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Neuroscience Letters 584 (2015) 292–295

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Neuroscience Letters
journal homepage: www.elsevier.com/locate/neulet

Short communication

Saccadic and smooth pursuit eye movements attenuate postural


sway similarly
Sérgio Tosi Rodrigues a,b,∗ , Paula Fávaro Polastri a , Jamile Cristina Carvalho a ,
José Angelo Barela c,d , Renato Moraes e , Fabio Augusto Barbieri a,f
a
Laboratory of Information, Vision, and Action (LIVIA), Department of Physical Education, Faculty of Sciences, University of São Paulo State,
Bauru Campus, Av. Luiz Edmundo Carrijo Coube, 14-01, Vargem Limpa, 17033-360 Bauru, SP, Brazil
b
Graduate Program in Design, Faculty of Architecture, Arts, and Communication, University of São Paulo State, Bauru Campus, Bauru, SP, Brazil
c
Department of Physical Education, Institute of Biosciences, University of São Paulo State, Rio Claro Campus, Rio Claro, SP, Brazil
d
Graduate Program in Human Movement Science, Institute of Physical Activity and Sport Sciences, Cruzeiro do Sul University, São Paulo, SP, Brazil
e
School of Physical Education and Sport at Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil
f
Graduate Program in Motricity Sciences, Institute of Biosciences, University of São Paulo State, Rio Claro Campus, Rio Claro, SP, Brazil

h i g h l i g h t s

• Saccadic eye movement and smooth pursuit reduce body sway compared to fixation.
• Different visual frequencies affect equally the body sway in both eye movements.
• Saccadic eye movements are anticipated, favoring a feed-forward modulation.
• Smooth pursuit eye movements appear to be controlled in an on-line manner.

a r t i c l e i n f o a b s t r a c t

Article history: Saccadic eye movements reduce body sway, yet visually pursuing a moving dot seems to increase body
Received 21 July 2014 sway. However, how these two types of eye movements affect postural control remains ambiguous,
Received in revised form 23 October 2014 particularly for smooth pursuit eye movements. The aim of this study was to examine the effects of
Accepted 27 October 2014
saccade and smooth pursuit eye movements on body sway magnitude during low and high frequencies.
Available online 4 November 2014
Ten young adults (19.5 ± 1.9 years) participants were required to stand upright, barefoot for 70 s using a
bipedal stance, with feet hip width apart, fixating or pursuing a target that was displayed on a monitor
Keywords:
positioned 100 cm away from their eyes. Each participant performed three trials using both types of
Postural control
Saccades
eye movements, in particular, slow and fast saccades, and slow and fast smooth pursuit movements.
Smooth pursuit Body sway was obtained using reflective markers attached to a participant’s head and trunk, which
Eye movements were recorded by two video cameras. The results indicated that body sway was reduced during both
saccadic eye movements and smooth pursuit movements when compared to fixation, independent of
visual frequencies. These results suggested similarities in the control of saccades and smooth pursuit on
postural control.
© 2014 Elsevier Ireland Ltd. All rights reserved.

1. Introduction especially when combined with a wide support base and a high
frequency of visual stimuli [2]. Saccade conditions seem to require
Body sway is attenuated while performing saccadic eye move- greater postural stability to spatially allow more accurate gaze
ments when compared to a fixed gaze on a static target [1], shifts, indicating a functional integration of posture and gaze con-
trol [1], which is attained by afferent and efferent copy mechanisms.
The afferent mechanism for the visual stabilization of posture tries
to minimize the changes of the projected image on the retina; [3]
∗ Corresponding author at: Laboratory of Information, Vision, and Action (LIVIA),
whereas, the efferent copy mechanism tries to attenuate body sway
Department of Physical Education, Faculty of Sciences, University of São Paulo State,
Bauru Campus, Av. Luiz Edmundo Carrijo Coube, 14-01, Vargem Limpa, 17033-360
in an attempt to connect pre- and post-saccadic views of the scene
Bauru, SP, Brazil. Tel.: +55 14 3103 6082x7617; fax: +55 1431036071. [4], which favors the spatial accuracy of the saccade with respect
E-mail address: srodrigu@fc.unesp.br (S.T. Rodrigues). to the target location. Despite all the importance of saccades, this

http://dx.doi.org/10.1016/j.neulet.2014.10.045
0304-3940/© 2014 Elsevier Ireland Ltd. All rights reserved.
S.T. Rodrigues et al. / Neuroscience Letters 584 (2015) 292–295 293

is not the only important eye motion, since sports and other activ- 1407, 60 Hz) positioned above the monitor. After data collection,
ities also require eye movements to track (pursuit) objects moving videos were analyzed to reconfirm the required eye movements
in the environment [5]. for each condition.
Although, saccadic eye movements reduce body sway [1,2,6,7], Body sway was measured using reflective markers attached
visually pursuing a moving dot systematically increases body sway to the participant’s head (posterior part, just above the occipital
[8]. The different effects between these two eye movements on bone) and trunk (between the scapulae). The reflective mark-
body sway may be attributed to the suppression of vision dur- ers were recorded using two video cameras (Sony DCR DVD 205
ing saccades, as well as the continuous participation of smooth and 405) during each task with a sample frequency of 60 Hz. The
pursuit eye movements in the visual control of posture [8] in a non- recorded video images of all trials were cropped, tridimensionally
stationary spatial frame of reference [9]. In addition, while saccade reconstructed, and analyzed based on the space coordinates of the
is a discrete movement that quickly changes the orientation of the tracked markers (Software APAS, Ariel Dynamics, version 1).
eyes, translating the object of interest’s image to the fovea, smooth A trial started 10 s after the subject and experimental condition
pursuit is a continuous movement that rotates the eyes to com- commenced. The following dependent variables were obtained:
pensate for the motion of the visual object, minimizing blur [10]. trunk and head mean sway amplitude in the anterior–posterior
Furthermore, saccades have their magnitude established before the (AP) and medial-lateral (ML) directions as the standard deviation in
movement begins without the possibility of corrections during its direction for the positional data throughout the trial; mean velocity
course; whereas smooth pursuit movements are feedback-based in the AP and ML directions using displacement in each direction
such that their initiation depends on target motion. Smooth pursuit divided by the time of each trial; trunk and head total displacement
eye movement’s velocity is linearly related to the target’s velocity calculated from the total trajectory length of the respective marker
[4,11]. during the trial; and the sway area as the 95% confidence ellipse
How these two eye movements affect postural control is still a area of the data. Furthermore, the trunk and head mean and 95% of
matter of debate, particularly for smooth pursuit eye movements. the frequency were calculated by employing spectral analysis of the
Therefore, the aim of this study was to examine the effects of sac- position time series separately in each direction (Matlab software
cade and smooth pursuit eye movements on body sway magnitude version 7.10, Mathworks).
during low and high frequencies. Considering, previous studies For each dependent variable, a one-way analyses of variance
[1,2,8], it was hypothesized that body sway will decrease during (ANOVAs) with the 5 conditions (fixation, slow saccade, fast sac-
saccades and increase during smooth pursuit movements, when cade, slow smooth pursuit, and fast smooth pursuit) treated as a
compared to fixation control conditions. Different stimuli frequen- repeated measures factor was performed. Tukey’s post-hoc tests
cies were expected to clarify whether changes in task demands were carried out to identify the significant differences when the
interact with effects of distinct eye movements on postural control main effect was identified. All the analyses were performed using
performance. SPSS (version 15.0) and the significance level was set at 0.05.

3. Results
2. Material and methods
The ANOVA indicated significant differences only for the trunk
Ten young adults (19.5 ± 1.91 years) participated in this study.
and head mean sway amplitude in the AP direction (trunk:
All participants were blinded to the purposes of the experiment and
F4,36 = 3.99, p = 0.05 | head: F4,36 = 4.67, p = 0.02), total displace-
reported no history of falls, dizziness, or postural instability. One
ment (trunk: F4,36 = 5.15, p = 0.01 | head: F4,36 = 4.52, p = 0.02), and
participant wore corrective glasses during the experiment. Prior
mean frequency in the AP direction (trunk: F4,36 = 3.34, p = 0.04
to experimental procedures, participants signed a written consent
| head: F4,36 = 2.77, p = 0.05). No statistical significant differences
form approved by the local ethics committee.
were found for any other variable tested.
Participants were required to stand upright, barefoot for 70 s
Trunk and head mean sway amplitude in the AP direction and
using a bipedal stance with feet hip width apart, fixating or pursu-
total displacement were significantly affected by the visual condi-
ing a target that was displayed in a monitor positioned 100 cm away
tion (Table 1). Specifically, post-hoc analysis indicated significantly
from their eyes. The target was a red dot 2 cm in diameter on a white
larger trunk and head sway during eye fixation when compared to
background with a subtended visual angle of approximately 1.15◦ .
the other four conditions. However, mean sway trunk and head fre-
The total distance between right and left side targets comprised
quencies, in the AP direction, were decreased during the fixation
a visual angle of 11◦ to avoid head movements [1]. Stimuli were
condition when compared to the other four conditions (Table 1).
generated by the software Flash Mx (Macromedia) and presented
on a LCD monitor (37.5 cm × 30 cm, LG, Faltron L1952H, 50/60 Hz,
0.8 A). Each participant performed three trials under each of the 4. Discussion
following experimental conditions: a) eye fixed on the target—the
target was displayed in the center of the monitor throughout the We manipulated visual conditions (fixation, saccades, and
trial and the participants fixated their gaze on it; b) slow saccadic smooth pursuit eye movements) in order to examine their effects
eye movement—participants performed saccades directed to the on postural control. We hypothesized that body sway would
target appearing on one side of the monitor, then disappearing and decrease during saccades and increase during smooth pursuit when
reappearing immediately on the opposite side with a frequency of compared to a fixed gaze. The findings of this present study con-
0.5 Hz; c) fast saccadic eye movement—same task as the previous firmed our hypothesis for saccadic eye movements, but not for
condition, but with a frequency of 1.1 Hz; d) slow smooth pursuit smooth pursuit eye movements. That is, eye movement using either
eye movement—participants pursued a target moving rectilinear type of movement, saccades or smooth pursuit, reduced body sway
and uniformly from one side of the monitor to the other with their when compared to fixation, which concurs with the notion that
eyes, with a frequency of 0.5 Hz; and e) fast smooth pursuit eye reduction of body sway occurred to facilitate eye movements [1,2],
movement—same task as the previous condition, but with a fre- contradictory to what previous studies reported about smooth pur-
quency of 1.1 Hz. Trials were performed in a randomized order. One suit effects on body sway [8]. Methodological differences between
experimenter observed and verified each participant’s appropriate this study and the study of Laurens et al. [8] might account for
eye movements using a small camera (Microsoft webcam, model the different results. Their experimental situation included hor-
294 S.T. Rodrigues et al. / Neuroscience Letters 584 (2015) 292–295

Table 1
Means and standard deviations of the global analyses of body sway.

Fixation Slow saccades Fast saccades Slow smooth pursuit Fast smooth pursuit

Trunk
Mean sway amplitude (cm) AP 0.73 ± 0.28a 0.50 ± 0.17 0.49 ± 0.15 0.50 ± 0.13 0.57 ± 0.27
ML 0.28 ± 0.14 0.28 ± 0.14 0.23 ± 0.06 0.21 ± 0.07 0.27 ± 0.22
Mean velocity (cm/s) AP 0.33 ± 0.08 0.33 ± 0.08 0.32 ± 0.07 0.34 ± 0.07 0.35 ± 0.05
ML 0.18 ± 0.07 0.19 ± 0.06 0.16 ± 0.04 0.18 ± 0.04 0.18 ± 0.04
Total displacement (cm) 1908.18 ± 776.34a 1426.85 ± 388.27 1279.39 ± 359.73 1356.78 ± 401.43 1476.54 ± 537.34
Sway area (cm2 ) 1.34 ± 1.03 0.98 ± 0.67 0.76 ± 0.52 0.86 ± 0.71 0.97 ± 0.70
Mean frequency (Hz) AP 0.13 ± 0.02a 0.16 ± 0.02 0.17 ± 0.02 0.16 ± 0.02 0.17 ± 0.03
ML 0.22 ± 0.05 0.24 ± 0.03 0.23 ± 0.06 0.23 ± 0.04 0.24 ± 0.07
95% of the total frequency (Hz) AP 0.39 ± 0.06 0.43 ± 0.05 0.43 ± 0.06 0.43 ± 0.05 0.42 ± 0.07
ML 0.70 ± 0.16 0.72 ± 0.14 0.73 ± 0.21 0.67 ± 0.14 0.67 ± 0.20

Head
Mean sway amplitude (cm) AP 0.89 ± 0.31a 0.63 ± 0.15 0.62 ± 0.15 0.61 ± 0.13 0.66 ± 0.24
ML 0.32 ± 0.18 0.33 ± 0.16 0.28 ± 0.09 0.26 ± 0.08 0.34 ± 0.25
Mean velocity (cm/s) AP 0.44 ± 0.10 0.44 ± 0.10 0.42 ± 0.07 0.46 ± 0.07 0.47 ± 0.07
ML 0.24 ± 0.07 0.25 ± 0.06 0.23 ± 0.05 0.24 ± 0.05 0.25 ± 0.05
Total displacement (cm) 2382.98 ± 859.11a 1845.54 ± 44.99 1678.17 ± 421.39 1746.08 ± 400.87 1832.51 ± 595.71
Sway area (cm2 ) 2.05 ± 1.37 1.54 ± 0.93 1.28 ± 0.80 1.36 ± 0.80 1.50 ± 0.98
Mean frequency (Hz) AP 0.14 ± 0.02a 0.16 ± 0.02 0.16 ± 0.02 0.17 ± 0.02 0.17 ± 0.03
ML 0.22 ± 0.04 0.24 ± 0.05 0.25 ± 0.07 0.22 ± 0.04 0.24 ± 0.07
95% of the total AP 0.41 ± 0.07 0.44 ± 0.06 0.43 ± 0.05 0.46 ± 0.05 0.86 ± 1.41
frequency (Hz) ML 0.72 ± 0.14 0.71 ± 0.14 0.74 ± 0.21 0.64 ± 0.12 0.71 ± 0.14

AP: anterior–posterior | ML: medial–lateral.


a
Fixation was different from the other four conditions.

izontal and vertical sinusoidal stimulus motions at 0.33 Hz, a on the retina, between saccades to connect pre- and post-saccadic
dark background (no large-field condition) or randomly positioned views of the scene [4] or, during smooth pursuit eye movements,
white dots on a dark background (stationary large-field condition to select a constant target to follow [8], in order to keep a stable
−3.1 m × 2.5 m), a force plate covered with a foam-cushion (10 cm relationship between visual information and body orientation [3].
height), participants wore a head-mounted device which restricted Although the distinctive properties of saccadic and smooth pursuit
the horizontal visual field to 80◦ , and their non-dominant eye was eye movements are well known [8,11], both eye movements share
occluded to suppress stereopsis cues. Differently, this experiment some neural networks, and, by implication, some similar process-
used only horizontal and linear stimulus motions at 0.5 and 1.1 Hz, ing mechanisms [4]. For instance, during our saccadic conditions,
a white background on a computer monitor (37.5 cm × 30 cm) in the stimulus disappeared on one side of the screen and reappeared
a fully illuminated room, no foam-cushion on a force plate, no immediately on the other side; even with a predictable target loca-
head-mounted device, full horizontal and vertical fields of view, tion, the saccadic task required spatial accuracy, which indicates
and binocular vision available. It is possible that a combination how body sway attenuation facilitated saccade planning and per-
of different aspects resulted and affected differently body sway of formance [1,2]. Similarly, during the smooth pursuit eye movement
participants from each study. Based upon the observed results, we conditions, the stimulus moved linearly and horizontally with a
present two lines of reasoning related to eye movement and body constant velocity, alternating between right and left directions,
sway effects. First, particular characteristics of each gaze behavior which required the eyes to change pursuit from a scan with a hor-
induced the same sway attenuation responses. Second, similarities izontal velocity, then momentarily stop, followed by a reversal in
between the control of saccades and smooth pursuit movements their direction and then, presumably catching up with the stimulus
have contributed to the observed effects on postural control. velocity in the other direction [8].
The availability of visual information, independent of the actual Both gaze conditions required relatively high spatial accuracy
gaze behavior, stabilizes body sway, which is demonstrated by and attentional resources for each stimulus’ cycle, especially during
increased sway magnitude during the absence of vision [12]. the transition between the refresh of the stimulus on the opposite
Despite, previous studies indicating that eye movement increases side of the monitor during the saccades stimulus and during the
body sway [9,13,14], eye movement signals can be used to con- transition between the direction of motion for the smooth pursuit
tribute to postural stabilization [3,9]. However, when eyes are stimulus, which potentially explain the improvement in postural
moved, the stationary large-field stimulus effect is reduced. This control leading to body sway attenuation under both conditions
reduction is compensated by retinal flow which is combined [4]. However, the strategies to control the changes of the moments
with information about the eye movements in order to recon- of transition appear different between eye movement conditions.
struct a fixed spatial reference [8] requiring a higher allocation That is, saccadic eye movements can be anticipated, favoring a feed-
of central processing resources in order to support the visual per- forward modulation of body sway [3,16] while smooth pursuit eye
formance and spatial requirements of the gaze behavior involved, movements appear to be controlled using an on-line mechanism
further attenuating postural sway [1,6,15]. In addition, the “out- due to its continuous visual information processing during a task.
flow” hypothesis suggests that a branch of the neural efferent Even with consistent and relevant results, this study has a few
signals (i.e., “corollary discharge” or “efference copy”) informs the limitations. Despite monitoring eye movements using video to
central nervous system and the mechanisms of afferent and effer- guarantee proper task performance, kinematics of the line of gaze
ent motion perception to maintain visual consistency [3]. in space and identification of fixation duration during each con-
Eye movements during quiescent stances create a functional dition were not quantified. This information is important, mainly
integration of postural and gaze control [1,2], which in our study to understand gaze control during a task. This procedure for future
occurred independent of task and stimulus frequency. Individu- studies is recommended. In addition, our manipulation of the visual
als might have tried to minimize changes of the projected image stimulus frequency (0.5 and 1.1 Hz) may has been insufficient to
S.T. Rodrigues et al. / Neuroscience Letters 584 (2015) 292–295 295

influence a measurable body sway, but frequencies higher than [3] M. Guerraz, A.M. Bronstein, Ocular versus extraocular control of posture and
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Straumann, Visual contribution to postural stability: interaction between
In conclusion, saccades and smooth pursuit eye movements target fixation or tracking and static or dynamic large-field stimulus, Gait
influenced body sway similarly, reducing the sway magnitude Posture 31 (2010) 37–41.
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Acknowledgement [12] W.M. Paulus, A. Straube, T. Brandt, Visual stabilization of posture:
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This study was supported by a scholarship for Jamile Cristina (1984) 1143–1163.
[13] K. Jahn, M. Strupp, S. Krafczyk, O. Schüler, S. Glasauer, T. Brandt, Suppression
Carvalho (Conselho Nacional de Desenvolvimento Científico e Tec-
of eye movements improves balance, Brain 125 (2002) 2005–2011.
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movements and balance, Ann. N. Y. Acad. Sci. 1004 (2003) 352–358.
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