently with an intra-auricular earphone for each
ear. All participants had detection thresholds below 25 dB
HL at every frequency, which corresponds to normal
hearing. Middle-ear function was assessed using a GrasonStadler GSI 38 tympanometer (GSI Grason-Stadler, Milford,
Massachusetts, USA) and all normally hearing individuals
had normal mobility of the eardrum and normal middle-ear
function.
The cochlear implant users suffered from severeprofound bilateral deafness before their surgery. All had
progressive hearing loss that had started from birth or
infancy and was present for a significant period time before implantation, and all used oral language as a primary
mode of communication. Pure-tone detection thresholds
were assessed using an adaptive method at 250, 500,
1000, 2000, and 4000 Hz in a free field at a distance of
1 m. This group presented detection thresholds that were
generally above 40 dB HL for all frequencies tested, corresponding to what is generally reported in the literature [17]. The clinical profile of each cochlear implant
user is presented in Table 1. None of the participants had
learning disabilities or other known medical conditions.
All the participants had normal or corrected-to-normal
vision as determined with the Snellen eye chart (model
R.J.’s) at a distance of 10 ft. All participants were unaware
of the nature of the experiment and they gave written
informed consent in accordance with the University of
Montreal’s Ethics Board. Recruitment was made possible
with the collaboration of the Centre de Recherche
Interdisciplinaire en Re´adaptation du Montre´al Me´tropolitain/Institut Raymond-Dewar and the Centre de
Re´adaptation en De´ficience Physique Le Bouclier.
Stimuli, design, and procedure
Before testing, each participant with a cochlear implant
was asked to adjust their implant processors at their usual
setting.
Frequency discrimination
The stimuli were luminance-modulated Gabors (i.e. a
sine wave grating multiplied by a Gaussian) with a spatial
frequency of 1 to 5 cycles per degree and a 50 ms cosine
rise–fall time. The Gabors had a width and height of 41
when viewed from a distance of 60 cm and they were
presented at a suprathreshold contrast of 50%. They
were generated by a Psychinematik software (version
1.0.0; KyberVision Consulting, Research and Development,
Table 1
Clinical profile of the cochlear implant users
Age
Etiology of
deafness
Number of years
with CI
Age at implantation
(years)
Side of the
implant
Aided thresholds with
implanta
Preimplant hearing
thresholds (R/L)b
Type of cochlear
implant
20
Congenital
2
18
L
37
> 110/ > 110
22
35
Congenital
Congenital
6
5
16
30
L
L
40
33
> 120/97
107/ > 120
45
Congenital
4
41
L
35
95/103
46
Congenital
5
41
L
27
95/93
22
Congenital
6
16
L
15
> 117/93
44
Congenital
1
43
L
33
117/ > 117
30
Congenital
2
28
L
32
93/ > 100
27
Congenital
2
25
L
22
> 107/ > 107
22
Unknown
12
10
R
27
> 120/ > 120
30
Meningitis
22
8
R
40
> 120/ > 120
55
Ototoxicity
3
52
L
23
68/97
23
Meningitis
2
22
L
23
110/91
51
Mumps
1
50
L
23
110/110
48
Congenital
2
46
L
18
118/107
38
Congenital
2
36
R
27
103/106
42
Unknown
4
38
R
22
88/88
39
Congenital
2
37
R
38
Cochlear-Freedom
Nucleus
Neurolec-Saphyr CX
Advances BionicClarion
Cochlear-Freedom
Nucleus
Advances BionicClarion
Cochlear-ESPrit 3G
Nucleus
Cochlear-Freedom
Nucleus
Advances BionicClarion
Cochlear-Freedom
Nucleus
Cochlear-Freedom
Nucleus
Cochlear-Freedom
Nucleus
Cochlear-Freedom
Nucleus
Cochlear-Freedom
Nucleus
Advances BionicClarion
Advances BionicClarion
Advances BionicClarion
Cochlear-Freedom
Nucleus
Cochlear-Freedom
Nucleus
101/ > 120
CI, cochlear implant; L, left; MPT, mean of pure-tone; R, right.
MPT = 500, 1000, 2000 Hz.
MPT = 500, 1000, 2000 Hz; > no measurable response at the limit of the audiometer for one of these frequencies (500, 1000, 2000 Hz).
a
b
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Visual function in cochlear implant users Turgeon et al. 387
Montreal, Quebec, Canada) and a Mactintosh 0S X (version 10.5.5; Apple Inc., Cupertino, California, USA) computer. The stimuli were displayed using a linearized lookup
table (calibrated with a Colour Vision Spyder 2 Pro; Datacolor, Lawrenceville, New Jersey, USA) and were presented on a 19-inch View Sonic G90fB CRT (View Sonic,
Walnut, California, USA). The maximum luminance was
100 cd/m2, the frame refresh rate was 85 Hz, and the resolution was 1024 " 768 pixels.
Frequency discrimination thresholds for each condition
(low and high frequencies) were determined using a twoalternative temporal forced choice procedure combined
with an adaptive staircase. For each trial, one interval presented a Gabor with the reference frequency, whereas the
other presented a Gabor with the probe frequency. The
presentation was randomized and the two Gabors were
separated by a 500 ms interstimulus interval. Each experiment was preceded by a training phase to ensure that
the participant understood the instructions. The first
presentation of a probe frequency was four cycles per
degree above the spatial frequency of the reference grating. Step size was subsequently adjusted according to
Levitt’s [18] transformed 2-down 1-up staircase. Step
size changed by 50% until the first reversal and then by
25%. On the way up, step size changed by 12.5%. An experimental session terminated once six response reversals
had been recorded for a specific frequency. No feedback
was provided. A subsequent pair was only presented once
the user response was received, allowing enough time to
make a decision. Two thresholds were obtained, one for
each spatial frequency, and the order of testing was randomized across participants. All experiments took place
in an audiometric sound-proof (Ge´nie Audio, Que´bec,
Canada) and dimly lit room, where each participant was
tested in a single session of about 40 min.
Results
Spatial frequency discrimination thresholds for normally
hearing and cochlear implant users are shown in Fig. 1.
A two-way analysis of variance with group (controls, cochlear implant users) and visual condition (one cycle per
degree, five cycles per degree) as a within-subjects factor
was carried out. Within-subject effects are reported according to the Greenhouse–Geisser’s correction. The
analyses showed a significant interaction F(1,32) = 7.41,
P = 0.01, a main effect of frequency F(1,32) = 17.04, P <
0.01, and a main effect of group F(1,32) = 43.45, P < 0.01.
Post-hoc analyses indicated that spatial frequency discrimination was significantly poorer in the cochlear implant users compared with the normally hearing group for
both the lower (t = 4.309, P < 0.01) and the higher spatial
frequency gratings (t = 6.602, P < 0.01). Regarding the
significant interaction, the visual inspection of the figure
suggests that the deficits were greater for the higher
compared to the lower spatial frequency.
We also conducted a series of correlations on the clinical
characteristics of the cochlear implant users that could
have impacted visual performance. No significant correlations were found between spatial frequency discrimination thresholds and the (i) age at testing (low frequency:
r = 0.220, P > 0.05; high frequency: r = – 0.017, P >
0.05), (ii) duration of cochlear implant use (low frequency: r = – 0.129, P > 0.05; high frequency: r = – 0.315,
P > 0.05), (iii) age at implantation (low frequency: r =
0.228, P > 0.05; high frequency: r = 0.103, P > 0.05), and
(iv) auditory thresholds with the cochlear implant (low
frequency: r = 0.107, P > 0.05; high frequency: r = – 0.172,
P > 0.05).
Discussion
The purpose of the present study was to assess low-level
visual perception in cochlear implant users. For this, we
measured spatial frequency discrimination, a fundamental building block of visual perception. Participants with
a cochlear implant, who had experienced a prolonged
period of progressive hearing loss since infancy, showed
significant reductions in spatial frequency discrimination
for both low-range and the mid-range spatial frequencies.
Cochlear implant users were half as sensitive as the normally
hearing controls on the discrimination task. The results
suggest that auditory deprivation leads to deficits in spatial
frequency discrimination and that these changes remain
after the restoration of hearing with the cochlear implant.
Several studies suggest that deafness alters visual perception. On the one hand, there appears to be an enhancement
in the perceptual abilities when higher-level visuocognitive
or peripheral tasks are performed [1,3,6,7,8]; on the other,
there is a reduction in perceptual abilities when low-level
visual tasks are performed. Our results agree with those
from studies on deafness. Specifically, when compared with
normally hearing individuals, the participants with a cochlear implant showed a reduction in spatial frequency
discrimination of about 55%. This is consistent with the
‘deficiency theory’ that proposes that the loss of one sensory modality disrupts the development of another [19,20].
Another possibility that could explain why our participants
have deficits in spatial frequency discrimination, is that the
restoration of hearing in this group of deaf participants
might overcome any visual gains associated with reorganization. Ultimately, our findings could be interpreted as
suggesting that the normal development of the auditory
modality is critical for the normal development of certain
aspects of visual function.
The visual deficits reported in the present study do not
seem to be related to any of the clinical characteristics of
our participants, including the age at which the cochlear
implant was received or the number of years the participants had used their cochlear implant. This is surprising,
given that there is evidence of better clinical outcomes
for individuals who had shorter periods of deafness before
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
388 NeuroReport 2012, Vol 23 No 6
that reached in grades 4 and 5 [26]. Future studies will be
needed to investigate the possible role of these deficits in
individuals who benefited from a cochlear implant.
Fig. 1
Conclusion
Frequency discrimination threshold Delta f /f ∗ (100)
25%
Control
Cochlear implant
20%
15%
∗
We found that extensive and progressive hearing loss
leading to deafness that is followed by cochlear implantation leads to significant deficits in fundamental aspects
of visual perception. The current findings support the
notion that the auditory modality is essential for the normal
development of the mechanisms underlying visual processes.
∗
Acknowledgements
This work was supported by grants from the CFI, CIHR,
and the NSERC to D.E. and grants from CIHR and
NSERC to F.L. The authors also wish to thank all of the
participants for their time and precious collaboration.
10%
5%
Conflicts of interest
There are no conflicts of interest.
0%
1 cpd
5 cpd
Spatial frequency discrimination thresholds for the control group (white
bar) and cochlear implant users (black bar) for the low (1 cpd) and the
high (5 cpd) spatial frequency discrimination conditions. *P < 0.001.
Examples of the low and high spatial frequencies are presented above
the bar graph.
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