Neuroscience Letters 725 (2020) 134890

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Neuroscience Letters
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Research article

Visually guided eye movements reduce postural sway in dyslexic children T

a, b b a,b
José A. Barela *, Newton Tesima , Vitor da Silva Amaral , Gabriella A. Figueiredo ,
Ana Maria F. Barelab
a
Institute of Biosciences, São Paulo State University, Rio Claro, SP, Brazil
b
Institute of Physical Activity and Sport Sciences, Cruzeiro do Sul University, Sao Paulo, SP, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: Dyslexic children present poorer postural control performance than their peers, perhaps due to different patterns
Postural sway of eye movements. It has been shown that guided eye movements decrease magnitude of body sway in young
Vision and older adults, but there is no evidence whether the search for visual information that occurs during eye
Saccades movements affects postural control in dyslexic children. The aim of this study was to examine the use of guided
Dyslexia
eye movements and its pattern in the performance of postural control of dyslexic children during upright quiet
stance. Twelve children with dyslexia (10.8 ± 1.1 years old) and 12 non-dyslexic children (10.4 ± 1.5 years old)
participated in this study. All children were instructed to maintain an upright quiet stance for 60 s either fixating
on a target (fixation condition) displayed 1 m ahead in the center of a monitor at eye level, or performing eye
movements to follow a target displayed on one side of a monitor, then disappearing and reappearing im-
mediately on the opposite side with a frequency of 0.5 Hz (guided condition). Three trials for each condition
were registered. Body sway was measured with an IRED (OPTOTRAK) placed on the children’s back. Eye
movements were tracked using eye-tracking glasses (ETG 2.0 – SMI). Dyslexic children swayed with larger
amplitude under both fixation and guided conditions than non-dyslexic children. Both dyslexic and non-dyslexic
children reduced postural sway magnitude under the guided compared to the fixation condition. All children
were able to modulate eye movement according to the conditions (fixation and guided) and no difference in eye
movements was observed between dyslexic and non-dyslexic children. Eye movements are modulated similarly
based upon the visual conditions in dyslexic and non-dyslexic children, and dyslexic children are capable of
using available visual information during eye movements to improve postural control, though they do not equal
the performance of non-dyslexic children. Eye movement patterns seem not to be related to poor performance of
postural control in dyslexic children.

1. Introduction
Besides reading and writing difficulties, dyslexic children show
different performance in several tasks such as maintaining an upright
quiet stance [1–3], locomotion [4], and hand coordination [5,6]. Al-
teration in the visual system has been suggested as a potential cause of
dyslexia [7], and several studies have shown that eye movements
during reading are abnormal in dyslexic children [8–10]. Usually,
dyslexic children employ a higher number and longer fixations, a
higher number and smaller saccades and a higher number of retro-
saccades when reading compared to non-dyslexic children [10]. How-
ever, different patterns of eye movements in dyslexic children have
been observed in motor tasks other than reading, such as fixating a
target [11] and visual search [10], with dyslexic children showing,
respectively, a higher number of saccades and retro-saccades, and
during upright stance maintenance [12], with dyslexic children also
showing a higher number of saccades and retro-saccades than their non-
dyslexic peers. Results from all those studies show that different pat-
terns of eye movement are more likely comorbidity than a specific
reading cause.
The relationship between the performance of postural control and
eye movements has motivated many studies with different populations.
A striking finding is that eye movements guided to a specific target
reduce body oscillation in young [13,14] and older adults [15], and
even in different-aged children [16]. Body sway attenuation is even
more remarkable in more demanding stance conditions [17]. Thus, it
has been suggested that conditions with visually guided eye movement
seem to require postural stability to allow accurate gaze shifts. It has
been suggested that such improvement is due to the necessary reduc-
tion in postural sway to allow accurate eye positioning, which is

⁎
Corresponding author at: Institute of Biosciences, UNESP, Av. 24-A, 1515, Bela Vista, Rio Claro, SP, 13506-900, Brazil.
E-mail address: jose.barela@unesp.br (J.A. Barela).

https://doi.org/10.1016/j.neulet.2020.134890
Received 2 September 2019; Received in revised form 28 February 2020; Accepted 3 March 2020
Available online 04 March 2020
0304-3940/ © 2020 Elsevier B.V. All rights reserved.
J.A. Barela, et al.
denominated supra-postural task [13]. Improvement on postural con-
trol performance was also explained by the use of afferent and efferent
copy mechanisms [18]. In this case, the afferent mechanism for the
visual stabilization during upright quiet stance seeks to minimize
changes of the projected image on the retina, while the efferent me-
chanism seeks to attenuate body sway in an attempt to connect pre- and
post-eye position of the scene views to provide a more accurate spatial
orientation toward the target location. More recently, it has been sug-
gested a synergetic model, in which both oculomotor and postural
dynamics should be controlled conjointly, leading to a higher cognitive
involvement and further postural control sway reduction [19].
Despite the importance and the interplay between eye movements
and postural control mechanisms to improve postural control perfor-
mance in adults, knowledge of how these mechanisms are used by
children is limited. For instance, children as young as 6 years old can
use visually guided eye movement to improve stability during upright
stance but still show different eye movement patterns from older chil-
dren [16]. Moreover, after the first decade of life, both postural control
and eye movement parameters seem to become stabilized with little
improvement [16]. Recently, a few attempts have been made to obtain
information about eye movement and postural control in children with
disabilities. For instance, Bucci and colleagues [20] observed that
children with attention deficit and with neurodevelopmental disorders
[21] were able to use saccadic eye movements to improve postural
control during upright stance. A direct verification of eye movement
saccades and postural control performance is scarce, with a solo study
showing postural control performance improvement in dyslexic (and
other) children [21]. Moreover, studies have shown that dyslexic chil-
dren can perform eye movement similarly to non-dyslexic children in
visual search tasks, though with a few abnormalities, suggesting that
dyslexic children have an immature visual system affecting ocular
motor saccade [10,22]. Likewise, when reading a text or nonsense
character sequence, dyslexic children use different eye movement pat-
terns, despite poorer postural control performance compared to their
non-dyslexic peers [12].
These inconsistent results leave many questions regarding eye
movements and postural control performance in dyslexic children un-
answered. Moreover, the use of visually guided eye movements to
control posture might indicate that the requisite eye movement me-
chanisms are present in dyslexic children, which could advance our
knowledge regarding the relationship between visual information and
motor task performance in dyslexic children. Therefore, the aim of this
study was to examine the effect of guided eye movements on the per-
formance of postural control and the patterns of eye movement of
dyslexic children during upright stance. We hypothesized that dyslexic
children could use guided eye movements to reduce the magnitude of
postural sway, and they would use a higher number of fixations and
saccades compared to non-dyslexic children.
2. Methods
2.1. Participants
Twelve dyslexic children (age = 10.8 ± 1.1 years, range 9.0–12.3
years, 5 girls and 7 boys) and 12 age- and sex-matched non-dyslexic
children (age = 10.4 ± 1.5 years, range 8.9–12.8 years) participated in
this study. It is important to note that we included children’s age be-
cause both postural control [23] and eye movement parameters [16]
seem to become stabilized with little improvement at the end of the first
decade of life. Dyslexic children were recruited from the Brazilian
Dyslexic Association, where each one had undergone a complete eva-
luation and dyslexia screening assessment including neurological, psy-
chological, and phonological capabilities. Non-dyslexic children were
recruited from the local community. All children’s participation in the
study was conditional upon permission being given by parents, who
signed an informed consent form. The local Institutional Review Board
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Neuroscience Letters 725 (2020) 134890
approved both the study procedures and the informed consent form.
2.2. Procedures
Each participant was brought to the laboratory and, after being
acquainted briefly with the laboratory facilities, was prepared for the
experimental procedures. Initially, participants were asked to wear an
eye movement tracking system (Eye Tracking Glasses – ETG 2.0 SMI) to
capture eye displacement (iViewETG SMI – version 2.7.1). Wearing the
eye tracking glasses, calibration procedures were performed following
the device requirements whereby the participant had to fixate on a
calibration matrix with known targets. An IRED marker (Optotrak
Certus – NDI) was then fixed on the participant’s back (around the 6th
thoracic vertebra) to measure body sway in the anterior-posterior,
medial-lateral, and vertical directions.
After this preparation, participants were instructed to stand still in
an upright position inside a small room (1 m × 1 m × 1.8 m – width,
depth, and height), all walls black, preventing any near environment
visual influence. Participants stood with their feet parallel and spaced
apart at pelvis width, letting their arms hanging at their sides, as they
performed under two experimental conditions, fixation and guided eye
movement. Under the fixation condition, participants had to fixate on a
target (1.5-cm diameter black circle) displayed in the center of a
monitor (LG, model Flatron L1753T8) with white background 1 m
distant in the front wall of the room and at the eye level of the parti-
cipant. In the guided eye movement condition, participants had to di-
rect and fixate on a target that appeared and disappeared on the left and
right sides of the monitor (9.75 cm from the monitor center), com-
prising a visual angle of 11 degrees in the horizontal plane, at a fre-
quency of 0.5 Hz, controlled by specific software (Flash Mx, version
6.0) [15,17]. This target distance and visual angle usually require only
eye movements, with no head displacement [14].
Each condition was repeated three times, with each participant
performing a total of six trials. Each trial lasted 60 s and the trials were
randomized in blocks of two trials (one for each condition). Each trial
was started after the participant had assumed the upright stance with
data from the eye tracking and Optotrak systems being synchronically
acquired at 120 and 100 Hz, respectively.
2.3. Data analysis
Data for body sway were filtered using a second-order digital
Butterworth filter with a cutoff frequency of 5 Hz. Medial-lateral (ML)
and anterior-posterior (AP) mean sway amplitude and frequency within
a trial were then calculated. Mean sway amplitude, which corresponded
to the variance of the trunk spatial coordinate values and which can be
used to estimate trunk stability, was obtained by removing a linear
trend from each data point of the time series and then calculating the
standard deviation of the time series. Mean sway frequency was cal-
culated by performing a Fast Fourier Transform (FFT) of the individual
ML and AP time-series data and obtaining the correspondent frequency
to half of the total power spectrum area for each trial. All these pro-
cedures were performed employing specific routines written in Matlab
(MathWorks, Inc.).
Eye movement analyses were performed using the specific software
of the eye tracking system (BeGaze, SMI, version 3.7), which auto-
matically detected both the onset and the end of each saccade with a
built-in saccade detection algorithm (employing the parameter of
minimum duration of 22 ms, peak velocity of 40 degrees/s and minimal
fixation of 50 ms, and the start and end as 20 % and 80 % of the saccade
lenght, respectively). The onset and end of each saccade identified by
the algorithm were visually inspected and verified by one of the in-
vestigators. Based on each saccade detection, the following variables
were obtained: number of fixations (events in which the eyes were kept
in a specific area) and number of saccades (events in which the eyes
moved from one fixation point to another). These variables were
J.A. Barela, et al.
computed for both fixation and guided conditions. Finally, for the
guided eye movement condition, the duration, amplitude, and velocity
of saccades were also obtained. Because children performed three trials
in each experimental condition, the variables for both postural control
and eye movement were averaged for each condition and each parti-
cipant.
2.4. Statistical analysis
After testing the normality and homogeneity of variance assump-
tions, six analyses of variance (ANOVAs) with group (dyslexic and non-
dyslexic) and condition (fixation and guided eye) as factors, with the
last treated as a repeated measure, were performed for each of the
following dependent variables: Mean sway amplitude in the ML and AP
directions, frequency in the ML and AP directions, number of fixations,
and number of saccades. For the guided condition specifically, three
ANOVAs with group as a factor were performed for each of the fol-
lowing dependent variables: Duration, amplitude, and velocity of sac-
cades. These analyses were performed using the SPSS software with the
level of significance set at p < 0.05.
3. Results
3.1. Postural control
Fig. 1 shows the mean sway amplitudes for the dyslexic and non-
dyslexic groups under both the fixation and guided eye conditions. The
ANOVA for the ML direction (Fig. 1A) showed no effect for group (F1,22
= 0.95, p > 0.05) or condition (F1,22 = 0.61, p > 0.05), and no in-
teraction between group and condition (F1,22 = 2.39, p > 0.05). For the
anterior-posterior direction (Fig. 1B), ANOVA showed effects for group
(F1,22 = 5.71, p < 0.05) and condition (F1,22 = 5.59, p < 0.05), but no
interaction between group and condition (F1,22 = 0.36, p > 0.05).
Dyslexic children swayed with larger magnitude than non-dyslexic
children in the AP direction, and both groups reduced the sway mag-
nitude under the guided condition compared to the fixation condition in
this direction.
Fig. 2 shows the mean sway frequencies for the dyslexic and non-
dyslexic groups under both the fixation and guided conditions. For the
ML direction (Fig. 2A), ANOVA showed no effect for group (F1,22 =
3.58, p > 0.05) or condition (F1,22 = 0.39, p > 0.05) and no interaction
between group and condition (F1,22 = 0.08, p > 0.05). For the AP di-
rection (Fig. 2B), ANOVA showed an effect for group (F1,22 = 9.61,
p < 0.005), no effect for condition (F1,22 = 0.83, p > 0.05), and no
interaction between group and condition (F1,22 = 0.30, p > 0.05).
Dyslexic children swayed with a lower mean frequency than non-dys-
lexic children in the AP direction.
Fig. 1. Mean ( ± SD) values of mean sway amplitude (MSA) in the medial-lateral (A) and anterior-posterior (B) directions in the fixation and guided eye conditions
for both dyslexic and non-dyslexic children.
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Neuroscience Letters 725 (2020) 134890
3.2. Eye movement
Fig. 3 shows the time series of the eye movements in the vertical and
medial-lateral directions under the fixation and saccadic conditions.
Both dyslexic and non-dyslexic children were capable of changing the
patterns of eye movement according to the visual task they had to
perform. Under the fixation condition, the eyes were kept looking in
one direction with small displacement, as happens regularly when fix-
ating on a target or environmental scene (Fig. 3A and 3C). Contrariwise,
when participants were asked to follow the target presented on opposite
sides of the monitor, the eyes followed its apparent movement ac-
cordingly in the medial-lateral direction (Fig. 3B) and also with greater
amplitude in the vertical direction (Fig. 3D).
Fig. 4 shows the number of fixations for the dyslexic and non-dys-
lexic groups under both the fixation and guided conditions. ANOVA
showed no effect for group (F1,22 = 0.04, p > 0.05), an effect for
condition (F1,22 = 97.61, p < 0.001), and no interaction between group
and condition (F1,22 = 0.03, p > 0.05). Both dyslexic and non-dyslexic
children made more fixations in the guided condition than in the
fixation one.
Fig. 5 shows the number of saccades for the dyslexic and non-dys-
lexic groups under both the fixation and guided conditions. ANOVA
showed no effect for group (F1,22 = 0.32, p > 0.05), an effect for
condition (F1,22 = 35.59, p < 0.001), and no interaction between group
and condition (F1,22 = 0.51, p > 0.05). Both dyslexic and non-dyslexic
children made more saccades under the guided than the fixation con-
dition.
Table 1 presents the duration, amplitude, and velocity of saccades
for both dyslexic and non-dyslexic groups under the guided condition.
Respective ANOVAs showed no group effect for duration (F1,22 = 1.87,
p > 0.05), amplitude (F1,22 = 0.71, p > 0.05), or velocity (F1,22 =
0.89, p > 0.05). Dyslexic and non-dyslexic children performed the
saccades with the same pattern under the guided condition.
4. Discussion
The aim of this study was to examine the effect of guided eye
movements on the performance of postural control and the patterns of
the eye movements of dyslexic children during upright stance. We hy-
pothesized that dyslexic children could use guided eye movements to
reduce the magnitude of postural sway, and they would use a higher
number of fixations and saccades compared to non-dyslexic children.
Overall, the results partially supported these hypotheses. Dyslexic
children, despite showing poorer performance of postural control per-
formance than non-dyslexic children, used guided eye movements to
improve and reduce their sway magnitude in the AP direction com-
pared to the fixation condition. However, no differences in eye move-
ment pattern were observed between dyslexic and non-dyslexic
J.A. Barela, et al. Neuroscience Letters 725 (2020) 134890

Fig. 2. Mean ( ± SD) values of mean sway frequency in the medial-lateral (A) and anterior-posterior (B) directions in the fixation and guided eye conditions for both
dyslexic and non-dyslexic children.

Fig. 3. Exemplar time series of a dyslexic child’s eye movement in the fixation (A, C) and guided (B, D) conditions, in the medial-lateral (A, B) and vertical (C, D)
directions.

Fig. 4. Mean ( ± SD) of the number of fixations in the fixation and guided Fig. 5. Mean ( ± SD) of the number of saccades in the fixation and guided
conditions for both dyslexic and non-dyslexic children. conditions for both dyslexic and non-dyslexic children.

4
J.A. Barela, et al.
Table 1
Mean ( ± SD) of duration, amplitude, and velocity of saccades in the guided
condition for both dyslexic and non-dyslexic children.
Dyslexic Non-dyslexic
Duration (ms) 57.89 ± 14.37 71.47 ± 31.15
Amplitude (deg) 6.58 ± 2.39 5.79 ± 2.18
Velocity (deg/s) 147.6 ± 68.2 160.7 ± 68.1
children.
Our results showed that non-dyslexic and dyslexic children were
capable of using guided eye movements to improve the performance of
postural control when they had to perform eye movements to watch an
appearing target. The reduction of body sway magnitude had already
been observed in young [13,14] and older [15] adults and healthy [16]
and neurological children, including dyslexic (Bucci et al., 2018). Thus,
our results corroborate previous results (Bucci et al., 2018) showing
that both groups of children reduced their body sway magnitude in the
AP direction when they performed guided eye movements compared to
the fixation condition. Interestingly, reduction in body sway occurred in
the AP but not in the ML direction [13,14], similarly to adults. As
mentioned previously, it has been suggested that such reduction in
body sway would be either due to the effect of a supra-postural task
[13] or due to the afferent and efferent mechanisms [18]. However, it
might be that the imposition of the guided eye movement would en-
force to function synergistically in such way that oculomotor and pos-
tural dynamics would be taken together to achieve the task goal [19].
Despite these possible explanations, our results showed that even dys-
lexic children can use such mechanisms to modulate postural sway
according to the visual conditions.
More interesting was the observation that even when reducing body
sway magnitude, dyslexic children still displayed larger body sway
magnitude in the AP direction than non-dyslexic children. Poor per-
formance of postural control, such as larger body sway, by dyslexic
children has been observed with no vision [24] and with visual fixation
and oscillation, in a visual stationary scenario [21] and in the moving
room [1,3], and the present results confirm previous findings. Based
upon the larger sway magnitude when using visual information to
control body sway, it has been suggested that poor performance of
postural control in dyslexic children is related to how sensory in-
formation is acquired from the environment and used to produce pos-
tural responses. Our results indicate that guided eye movements can be
used to improve their postural control either by providing additional
sensory cues or by enforcing the central nervous system to use such
information linked to postural dynamics. However, even with such
improvement, the postural control performance of dyslexic children is
still inferior to their non-dyslexic peers, as they present greater body
sway magnitude.
Larger postural sway magnitude has been suggested to occur in
dyslexic children because they are not capable of extracting most of the
informational sensory cues used to accurately indicate body sway dy-
namics so as to produce appropriate muscle activity to reduce and/or
maintain a desirable postural orientation [1,3,24]. Interestingly, we
observed that non-dyslexic children sway with a higher mean frequency
than dyslexic children. Similar results were observed when adults re-
duced postural sway during saccadic eye movements, indicating that
further control of body sway also relates to efforts to refine body os-
cillation and increase the central control of postural adjustments
[14,17]. Our results show that dyslexic children employed fewer cor-
rections in body sway under both fixation and guided conditions than
non-dyslexic children, revealed by their lower mean frequency of sway.
Despite such a difference, we did not observe any visual effect under
either the fixation or guided conditions in the body sway of dyslexic and
non-dyslexic children. The lack of body sway modulation between these
two visual conditions in children is an issue that requires further
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Neuroscience Letters 725 (2020) 134890
investigation.
Unlike sway magnitude, no difference was observed in eye move-
ment patterns between dyslexic and non-dyslexic children, despite
children modulating their eye movements based upon the visual con-
dition. Dyslexic and non-dyslexic children both showed more fixation
and saccadic occurrences under the guided condition than under fixa-
tion. When required to fixate on a target appearing and disappearing on
the monitor’s left and right sides, children followed the instructions and
performed eye movements to the target, whereas they performed less
fixations and saccadic movements compared to the guided eye move-
ment condition when the target was stationary in the center of the
monitor.
Several studies have shown different eye movement patterns in
reading [8–10,22] and during upright stance [12] tasks in dyslexic
children. Our hypothesis was that differences in eye movement patterns
would also be observed in dyslexic children under fixation and saccadic
visual conditions. However, this hypothesis was refuted, as there was
no difference in eye movement between dyslexic and non-dyslexic
children under either visual condition. Moreover, we did not observe
any difference when dyslexic children had to perform eye saccadic
movements to the target’s changing position, as no difference was ob-
served in the duration, amplitude, or velocity between dyslexic and
non-dyslexic children when performing saccadic movements toward the
appearing/disappearing target. We have recently shown that dyslexic
children employ smaller pro-saccade amplitudes and more saccadic
movements when reading [25], but it seems that such differences are
not observed when a specific target is presented. More saccades per-
formed by dyslexic children were observed during fixation except in
reading set up conditions [8,11], which might change postural demands
and affect eye movement patterns. Interestingly, when dyslexic children
performed visual search [10] and Landolt reading [12], no saccade
different patterns were observed between dyslexic and non-dyslexic
children. Thus, it seems that eye movement patterns are task-dependent
and, definitely, more detailed studies and analyses should be employed
to further our understanding of the use of saccadic eye movements by
dyslexic children under different visual conditions. Such suggestion is
in agreement with recent results in which children with neurodeve-
lopmental disorders showed poor eye movement patterns in more dif-
ficult postural tasks [21]. Definitely, this issue needs to be further in-
vestigated.
In summary, dyslexic and non-dyslexic children use saccadic eye
movements to improve their performance of postural control, reducing
their sway magnitude compared to a fixation visual condition. Despite
using saccadic eye movements, dyslexic children still sway with larger
magnitudes than non-dyslexic children. Finally, both dyslexic and non-
dyslexic children modulate eye movements according to visual condi-
tions (i.e., fixation and guided conditions), and no differences were
observed in this respect between dyslexic and non-dyslexic children.
Declaration of Competing Interest
None.
Acknowledgment
This work was supported by São Paulo State Research Foundation
(FAPESP - #2015/26637-0).
The authors are grateful to the children who participated in this
study and their parents.
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