Changes in early cortical visual processing predict enhanced reactivity in deaf individuals.

Abstract

Individuals with profound deafness rely critically on vision to interact with their environment. Improvement of visual performance as a consequence of auditory deprivation is assumed to result from cross-modal changes occurring in late stages of visual processing. Here we measured reaction times and event-related potentials (ERPs) in profoundly deaf adults and hearing controls during a speeded visual detection task, to assess to what extent the enhanced reactivity of deaf individuals could reflect plastic changes in the early cortical processing of the stimulus. We found that deaf subjects were faster than hearing controls at detecting the visual targets, regardless of their location in the visual field (peripheral or peri-foveal). This behavioural facilitation was associated with ERP changes starting from the first detectable response in the striate cortex (C1 component) at about 80 ms after stimulus onset, and in the P1 complex (100-150 ms). In addition, we found that P1 peak amplitudes predicted the response times in deaf subjects, whereas in hearing individuals visual reactivity and ERP amplitudes correlated only at later stages of processing. These findings show that long-term auditory deprivation can profoundly alter visual processing from the earliest cortical stages. Furthermore, our results provide the first evidence of a co-variation between modified brain activity (cortical plasticity) and behavioural enhancement in this sensory-deprived population.

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Changes in Early Cortical Visual Processing Predict
Enhanced Reactivity in Deaf Individuals
Davide Bottari1,2*, Anne Caclin3,4, Marie-He ´le `ne Giard3,4, Francesco Pavani1,2
1Department of Cognitive Sciences and Education, University of Trento, Trento, Italy, 2Center for Mind/Brain Sciences, University of Trento, Trento, Italy, 3INSERM,
U1028; CNRS, UMR5292; Lyon Neuroscience Research Center, Brain Dynamics and Cognition Team, Lyon, France, 4University Lyon 1, Lyon, France
Abstract
Individuals with profound deafness rely critically on vision to interact with their environment. Improvement of visual
performance as a consequence of auditory deprivation is assumed to result from cross-modal changes occurring in late
stages of visual processing. Here we measured reaction times and event-related potentials (ERPs) in profoundly deaf adults
and hearing controls during a speeded visual detection task, to assess to what extent the enhanced reactivity of deaf
individuals could reflect plastic changes in the early cortical processing of the stimulus. We found that deaf subjects were
faster than hearing controls at detecting the visual targets, regardless of their location in the visual field (peripheral or peri-
foveal). This behavioural facilitation was associated with ERP changes starting from the first detectable response in the
striate cortex (C1 component) at about 80 ms after stimulus onset, and in the P1 complex (100–150 ms). In addition, we
found that P1 peak amplitudes predicted the response times in deaf subjects, whereas in hearing individuals visual
reactivity and ERP amplitudes correlated only at later stages of processing. These findings show that long-term auditory
deprivation can profoundly alter visual processing from the earliest cortical stages. Furthermore, our results provide the first
evidence of a co-variation between modified brain activity (cortical plasticity) and behavioural enhancement in this sensory-
deprived population.
Citation: Bottari D, Caclin A, Giard M-H, Pavani F (2011) Changes in Early Cortical Visual Processing Predict Enhanced Reactivity in Deaf Individuals. PLoS ONE 6(9):
e25607. doi:10.1371/journal.pone.0025607
Editor: Angela Sirigu, French National Centre for Scientific Research, France
Received March 18, 2011; Accepted September 8, 2011; Published September 29, 2011
Copyright: ? 2011 Bottari et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by a PRIN 2006 grant (Prot. 2006118540_004) from MIUR (Italy), a Galileo grant from Italian and French Universities, and a
PAT-CRS grant from University of Trento (Italy). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the
manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: davidebottari@gmail.com
Introduction
When coping with profound sensory deprivation, processing of
inputs from the intact modalities is critical. In profound deafness,
detection of changes in the environment and orienting of attention
occurs primarily through vision. Deaf individuals are faster at
detecting abrupt visual onsets [1,2,3,4], faster and more accurate
at discriminating motion direction of visual stimuli [5], and more
efficient in re-orienting attentional resources in visual space
[6,7,8]. These abilities have mainly, though not exclusively, been
documented for events occurring towards the periphery of the
visual field [9].
For profound deafness, it has been proposed that crossmodal
changes involving the visual modality occur beyond the early
processing stages, through the recruitment of higher-order visual
areas as well as the de-afferented auditory cortices [10]. Differ-
ences in brain activation between deaf and hearing individuals
have been found in the dorsal processing pathway (e.g., MT,
MST) in response to motion stimuli [11,12]. In addition, responses
to visual stimuli have been recorded outside visually responsive
brain regions, in the primary and secondary auditory cortices of
deaf individuals [13,14]. Recently Lomber and colleagues [15]
showed in deaf cats a causal relationship between the reorgani-
zation of portions of the auditory cortex and specific enhance-
ments of visual functions. Finally, two event-related potential
(ERP) studies in humans [5,16] found that the visual cortical
responses elicited by deaf and hearing individuals started to differ
from 180–200 ms latency, in the N1 component known to be
generated in extra-striate cortex [17] and sensitive to high-order
cognitive processes such as attentional orienting [18].
While ERPs are ideally suited to address the question of when
changes in sensory processing occur, the possibility to reveal effects
of crossmodal plasticity in early visual processing likely depends
upon the specific task demands. The observation of modulations
starting from the N1 component, for instance, could result from
the use of visual discrimination tasks [5]. Indeed, target
identification requires stimulus-feature binding before the response
choice: this in turn necessitates orienting of attention towards the
stimulus, which is known to modulate the N1 component of visual
ERPs [18]. A simple detection task would not imply such processes
and could reveal deafness-induced changes in earlier visual
processing stages. In the present study, we tested this hypothesis
by measuring reaction times and ERPs while deaf and hearing
adults performed a simple speeded detection task. We focused our
analyses on early (C1, P1) and later (N1) ERP components. In
addition, we analysed the relationship between response times and
visual ERP components, to highlight possible correlations between
behavioural changes and brain responses in the deaf. As a large
body of literature suggests that the deaf display enhanced visual
performance particularly when the task involves the peripheral
portion of the visual field [3,5], we asked our participants to detect
targets presented at either peri-foveal or peripheral eccentricities.
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Methods
Participants
Ten profoundly deaf individuals (mean age=33 years, SD=4,
range 18–50 year-old; mean years of education=14, SD=2.6; 6
female) were recruited at the National Association for Deaf (Ente
Nazionale per la protezione e assistenza dei Sordi, Trento, Italy)
and gave their informed consent to participate in the study. All
deaf participants had uncorrected bilateral profound hearing loss
(.90 dB), and acquired deafness within the first 3 years of age (8
had congenital deafness). All deaf participants were proficient sign-
language users (6 learned sign language as first language, the other
four had first a training based on Italian lip reading). Ten hearing
matched controls (mean age=29 years, SD=2.5, range 23–50
years old; mean years of education=16, SD=2.6; 5 females) were
also recruited to take part in the study. All participants had normal
or corrected-to-normal vision and were right-handed by self-
report.
The study was approved by the ethical committee at the
University of Trento (Italy), and written informed consent was
obtained from all participants prior to testing.
Stimuli and apparatus
Visual fixation was a white cross, presented at the centre of the
screen throughout the experimental session. The target was a
circle opened on left or right side that could be presented at eight
possible locations arranged on two invisible concentric circles
centred on visual fixation. The radius of the inner circle was 3
degrees of visual angle, and the radius of the outer circle was 8
degrees. Four possible target locations were on the inner circle and
four were on the outer (see Fig. 1a). Each location was placed
along the two diagonals of the screen, thus resulting in 4 possible
stimulus locations in the upper portion of the visual field, and 4 in
the lower. From now on we will refer to locations on the inner
circle as peri-foveal, and locations on the outer circle as peripheral.
Targets appearing at peripheral locations were corrected for the
cortical magnification factor [19]. Peri-foveal targets covered a
visual angle of 1.5u and peripheral targets of 2.6u. The widths of
the lines of the open circles were 1.5 mm and 2.4 mm for the peri-
phoveal and peripheral targets, respectively. All stimuli were
clearly presented suprathreshold. The luminance of the back-
ground was Y=23, x=.278, y=.301, that of the target stimulus
was Y=83.3, x=.277, y=.297, and that of the cue was Y=24.2,
Figure 1. Experimental protocol and behavioural results. (a) The target was a single circle opened on the left or right side, presented at one
of 8 possible locations. Peri-foveal targets were centred at 3u from fixation and covered a visual angle of 1.5u; peripheral targets were centred at 8u
from fixation and covered a visual angle of 2.6u (i.e., targets were corrected for the cortical magnification factor). Dotted place-holders and examples
of targets are shown in (a) for illustrative purposes only. (b) Each trial began with a warning signal (a red square covering 1.5u of visual angle,
presented for 500 ms). The inter-stimulus intervals (ISIs) between the warning signal and the target were, equiprobably, either 500 ms (short ISI) or
1800 ms (long ISI). The target appeared for 50 ms, at any of the 8 possible locations randomly. Participants were instructed to press the response
button as soon as possible. The inter-trial interval (ITI) ranged randomly between 1250 and 1750 ms. (c, d) Mean (of individual subjects medians)
response times (RTs) for deaf and hearing participants as a function of (c) target eccentricity (perifoveal or peripheral) and (d) ISI (short or long)
between the warning and the target. Deaf were overall faster than hearing controls. In addition, they showed no RT cost when reacting to peripheral
vs. perifoveal targets, unlike hearing controls (c). Finally, the ISI modulated the reactivity performance in the two groups (d).
doi:10.1371/journal.pone.0025607.g001
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x=.510, y=.301 (measured with Chroma Meter CS-100A,
http://www.konicaminolta.com/). All stimuli were presented on
a standard 17 inches monitor, with 10246768 pixels resolution,
and 60 Hz refresh rate. The experiment was programmed with E-
Studio 1.1.4.1, and run using E-Prime 1.1.4.1 (http://www.pstnet.
com).
Procedure
Participants sat at approximately 60 cm from the computer
monitor inside a sound-attenuated chamber and were instructed to
keep their head and eyes oriented towards fixation throughout
testing. The experimental session lasted approximately 60 min. All
hearing participants wore ear-plugs.
Each trial began with a warning stimulus consisting of a red
square covering 1.5u of visual angle and presented for 500 ms (the
visual fixation cross was superimposed on the red square, see
Fig. 1b). The warning stimulus was presented for several reasons:
first to give an attentional cue to the participants, second to
analyze the ERPs to an event placed at fixation, and third to
replicate our previous behavioural findings using the same
paradigm [3]. The inter-stimulus intervals (ISIs) between the
warning stimulus (offset) and the target (onset) were, randomly and
equiprobably, either 500 ms (short ISI) or 1800 ms (long ISI). The
visual target was presented randomly at any of the 8 possible
locations (i.e., 4 central and 4 peripheral) for 50 ms. Participants
were required to press as fast as possible the space bar of a
computer keyboard upon detection of the target. The inter-trial
interval (target offset to warning onset) ranged randomly from
1250 to 1750 ms. This task was designed on the basis of the
paradigm used by Bottari and colleagues [3], which showed RT
differences between deaf and hearing participants.
In case of anticipated responses (in the first 100 ms after
stimulus onset), the sentence ‘‘do not anticipate!’’ appeared on the
screen. Before data recording, participants completed a practice
block of 24 trials. The experimental session was divided into 10
blocks comprising 96 trials each and lasting approximately
5 minutes. Between blocks, participants were invited to take short
breaks. The experiment was a 2 by 2 by 2 factorial design, with
target eccentricity (peri-foveal or peripheral) and ISI (short or long)
as within-participant factors, and group (deaf individuals or
hearing controls) as between-participants factor.
Event-related potentials
The EEG was recorded (analog bandwidth: 0.1–200 Hz,
sampling rate: 1 kHz) from 34 scalp sites using the International
10–20 System extended montage (documentation in http://www.
easycap.de). Standard 10–20 sites were Fp1, Fp2, F7, F3, Fz, F4,
F8, T7, C3, Cz, C4, T8, T5 (P7), P3, Pz, P4, T6 (P8), O1, and O2.
Additional intermediate sites were FC5, FC1, FC2, FC6, TP9
(M1), CP5, CP1, CP2, TP10 (M2), PO3, PO4, PO9, Iz, and
PO10. All scalp channels were referenced to the nose. Horizontal
eye-movements were monitored with a bipolar montage from
electrodes at left and right outer canthi. To eliminate the artefacts
due to blinks, we performed an Independent Component Analysis
(ICA; [20,21]; runica version, implemented on EEGLAB running
in MATLAB, http://www.mathworks.com/). The ICA was
conducted on EEG epochs running from 1250 ms before the
warning signal onset to 2200 ms after (for short-ISI trials), or
3500 ms after (for long-ISI trials). After removal of blink effects,
trials including incorrect responses (anticipations, i.e. responses
before the target or in the 100 ms following it) or with signals
exceeding 100 mV at any electrode were excluded from averaging.
ERPs to the warning signal were averaged over a period of
2700 ms including 500 ms pre-stimulus (on average, 680 trials
after artefact rejection). ERPs to the targets were averaged
separately for each ISI and target location over a period of
1000 ms including 500 ms pre-stimulus (on average, 188 trials per
condition). The responses were corrected relative to a [2100,
0 ms] pre-stimulus baseline with respect to both warning signal
and target onsets. In addition, the ERPs to targets were also
corrected relative to a [2300, 2200 ms] baseline to assess possible
group differences in anticipatory activities occurring before the
target onset and their potential effects on the subsequent brain
responses. Finally, the ERPs were digitally filtered (low-pass filter
with a 30-Hz cut-off, slope 24db/octave). Scalp potential maps
were generated using spherical spline interpolation [22,23]. All
EEG data were analysed with the ELAN-pack software developed
at the Brain Dynamics and Cognition team in Lyon [24].
Statistical approach
Before comparing the cortical activity between groups, we
evaluated the emergence of visual evoked responses within each
group. To this purpose, we run a series of Wilcoxon tests across all
participants, comparing to zero the activity recorded at each time
sample. We performed this exploratory analysis for the ERPs to
the warning signal and to the targets, to select the time windows
and electrodes for the main analyses. The selected time windows
were thus: C1 [40–95 ms], P1 [80–150 ms] and N1 [150–
220 ms]. Main analyses were conducted on peak amplitude and
peak latency for the C1, P1 and N1 components, adopting mixed
ANOVAs and between-group t-tests. When necessary the Tukey
test was used for post-hoc comparisons.
Results
Enhanced visual reactivity in deaf relative to hearing
individuals
Response times (RTs) in deaf and hearing participants were
computed as the medians for each participant in each condition,
and analyzed using an ANOVA with Target Eccentricity (3u or 8u)
and Inter-stimulus interval (ISI) between warning signal and target
(short or long) as within-subject factors, and Group (deaf, hearing)
as between-subject factor. Deaf participants were overall faster
than hearing controls at detecting the visual targets (269610
(SEM) ms vs. 305610 (SEM) ms, respectively; F(1,18)=6.7,
p,0.02). In addition, while hearing controls showed a small but
consistent RT cost (4 ms; t(9)=2.6, p,0.03) when responding to
peripheral relative to peri-foveal targets, this cost was negligible in
deaf participants (0.4 ms; t,1). This resulted in a marginally
significant interaction between Group and Target Eccentricity
(F(1,18)=3.3, p,0.08; see Fig. 1c). Importantly, the faster RTs
found in the deaf group compared to hearing controls was not due
to a larger number of anticipation responses, as the amount of
trials in which the RTs were below 100 ms was comparable in the
twogroups(proportion of
0.000460.0002; Deaf=0.000960.0004;
Overall, these findings replicate previous reports [1,2,3] and
indicate that profound deafness can enhance reactivity to visual
events, particularly towards the periphery of the visual field.
An additional behavioural finding was the significant inter-
action between the warning-to-target ISI and Group factors
(F(1,18)=8.8, p,0.01; see Fig. 1d). Hearing controls were faster at
detecting targets at long than short ISI (285610 ms vs.
324610 ms, respectively; p,0.0002, Tukey HSD post-hoc test),
as predicted by the increased posterior probability for the long ISI
targets [25]. This ISI-related difference did not significantly
emerge in deaf individuals (26168 ms vs. 276612 ms). As a result,
reactivity difference between groups was substantial at the short
anticipationtrials:
t(18)=1.2,
Hearing=
p=0.2).
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ISI (p=0.02), and not significant at the long ISI (p=0.4, Tukey
HSD tests). Note however that a ceiling effect in deaf individuals
might explain this last result.
Brain responses to the central warning signal
The warning signal elicited ‘‘classical’’ visual ERP components
on posterior scalp areas in both groups, with however differences
between deaf and hearing participants in the latency, amplitude,
and morphology of the early visual responses (C1, P1, N1
components).
Both deaf and hearing participants exhibited a significant C1
component of negative polarity [26] within the 40–95 ms time
interval, with a maximum amplitude around Iz electrode (see
Fig. 2a). Its peak latency was significantly shorter in deaf
individuals (8062 ms) than in hearing participants (8762 ms;
t(18)=2.3, p,0.04). There was no significant group difference in
peak amplitudes (t(18),1.4). This difference in the C1 peak
latency between groups would indicate that the cortical processing
between deaf and hearing subjects already differs at the level of the
striate cortex [17]. An increasing number of evidence suggests that
visual attention might modulate the C1 component [27,28,29,30].
Nonetheless all the observed C1 modulations as a function of
attentional and/or perceptual load manipulations emerged as
amplitude changes. The present latency difference might reflect
changes in striate cortex activity or even in earlier processing
stages of deaf individuals’ visual pathway. In any case, this result
shows that differences in visual processing between deaf individ-
uals and hearing controls can emerge for a central visual event,
presented directly at fixation.
Following the C1 deflection, a prominent P1 component was
recorded over the posterior electrodes between 80 and 150 ms,
with a substantially different morphology between the two groups.
As shown in Fig. 2b, the two groups present a similar P1 profile
until about 125 ms, with a positive peak around 105 ms. Then,
unlike hearing controls, deaf displayed a second positive deflection
around 145 ms. This double deflection was observed in 7 out of 10
deaf participants (but only in 2 out of 10 hearing controls). To
assess the consistency of these different P1 profiles, we compared
between the two groups the mean amplitude of the P1 response in
two different latency ranges: 105 ms610 ms (first P1 peak), and
145 ms610 ms (second P1 deflection), over the subset of posterior
electrodes that better captured this activity (T5-T6-PO9-PO10-
TP9-TP10). As expected from the ERP waves in Fig. 2b, the mean
amplitude around the first P1 peak did not differ between the two
subjects’ groups (t(18),0.4), whereas around the second P1 peak
deaf individuals displayed a greater positive activity (0.960.6 mV)
Figure 2. Brain responses to the central warning signal in deaf subjects and in hearing controls. (a) Visual ERPs and topography of the
C1 component around its peak latency for each group. Arrows indicate the electrode (Iz) at which the ERP curves are shown. (Note that because the
C1 peak latency is later in hearing controls than in deaf participants, the emerging P1 can be seen for the controls on each side of the C1 in this
figure.) (b) P1 and N1 responses at 4 posterior electrodes (T5, PO9, T6, PO10, identified by arrows in the first potential map). The P1 components have
a similar profile in the two subjects groups until about 125 ms, then deaf subjects present a second positive deflection (145 ms) compared to hearing
controls. The prolonged positivity in deaf subjects (145–165 ms) is clearly seen in the spatiotemporal distribution of the responses (back view of the
head). By contrast, although the negative N1 component emerged earlier in control than in deaf subjects, there was no difference in morphology or
topography between the two subjects groups.
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compared to hearing controls (21.260.8 mV , t(18)=4.1,
p,0.05). The different morphology of the P1 complex between
groups is also evident in the spatiotemporal distribution of the
responses between 105 and 195 ms (see lower panel in Fig. 2b).
From about 135 to 165 ms, while hearing controls present
negative potential fields at the most occipital electrodes (emerging
N1 component), deaf individuals still show an enduring positive
activity centred over parietal electrodes. This corroborates further
our findings that cortical changes in deaf compared to hearing
individuals can be detected in early processing and for a centrally
displayed stimulus (see also [31] for a result in this direction,
showing ERP differences at the P2 level, between cochlear im-
planted patients and hearing controls for visual stimuli presented
at fixation).
Although visual inspection of the topographies (see Fig. 2b)
suggests that the N1 component emerged earlier in controls than
in deaf individuals around the occipital electrodes (e.g. PO9 and
PO10), its morphology was similar between the two groups, and
there was no significant difference in the peak amplitude (5.3 vs.
5.0 mV) or peak latency (177 vs. 180 ms, hearing controls vs. deaf
individuals respectively, both ts,1).
Brain responses to peri-foveal and peripheral targets
In paradigms using a warning signal prior to the occurrence of a
visual target, subjects may generate anticipatory activities in
sensory cortices before target appearance. To test for this
possibility, we measured in each subject the mean ERP amplitude
over the 200 ms preceding the target (relative to a baseline taken
over the [2300, 2200 ms] pre-stimulus period), averaged across
parieto-occipital electrodes(PO3-PO4-O1-O2-PO9-PO10-Iz).
This mean pre-stimulus activity did not differ from the baseline
for either (short or long) ISI condition in the control group. It was
however significantly different from the baseline in the deaf group
for the targets presented at short (but not at long) ISI (t(9)=4.5,
p,0.005). This result was further confirmed when comparing the
mean pre-stimulus amplitudes of the two groups in a two-way
ANOVA with the factors ISI and Group, with a significant
interaction between the two factors (F(1,18)=4.6, p,0.05): this
was caused by greater mean amplitude (sustained anticipatory
activity) in deaf than hearing participants when the target was
presented at short ISI (p=0.05, Tukey HSD post-hoc test; Fig. 3).
Because the different anticipatory activities in deaf and hearing
subjects (over the 200 ms preceding the target presentation) could
impact differently on subsequent brain responses, we kept the
same [2300, 2200 ms] pre-stimulus baseline for ERP component
analyses. For completeness, however, we also report the results of
the analyses when adopting a [2100, 0 ms] baseline, as for the
warning signal, in Table 1. The results remain globally unchanged
irrespective of the adopted baseline.
The C1 component elicited by the targets was observable in the
grand average responses, with the typical inversion of polarity for
upper vs. lower visual field stimulation [26]. However, it could not
be further analyzed because it was not well defined in every
participant.
Visual inspection of the P1 component to targets did not
reveal the clear biphasic morphology seen in the response to the
warning signal (see ERP waves in Fig. 4). This can be due to
the fact that P1 is usually sensitive to the visual contrast of the
stimulus: this contrast was much lower for the targets than for
the warning signal (red square). In addition, ERPs to the targets
(peri-foveal or peripheral) are averaged responses to stimuli
presented at four distinct locations (upper and lower, right and
left positions, see Fig. 1a) while the warning signal was always
delivered at fixation. Nevertheless, the spatiotemporal distribution
of the responses to targets (see topographies in Fig. 4a and Fig. 4b)
shows that the development of the P1 and N1 components in the
two subjects’ groups is similar to that observed in response to the
warning signal: deaf display a prolonged P1 relative to hearing
controls, with a prominent late phase distributed over parietal
scalp sites.
The peak latencies and amplitudes of P1 (determined within
the 80–150 ms time window across the posterior electrodes T5-
T6-PO3-PO4-P3-P4-Pz-O1-O2-TP9-TP10-PO9-PO10-Iz)
compared between the two groups using ANOVAs with Target
Eccentricity (peri-foveal or peripheral) and ISI (short or long) as
within-participant factors and Group as between-participant
factor. Analysis on P1 peak latency revealed a significant effect
of ISI (F(1,18)=8.4, p,0.01) due to a delayed P1 peak for targets
presented at long compared to short ISI, and a marginally
significant effect of Target Eccentricity (F(1,18)=4.2, p,0.06),
showing a tendency for delayed P1 peak for peripheral relative to
central targets. Most importantly, deaf participants showed a
significant peak latency delay (13065 ms) compared to hearing
controls (11565 ms, F(1,18)=4.8, p,0.05). There were no other
significant interactions involving the Group factor (Fs,1.5). In
particular, the absence of an ISI-by-Group interaction (F,1 with
both baseline corrections) suggested that the difference between
the two groups in anticipatory activities as a function of ISI
reported above had no effect on the P1 peak latency. ANOVA on
the P1 peak amplitude showed again a significant effect of ISI
(F(1,18)=13.3, p,0.01), indicating that participants generated
larger P1 amplitudes to targets presented at long compared to
short ISIs. The interaction between the ISI and Group factors
tended towards significance (F(1,18)=4.2, p,0.06). In particular,
deaf tended to show a larger difference between the P1 peak
amplitude in the long- compared to the short-ISI condition than
hearing controls. (Note that this interaction may have contributed
to the main effect of ISI reported above). Lastly, although it did
not reach statistical significance, there was a trend for a larger P1
amplitude in deaf (4.660.6 mV) than in hearing subjects
(3.260.6 mV, F(1,18)=2.5, p=1.3).
Analysis of the N1 component (assessed over the 150–220 ms
time window) using the same procedure as for the P1 response did
not reveal any significant effect of ISI or Group, nor interaction
involving the Group factor (all Fs,3.5).
were
Figure 3. Anticipatory activity recorded before target onset.
Deaf individuals show enhanced anticipatory activity (mean amplitude
over the 200 ms preceding target onset, with a 2300 to 2200 ms
baseline) compared to hearing controls for target presented at short ISI.
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Changes in early visual ERPs of the profoundly deaf
predict enhanced reactivity
Having demonstrated substantial early visual ERPs differences
between deaf and hearing subjects in particular in the P1 latency
range, we turned to investigate whether these different ERP
profiles could predict the observed behavioural differences in
terms of reactivity to the visual targets. To this aim, we separated
the RT distribution for each condition (target eccentricity and ISI)
and in each participant into four quartiles (Fig. 5b). Trials
belonging to each quartile were used to calculate four ERPs for
each participant. We could thus re-analyze the main responses to
the targets (anticipatory activities, P1, and N1 components) as a
function of the RT quartiles. The overall outcome of these
analyses is illustrated in Fig. 5.
As we reported above, deaf individuals showed enhanced
sustained activity prior to the appearance of the target in the short
ISI condition. Because we observed the larger behavioural
advantage for deaf compared to hearing subjects precisely for
the short ISI, we examined whether enhanced pre-stimulus activity
(within the 200 ms prior to target presentation, relative to a
[2300, 2200 ms] baseline; see Figure 3) could be related to the
RTs. A mixed ANOVA with ISI (short or long), Quartile (1, 2, 3,
4) and Group as factors did not reveal significant main effects of
Group or Quartile (F(1,18)=3, p,0.1 and F,1, respectively) on
pre-stimulus activity, nor significant interactions between Quartile
and Group, or between ISI, Quartile and Group (Fs,1; as
expected from the previous analysis on the anticipatory activity,
the ISI6Group interaction was significant F(1,18)=4.4, p=0.05).
These results thus indicate that, whatever the ISI the RTs did not
– at least directly – depend on anticipatory activities in visual areas
before target appearance (Fig. 5c).
A very different pattern of results emerges when considering the
peak amplitude of the P1 component as a function of ISI, Quartile,
and Group (note that for this analysis data were pooled across
target locations as this factor did not affect P1 or N1 latencies or
amplitudes in previous analysis). An ANOVA with ISI, Quartile,
and Group as factors revealed a significant main effect of ISI
(F(1,18)=13.7, p,0.01) and an interaction between ISI and
Group (F(1,18)=4.9, p,0.04) showing that deaf individuals
displayed an enhanced P1 peak amplitude for targets presented
at long than at short ISI (p,0.01, Tukey HSD post-hoc test). Most
importantly, the analysis revealed a significant main effect of
Table 1. Analyses (ANOVAs) of the ERPs to targets and their relationships with behavioural responses relative to a baseline taken
over the 100 ms preceding the target onset.
Brain responses to peri-foveal and peripheral targets
P1 component Factors - 2 within-subjects: Target Eccentricity (peri-foveal, peripheral), ISI (short, long)
- 1 between-subjects: Group
Peak latencyMain effects ISI: F(1,18)=8.7, p,0.01
Target Eccentricity: F(1,18)=6.5, p,0.02
Group: F(1,18)=5.7, p,0.03
No interactions involving GroupAll Fs,1
Peak AmplitudeMain effects ISI: F(1,18)=5.7, p,0.03
Interactions involving Group ISI6Group: F(1,18)=13.4, p,0.01
N1 componentFactors- 2 within-subjects: Target Eccentricity (peri-foveal, peripheral), ISI (short, long)
- 1 between-subjects: Group
Peak latency No main effects or interactions
involving Group
Target eccentricity: F(1,18)=3.7, p,0.08
Peak AmplitudeNo main effects or interactions
involving Group
All Fs,2.8
Changes in early visual ERPs of the profoundly deaf predict enhanced reactivity
P1 component Factors- 2 within-subjects: ISI (short, long), Quartile (1,2,3,4)
- 1 between-subjects: Group
Peak latencyNo main effects or interactions
involving Group
All Fs,1.8, n.s.
Peak AmplitudeMain effects ISI: F(1,18)=8.01, p,0.02
Quartile: F(3,54)=6.3, p,0.001
Interactions involving GroupISI6Group: F(1,18),1, n.s.
Quartile6Group: F(3,54)=3.5, p,0.02
Post-hoc ANOVAs for each group
with ISI and Quartile as factors
Deaf: Quartile F(3,27)=8.3, p,0.001 (linear contrast F(1,9)=15.7,
p,0.003)
Hearing: Quartile F,1.5, n.s. (linear contrast: F,1, n.s.)
N1 componentFactors - 2 within-subjects: ISI (short, long), Quartile (1,2,3,4)
- 1 between-subjects: Group
Peak latencyNo main effects or interactions
involving Group
All Fs,2.4, n.s.
Peak AmplitudeMain effectsQuartile: F(3,54)=14.7, p,0.0001 (linear contrast F(1,18)=22.1, p,0.0001)
No Interactions involving GroupAll Fs,1
Significant effects involving the group factor are highlighted with a grey background. Note that the results are similar to those obtained with a [2300, 2200 ms]
baseline reported in the main text.
doi:10.1371/journal.pone.0025607.t001
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Quartile (F(3,54)=5.1, p,0.01) and a significant interaction
between Quartile and Group (F(3,54)=3.7, p,0.02). A separate
ANOVA on the deaf data showed a significant effect of Quartile
(F(3,27)=7.9,p,0.001), and
(F(1,9)=19.5, p,0.003; see Fig. 5d). Conversely, this relationship
between ERP and behaviour was entirely absent in hearing
controls (for both baseline corrections, main effect of Quartile:
F,1.5; linear contrast: F,1).
In sum, RTs of deaf individuals slow down as P1 peak
amplitude decreases, with a clear linear relationship, whereas no
such relationship emerged in hearing controls. Figure 5f illustrates
these effects in the topography of the P1 component (around its
peak latency) as a function of quartiles. The same analysis on peak
latency did not show any significant effect of Quartile (F,1 for
both baseline corrections) nor any interaction involving the Group
factor (F,1.8, n.s. for both baseline corrections).
Finally, in both deaf and hearing participants the amplitude of
the N1 component predicted RTs. A similar relationship between
ERPs and behaviour emerged in the two groups (Fig. 5e; see also
Fig. 5g for the topography of the N1 peak as a function of
quartiles). ANOVA on the N1 peak amplitude showed a
significant main effect of Quartile (F(3,54)=10.7, p,0.0001) and
a linear pattern for this factor (linear contrast: F(1,18)=17.5,
p,0.001). However, no significant interaction involving the
Group factor was found (F,1 for both baseline corrections).
Thus, for both groups faster RTs were associated with an increase
in N1 peak amplitude. Similar to the P1 component, there was no
effect of the Quartile or Group factors on the N1 peak latency
(F,2.4, n.s. for both baseline corrections).
a significantlinearcontrast
Discussion
The current view on visual changes in profound deafness is that
they entail crossmodal plasticity resulting in modifications in late
visual processing [9,10]. Using a simple speeded detection task,
our study challenges this dominant view by providing evidence for
modulations of the brain responses in deaf individuals at very early
visual processing stages. Neural responses to visual events differed
between deaf and hearing participants already in the C1 ERP
component (50–95 ms) associated with striate cortex activity.
Furthermore, substantial differences between the two subjects’
groups emerged in the latency range of the P1 component
(80–150 ms) for both warning and target stimuli. The P1 complex
was prolonged in deaf relative to hearing participants, with a
biphasic morphology in 7 out of 10 deaf participants at least in the
responses to the (salient) warning signal. This finding thus sets the
initial hallmark for a divergence in visual processing between deaf
and hearing individuals at the first cortical stages, about 100 ms
before that documented in previous reports [5,16].
Our findings also provide the first evidence that this altered
dynamics of early visual ERPs may play a functional role in the
changes observed at the behavioural level in the deaf. In both
subjects’ groups, the speed of the upcoming response was linearly
related to the N1 peak amplitude. This finding corroborates
previous evidence in hearing individuals [32] showing a linear
relationship between RTs and N1 amplitude. Strikingly, our
results also revealed that the relationship between the electrical
brain response and reaction time dissociates between the two
groups, precisely in the early ERP component that differs the most
substantially between deaf and hearing individuals (i.e., the P1
complex). In the deaf group only, RTs decreased linearly with P1
peak amplitude . This calls for two remarks. First, it may seem
paradoxical that RTs in the Deaf were not related to P1 latency
(rather than amplitude) as this component was prolonged in this
group, resulting in a change in its peak latency. As noted above
however, this prolonged P1 complex stems more from a change in
P1 morphology rather than an actual delay of the response.
Second, the important point is that the ERP component that
predicts the behavioural measures is anticipated in deaf (P1)
compared to hearing subjects (N1) by a time globally correspond-
ing to the anticipation of the behavioural responses (it is
remarkable to note that the difference between the P1 and N1
peak latencies is around 50 ms, roughly the amount of difference
between the RTs of deaf and hearing subjects).
To sum up, changes in initial stages of visual processing predict
enhanced visual reactivity in deaf individuals. Thus, the reactivity
Figure 4. Brain responses to (a) peri-foveal and (b) peripheral targets. Upper panels show ERPs at T5 and T6 electrodes for the targets.
Lower panels show spatiotemporal distribution of the responses between 85 and 185 ms in each group. Like in the responses to the warning signal,
the P1 component is prolonged in deaf compared to hearing subjects, whereas the N1 is similar.
doi:10.1371/journal.pone.0025607.g004
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advantage in this sensory deprived population cannot be ascribed
to response preparation alone, but emerge also within the visual
system before response release. This is also corroborated by two
observations: (i) in behavioural measurements, the occasional
anticipatory responses were comparable between groups, and (ii)
in ERPs, the amplitude of preparatory activities did not predict
RT advantages (Fig. 5c).
One possible account for the early visual changes we observed
in deaf adults is linked to selective attention. Behavioural and
neural changes in the visual processing of the profoundly deaf have
been linked to changes in selective visual attention [5,6,9].
Although in our task orienting of attentional resources to the
target was not a mandatory stage before the response (unlike in
visual discrimination tasks), the visual onsets of the salient warning
Figure 5. Correlation between behavioural reactivity and brain responses. The figure depicts the main ERP components as a function of RTs
in deaf individuals and in hearing controls. (a, b) For each participant trials were sorted into 4 quartiles as a function of the response speed, from the
fastest (Qu1) to the slowest (Qu4), and ERPs were averaged within each quartile. (c) In both groups the mean amplitude of the pre-stimulus activity
(leftmost dashed area in (a) see text) was unrelated to the RTs. (d) By contrast, the peak amplitude of the P1 component (central dashed area in (a))
decreaseslinearly asa functionofRTs indeafparticipants,but not inhearingcontrols.(e) Finally, in bothgroups thepeak amplitudeoftheN1component
(rightmostdashedareain(a)decreasedmonotonicallyasafunctionofRTs.ThelowerpanelillustratestheseresultsbyshowingthetopographiesoftheP1
(f) andN1(g) components aroundtheir respective peaklatencies in bothsubjects’groupsas a function ofthe four quartiles: the potentialfields relatedto
P1 peak decrease with increasing RTs only for the deaf group, whereas N1 potentials decrease similarly in the two groups with increasing RTs.
doi:10.1371/journal.pone.0025607.g005
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signal and the targets surely captured the participant’s exogenous
attention. The changes in the P1 dynamics in the deaf may thus
reflect stronger exogenous attention capture in deaf compared to
hearing subjects. This is compatible with recent data showing that
exogenous attention can indeed affect the P1 ERP complex [33],
and that specifically the second phase of the P1 component could
be modulated by attentional capture [34].
Nonetheless, this attentional account cannot easily explain the
latency difference observed in the C1 component. Although an
increasing number of evidences suggests that attention and
perceptual load can modulate the C1 component [27,28,29,30],
all the effects reported were expressed by C1 amplitude changes.
As the C1 component reflects the initial stage of striate cortex
activity, the observed latency difference could represent a plastic
change in V1 or in an earlier visual stage in deaf individuals. As a
general remark, it should be noted that morphological changes at
various stages of the central nervous system as a consequence of
profound deafness could indeed have contributed to the early
changes we observed in visual ERPs. Recently Codina and
colleagues (2011) [35] found evidence for cross-modal plasticity
effects as early as at the retinal level (larger neural rim areas within
the neural optic nerve head, suggesting a greater number of retinal
ganglion cells in deaf individuals compared to hearing controls). In
addition, at the subcortical level, aberrant retinal projections to the
auditory thalamus and to the intermediate layers of the superior
colliculus have been described in deaf mice [36]. Although to our
knowledge, gray matter changes have not been documented in the
visual cortex of deaf humans [14], the existence of atypical white
matter fibers has been reported in deaf animals and deaf humans.
At the cortical level, recent studies using DTI (diffusion tensor
imaging) have reported increased anisotropy in the forceps major
of the corpus callosum in early deaf adults, suggesting increased
connectivity between visual cortices in these individuals [37,38].
These morphological changes, observed at several stages of the
visual pathway could be responsible for the modified dynamics of
the C1 (striate cortex) and P1 (extra-striate cortices) ERP
components in deaf compared to hearing subjects, without
claiming an attentional explanation.
A final important aspect of our findings is that the ERP
differences between deaf and hearing subjects were largely
comparable for visual events at 3 or 8 degrees of eccentricity
(targets) and, perhaps more surprisingly, even for visual events
delivered at fixation (warning signal). This result is compatible
with the observation of enhanced visual reactivity regardless of
stimulus eccentricity in deaf compared to hearing subjects [4], but
it contrasts with the widespread assumption that compensatory
changes of visual processing in the deaf should emerge selectively
for events appearing towards the periphery of the visual field.
While a special role of the visual periphery in profound deafness is
undisputed, and documented also by some aspects of the present
findings (see behavioural results in Fig. 1c), our results clearly
indicate that early changes in visual processing occur for events at
both central and peripheral portions of the visual field.
In conclusion, the present findings extend previous views on the
cross-modal effects of deafness on visual processing in various
ways. First, they show that auditory deprivation can alter visual
processing from the earliest cortical stages. Second, they reveal a
link between reactivity to visual events in profound deafness and
changes occuring at early stages of visual processing, thus
providing the first evidence of co-variation between modified
brain activity (cortical plasticity) and behavioural enhancement in
this sensory deprived population. This suggests that the stage of
visual processing which accumulates the critical perceptual
evidence to trigger the simple detection response may be
anticipated in deaf compared to hearing individuals. While
speculative this interpretation of the relation between brain
response and behavioural reactivity suggests that profound
deafness may not just re-structure the spatial processing of the
visual scene (with enhanced abilities for the periphery of the visual
field), but may also modify the timing of visual functions.
Acknowledgments
We wish to thank the Ente Nazionale Sordi (Trento), and particularly
Brunella Grigolli for coordinating the recruitment of the deaf participants.
We are grateful to Pierre-Emmanuel Aguera, Emmanuel Maby and
Massimo Vescovi for the technical support, Veronica Mazza for the help
during the EEG recordings, and David Melcher for comments on an
earlier version of this manuscript.
Author Contributions
Conceived and designed the experiments: DB FP. Analyzed the data: DB
AC M-HG. Wrote the paper: DB AC M-HG FP. Acquired the ERP data:
DB.
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