Keywords Saccades - Athletes - Electroencephalography - Reaction Time
Palavras-chave Movimentos Sacádicos - Atletas - Eletroencefalografia - Tempo de Reação
INTRODUCTION
The saccadic eye movements are fast and precise oculomotor shifts responsible for
locating external visual targets, bringing the objects of interest to the retina.[1 ]
[2 ] In a visual search task, the focus of attention is usually determined by the fixation
point, and, in this scenario, one observes the need to effectively concentrate on
the performance of many sports in which information is relevant.[3 ]
[4 ] Perceptual ability is linked to the athlete's ability to select critical components
within a dynamic environment.[5 ]
[6 ] Experienced athletes respond efficiently to information that is relevant to their
task, while leaving irrelevant and distracting information unattended.[7 ]
[8 ] Thus, specialized neural processing favors their superior abilities.[4 ] The ball in movement and the position of the positioning are starting situations
in which the athletes must use saccadic eye movements to have an efficient performance;
therefore, a relationship is observed between the ease of fixation of the saccade
and the sports performance.[9 ]
During the planning and execution of saccadic eye movements, the prefrontal and frontal
cortices are involved, causing changes in cortical electrical activity. These changes
can be observed through quantitative electroencephalography (EEG).[10 ]
[11 ]
[12 ] Investigations point to the theta frequency band (range: 4 Hz to 7 Hz) as the neural
correlate of the integration of sensory information to a motor response in the production
of voluntary movement.[13 ]
[14 ] Theta is widely distributed through the brain, reflecting actions in the cortex,
specifically during complex executive processes such as attention mechanisms, spatial
navigation, coding, and memory retrieval.[15 ]
[16 ]
Velasques et al.[17 ] investigated the absolute theta power on the frontal cortex during the planning,
execution, and cognitive control of saccadic eye movements. They have shown that the
presentation of the stimulus induces distinct patterns of cortical activation between
the left and right hemispheres. Moreover, Jafarzadehpur et al.[18 ] examined the visual accommodation capacity of non-players, beginner volleyball players,
and intermediate and advanced volleyball players. Significant differences between
non-players and beginners were detected compared to the intermediate and advanced
group. In addition, differences in saccadic eye movement have been observed between
non-athletes, badminton players, and squash players. However, although the role of
theta activity in the planning and execution of saccadic eye movement tasks and distinctions
in habituation between athletes and non-athletes have been demonstrated, no experiment
has directly investigated the electrophysiological differences between athletes and
non-athletes during a saccadic eye movement task.
Therefore, the present experiment aims to directly address this issue by analyzing
saccade latency and the absolute theta power in athletes and non-athletes. We want
to specifically compare the differences in the average latency during the saccadic
eye movement and interhemispheric changes in EEG activity between athletes and non-athletes.
We hypothesize a decrease in saccade latency and the theta frequency band in athletes
in the frontal and prefrontal regions because of the volleyball training and the perceptual-cognitive
expertise of the players.
METHODS
Sample
We recruited 30 volunteers: 15 volleyball players (11 men and 4 women; mean age: 15.08 ± 1.06
years) and 15 non-athletes for the control group (5 men and 10 women; mean age: 18.00 ± 1.46
years). The athletes had about 4 years of playing experience, with an average of 15 hours
a week of training at elite national-level teams within their age group, while the
non-athletes participated in physical activities in high school. All participants
had normal vision and no sensory, cognitive, motor, or attentional deficits that would
affect the saccadic eye movement. All individuals were right-handed according to the
Edinburgh Inventory.[19 ] In addition, they had had at least 6 to 8 hours of sleep the day before the experiment
was performed. The participants signed a consent form that described in detail the
experimental procedure. Those responsible for individuals under the age of 18 years
signed the consent form. The study was approved by the Ethics Committee of Instituto
de Psiquiatria da Universidade Federal do Rio de Janeiro (IPUB-UFRJ) (CAAE: 94619218.3.000.5257),
according to the principles of the Declaration of Helsinki (FR 233406) .
Experimental procedure
The room used to capture the electroencephalographic signal was sound protected, and
during data acquisition, the room's brightness was reduced to minimize sensory interference.
The individuals sat comfortably in a chair with arm support to minimize muscle artifacts.
A bar made up of 13 light-emitting diodes (LEDs) was placed in front of the participants
and positioned at the level of their eyes. The bar was composed of six LEDs on the
left side of fixation and another six LEDs on the right side, and a bicolored central
warning LED. The subjects were within 100 cm of the LED bar. A computer program controlled
the bar and determined the presence of the stimulus. The participants were asked to
keep their eyes fixed on the center of the bar and to slide them when they noticed
that one of the diodes was illuminated; then, they were instructed to follow the LEDs
with their eyes so that their heads remained static. The paradigm constituted the
realization of a fixed condition of presentation of the luminous stimulus. In this
situation, the target stimulus alternated from a predetermined two-point position,
that is, the six LEDs on each side of the bar (left or right). This condition was
characterized by the predictability of the appearance of the stimulus in time and
space, being considered directed by memory. The LEDs blinked alternately between the
left and right sides of the bar. The flash of each LED lasted for 250 ms, and the
interval between flashes was of 2 s. Each participant was submitted to six blocks
of stimulation and two resting periods (without stimulus), one before starting the
task and another one after the end. Each block consisted of 20 tracks, with 10 LEDs
on the right side of the bar and 10 on the left side, from the warning in the center
of the bar.
Acquisition of electroencephalographic data
The Braintech 3000 device (EMSA Equipamentos Médicos Ltda., Rio de Janeiro, RJ, Brazil)
was used to capture the electroencephalographic signal, using a 20-channel analog-digital
converter (A/D) board. A capture program, called EEG_Captação (created using the Delphi
5.0 software [Embarcadero Technologies, Austin, TX, United States]), produced at the
Brain Mapping and Sensory-Motor Integration Laboratory at UFRJ, was used to acquire
the electroencephalographic signal and control the LED lighting. The EEG signal was
amplified with a gain of 22 thousand, analogously filtered between 0.1 Hz (high pass)
and 100 Hz (low pass), and the sampling was 200 Hz. A 60-Hz digital notch filter was
used. The International Federation's 10-20 electrode system (Jasper, 1958) was used
to place 20 electrodes along the scalp (areas: frontal, central, temporal, parietal,
and occipital) and an electrode in each ear (lobe). The electrodes were mounted on
a nylon cap, produced at the same laboratory as mentioned before, with prefixation
of the system 10-20. The earlobes were used as a reference (binaural). The impedance
of each electrode was maintained between 5 kΩ and10 kΩ. The acquired data had a total
amplitude (peak to peak) < 70μV.
Acquisition of the saccadic eye movement
The ocular electrical activity, or electrooculogram (EOG), was estimated by placing
2 electrodes with 9 mm in diameter mounted bipolarly; they were placed in the outer
corner of the left and right eyes that recorded the horizontal eye movements (hEOG).
Data processing and analysis
In order to remove the possible artifacts produced by the task (blinking, muscular
activity, and artifacts related to saccade), we applied the independent component
analysis (ICA). The data, collected using the biauricular reference, were transformed
(re-referenced) using the average reference; then, they were conducted to eliminate
artifacts through ICA. Removed by visual inspection, the tracks that demonstrated
the blink of an eye and artifacts related to the saccade, as well as the components
that showed blinking and artifacts related to “contamination” of the saccade through
ICA, were excluded. The number of samples was of 800 (4 × 200 Hz), with a rectangular
window. The quantitative EEG parameters were extracted with a time window of 500 ms
before the presentation of the stimulus, and 500 ms after the trigger (moment 1 and
moment 2 respectively). After that, all EEG trials were visually controlled, and if
there was still a “contaminated” track with muscle artifacts, it was discarded. To
test the stationarity of the signal, the Runs test and Reverse Arrangement test was
applied. Significantly, the null hypothesis of the stationary process was accepted
for every 4 s (period duration in this period).
Statistical analysis
The statistical analysis was performed using the IBM SPSS Statistics for Windows (IBM
Corp., Armonk, NY, United States) software, version 21.0, and saccade latency and
absolute theta power (4 Hz to 7 Hz) were the 2 dependent variables of interest. We
used a semiautomated method to detect saccade latency; in particular, the saccades
were determined at the start of the curve's inflection point, consistently recognized
from visual inspection. The saccade was separated 500 ms after the presentation of
the stimulus. The highest velocity (first derivate) was detected at the deflection
point. From the moment the LEDs are lit, we define a period of 500 ms to seek the
EOG inflection and mark the point with the highest ‘‘acceleration’' or the initiation
(second derivate) of the EOG signal. Saccades with latencies shorter than 100 ms and
longer than 400 ms were not considered.
The independent samples t -test (non-athletes and volleyball athletes) was applied to analyze the average change
in latency of the saccadic eye movement. In addition, the electrophysiological analysis
of the absolute theta power was performed through two-way analysis of variance (ANOVA)
determined by two factors: group (non-athletes and volleyball athletes) and momentum
(before and after the stimulus to the fixed condition during the task of saccadic
eye movement). For those electrodes in which we found an interaction between factors,
a paired t -test was applied to examine the possible differences. We estimated the effect size
as partial squared eta (ƞ2 p), and we calculated the statistical power and the 95% confidence interval (95%CI)
for the dependent variables. Each electrode was seen separated precisely to avoid
a type I error. Significance was set at p ≤ 0.05 for all analyses.
RESULTS
Behavioral measures
The independent samples t -test for the “group” factor (non-athletes and volleyball athletes) was performed
to examine changes in saccadic eye movement. We observed that the latency in the “fixed”
paradigm of the task of saccadic eye movement presented a significant difference (t
[1.1488] = 2.039; p = 0.042). We identified a decrease in the average time for the group of athletes
(mean = 320.369 ± 69.382 ms) compared to the group control of non-athletes (mean = 328.250 ± 79.475 ms).
The mean difference in reaction time between the control group and athletes is shown
in [Figure 1 ].
Figure 1 Mean and standard deviation of values for saccade latency (ms) for the two groups
(saccade latencies are shown separately for each group). The statistical analysis
revealed differences between the group athletes and the control group (p = 0.042).
Electrophysiological parameters
The two-way ANOVA (p ≤ 0.05) indicated a significant effect on absolute theta power for the “group” factor.
We observed a decrease in the theta frequency in the group of athletes compared to
the non-athletes in the electrodes: Fp1 (F [1.3367] = 138.815; p < 0.001; ƞ2 p = 0.040; power = 99.9%); Fp2 (F [1.3376] = 182.930; p < 0.001; ƞ2 p = 0.051; power = 99.9%); F7 (F [1.3393] = 39.067; p < 0.001; ƞ2 p = 0.011; power = 99.6%); F8 (F [1.3380] = 51.138; p < 0.001; ƞ2 p = 0.015; power = 99.9%); F3 (F [1.3389] = 27.661; p < 0.001; ƞ2 p = 0.008; power = 90.6%); Fz (F [1.3382] = 31.768; p < 0.001; ƞ2 p = 0.009; power = 97.3%); and F4 (F [1.3386] = 96.518; p < 0.001; ƞ2 p = 0.028; power = 99.9%). [Figures 2 ], [3 ] and [4 ] show the mean and standard deviation (SD) differences in absolute theta power for
the two groups in the frontopolar cortex the inferior prefrontal gyrus, and the anterior
frontal cortex respectively.
Figure 2 Mean and standard deviation values for absolute theta power (μV2 ) in the frontopolar cortex. The figure illustrates the difference among groups for
each pair of electrodes located on the frontopolar cortex. For Fp1, the statistical
analysis revealed differences in the left frontopolar cortex between the athlete group
and the control group (p < 0.001); for Fp2, the statistical analysis revealed differences in the right frontopolar
cortex between the athlete group and the control group (p < 0.001).
Figure 3 Mean and standard deviation values for the absolute theta power (μV2 ) in the inferior prefrontal gyrus. The figure illustrates the difference among groups
for each pair of electrodes located on the inferior prefrontal gyrus. For F7, the
statistical analysis revealed differences in the left inferior prefrontal gyrus between
the athlete group and the control group (p < 0.001); for F8, the statistical analysis revealed differences in the right inferior
prefrontal gyrus between the athlete group and the control group (p < 0.001).
Figure 4 Mean and standard deviation values for the absolute theta power (μV2 ) are shown separately for the three frontal electrodes (F3, Fz, and F4) on the anterior
frontal cortex. For F3, the statistical analysis revealed differences in the left
anterior frontal cortex between the athlete group and the control group (p < 0.001); for Fz, the statistical analysis revealed differences in the midline anterior
frontal cortex between the athlete group and the control group (p < 0.001); for F4, the statistical analysis revealed differences in the right anterior
frontal cortex between the athlete group and the control group (p < 0.001).
DISCUSSION
The experiment proposed to analyze saccade latency (behavioral measurement) and the
absolute theta power (electrophysiological measurement) in the prefrontal and frontal
cortices during the execution of the “fixed” paradigm in the task of saccadic eye
movement.
Behavioral measure
The behavioral analysis revealed a significant difference expressed by a shorter average
saccade latency for the athletes. A decrease in latency among the athletes is mainly
associated with their superiority in terms of cognitive abilities. Such a finding
supports our hypothesis because of the volleyball players' excellent proficiency in
visual information fixation and, consequently, more extraordinary visual allocation
ability.[5 ]
[18 ]
[20 ] These play a crucial role in performing sports tasks, including information processing
speed and working memory capacity.[21 ]
[22 ]
The neural circuits for the initiation of the saccadic eye movement and the development
of attention are interconnected.[23 ] Our results indicate that the athletes responded to the task of saccadic eye movement
more efficiently, mainly associated with decreased attentional processes.[24 ]
[25 ] In such a way, continuous training results in shortening of the preparation of saccadic
eye movements, and, as a result, athletes move their eyes towards a visual target
more quickly, reducing saccade latency.
Electrophysiological parameters
Anterior prefrontal cortex
The anterior prefrontal cortex is located anatomically in the anterior frontal region
of the cerebral cortex (areas 9 and 10 of Brodmann). Responsible for planning, organization,
and motor representation, it is essential in integrating sensory and mnemonic information.[26 ]
[27 ] The pair of electrodes (Fp1 and Fp2) presented similar results for the main group
effect. A decrease in the absolute theta power in the left electrode (Fp1) was observed
for the group of athletes. Despite the current understanding that there is a complementarity
between the hemispheres, the left is known for its specialized role in analytical
aspects and motor functions, such as the preparation and execution of saccadic eye
movements.[28 ]
This decrease in theta can represent a specialization of the athletes in responding
to the demands of the experimental task, producing superior performance in the allocation
of perceptual processes, in the reaction time, and in the behavior of the saccadic
eye movement.[29 ] Acquiring motor skills leads to plastic changes in the cortical activation of broad
neural connections, leading to functional specificity. Another experiment[7 ] that analyzed the differences in theta in basketball players during the aiming period
between successful and unsuccessful free throws investigated this qualified processing
of the athletes. The authors[7 ] found that the group of experienced athletes demonstrated more cortical activity
in the frontal region than the novices, suggesting the superiority of this group in
concentrating on the relevant aspects of the specific behavior.[7 ]
The right hemisphere (Fp2) is more related to mnemonic processes, such as working
memory,[6 ] which is a skill that individuals acquire to satisfy the demands of cognitive activity
in a domain.[30 ] Theta reduction can be explained by the functional plasticity underlying cognitive-motor
training in athletes in the fixed condition of the experiment. This principle can
be observed in the reduction of the power of cortical activity in specific brain regions
since a skill becomes less controlled and automated after learning a complex task.[31 ] The result found in the Fp2 electrode supports the hypothesis of neural efficiency.
The neural advantages observed in athletes are characterized as neural efficiency,
suggesting lower energy expenditure and better performance during task performance
since a skill becomes less controlled and automated after learning a complex task.[31 ] Volleyball players have better cognitive abilities compared to non-athletes.[32 ]
[33 ]
Inferior prefrontal gyrus
Traditionally, the inferior prefrontal gyrus is associated with language and semantic
functions, as well as with working memory[34 ] and long-term memory processes.[27 ] The data of the present study suggest that prefrontal gyration is not limited to
aspects of speech and understanding of speech. A decrease in the theta power in the
athletes was verified for the electrode located in the left hemisphere, characterized
by analytical processes (F7). The decrease in F7 can be explained by the athletes'
ability to detect, retain, and allocate attention to information during the experimental
protocol. Repeating the motor gesture during training leads to plastic adaptations
in the cognitive-motor system, improving executive functions, such as working memory
and attention. Successful players have significant neuroplastic advantages in neural
processing compared to novices or non-practitioners in cognitive-motor tasks. The
athletes skillfully perceive and determine the ball's position and other players by
focusing on relevant stimuli.[35 ]
The right inferior prefrontal gyrus (Brodmann area 45) has functions related to episodic
and prospective memory. Episodic memory is the ability to recall specific events,
and prospective memory is the ability to evaluate and plan future actions.[36 ] Our results show a decrease in the absolute theta power in the group of athletes
in electrode F8. The results also suggest a greater involvement of episodic and prospective
memory over the fixed paradigm in the task of saccadic eye movement associated with
functional plasticity, indicating the improvement of the executive functions in the
group of athletes according to the neural efficiency hypothesis.
Anterior frontal cortex
Located in the premotor cortex, the anterior frontal cortex is also known as the frontal
visual field. This region plays an essential role in the control of saccadic eye movements.[17 ] We observed significant results in the electrodes of the anterior frontal cortex
(F3, Fz, and F4). A possible interpretation for such a finding can be attributed to
the absence of correction and modulation of motor programs due to the fixed task of
experiment.[5 ] Furthermore, the frontal theta midline frequency (Fz) is a sustained attention indicator
candidate.[7 ] Our data showed a decrease in the absolute theta power in the group of athletes
compared to non-athletes, suggesting that expertise practically modified neural structures
underlying sustained attention. Therefore, the results of the present study indicate
a cognitive enhancement of volleyball players in applying sustained attention at the
beginning of the saccadic eye movement.
Limitations of the present study
Although the present study has shown interesting results, some limitations are listed
below:
We initially limited the electroencephalographic analysis to only 20 channels, thus
leaving adequate spatial sampling for future analyses;
Claims regarding EEG activity between athletes and non-athletes should be more moderate;
further analysis with another modality of elite athletes is needed;
Our experimental task was characterized by the predictability of the location and
direction of the saccadic stimulus (guided by memory). Therefore, future works should
investigate another paradigm (such as visually guided) in order to better elucidate
the cortical dynamics between athletes and non-athletes;
Based on the literature, which indicates that the practice of physical exercise is
a neuroenhancer, in future studies, it is also essential to consider the use of event-related
potentials (ERPs) associated with cognition before and after physical training.
In conclusion, the present study examined differences in latency and absolute theta
power between athletes and non-athletes during a saccadic eye movement task. In general,
our results support the premise of cognitive improvement of the players in the experiment.
The results supported the principle of neural efficiency associated with plasticity
in the group of players on the complex executive functions. The neural correlates
of prefrontal and frontal regions are critical in identifying more talented players,
or they could be used for pre- to posttraining performance feedback.
