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Correspondence: Sheng Tong Lin, 27 PURPOSE. Currently, the test for useful field of view (UFOV) typically relies on subjective
Medical Drive #11-00, Singapore feedback for detecting peripheral targets while attending to a central target. Steady-state visual
117510, Singapore; evoked potential (SSVEP) recorded from the occipital region of the brain has been frequently
shengtong@u.nus.edu, used as an objective alternative to replace subjective responses. Our aim was to investigate if a
lshengto@dso.org.sg.
short screening test can approximate UFOV performance objectively.
Submitted: October 18, 2015
Accepted: April 26, 2016 METHODS. We recorded SSVEPs during a simple peripheral task and a UFOV task with and
without distractors as well as 30-second offline SSVEPs for eight participants. In all tasks, a
Citation: Lin ST, Tey LK. A preliminary peripheral annulus ring of checkered reversal pattern was concurrently presented to the
study on normalized pattern-reversal
peripheral field SSVEPs as a potential
participants to elicit SSVEPs.
objective indicator of useful field of RESULTS. Orthogonal linear regression analysis found that normalized SSVEP during the UFOV
view performance. Invest Ophthal- task is predictive of peripheral target detection accuracy (F(1,6) ¼ 16.250, P < 0.01, n ¼ 8)
mol Vis Sci. 2016;57:3248–3256. for a task with peripheral distractors. However, this is not the case for a task without
DOI:10.1167/iovs.15-18439 distractors (F(1,6) ¼ 0.397, P ¼ 0.552), possibly due to near-perfect accuracy across most
participants. Offline normalized SSVEPs also only predicted the peripheral target detection
accuracy (F(1,6) ¼ 26.799, P < 0.01) for the UFOV task with peripheral distractors.
CONCLUSIONS. Difficult peripheral target detection with distractors is required to differentiate
UFOV performance in healthy young adults. The results suggested that offline normalized
SSVEPs elicited by 30 seconds of pattern-reversal checkered annulus from the peripheral
vision field can identify individuals with good UFOV performance under the stress of a
difficult peripheral task.
Keywords: SSVEP, UFOV, EEG
ypically, the current means of assessing attention is to put fixation point. It has been found that driving accidents are
T individuals through psychophysical tests. These tests rely
on subjective feedback and critical reaction-time response;
correlated with poorer UFOV in elderly drivers.3,4 On the other
hand, SSVEP is the neuronal signal typically from the occipital
hence time must be set aside for multiple trials to gather brain region that oscillates at the same frequency as the flicker/
accurate averages and to minimize effects of noise on data. flashing rate of the visual stimulus presented, and this oscillation
When a test has to be repeated to confirm results, the lengthy is modulated by how and where visual attention is deployed.5
testing time multiplies with each repetition. Also, a subjective The SSVEPs can be identified by recording brain signals using
test tends to rely on the motivational level of the individual. In electroencephalography (EEG) and then transforming the
the case in which a subjective test is used to select suitable recorded data into the frequency domain where SSVEP is seen
candidates for sports or military vocation, those mandated by as an increase in amplitude or power in the same frequency as
rules to participate may respond suboptimally to avoid good the stimulus presentation frequency.5,6 Relationships between
scores while those who are keen but are not confident about SSVEP and psychophysical assessment of attention have often
passing the test may try guessing tricks to achieve high scores. been studied. Mishra et al.7 found that action game players have
Recruiters would prefer shorter testing times while avoiding increased suppression of SSVEP amplitudes to unattended
subjectivity by having objective markers. peripheral stimuli. Many other effects of attention phenomena
In this study, the aim was to investigate steady-state visual in modulating SSVEP have also been studied.8–12 Not surprising-
evoked potential (SSVEP) as a neurosignal marker that can ly, objective feedback using SSVEP have become potential
quickly and objectively assess individuals for their attentional objective assessments for retinal functions,13 visual acuity,14
span around their primary gaze, or, to use a more recognized amblyopia,15 stereoscopic vision,16 binocular rivalry,17–19 and
term, the useful field of view (UFOV). Useful field of view is fatigue.20 In the past two decades, frequency-tagging technique
defined as the visual area from which one captures visual for SSVEPs has been used to study localized attention.21–24 This
information with a single glance without any eye movement.1–4 technique requires the visual stimulus of interest to flash at a
It indicates attentional performance toward the peripheral visual specific frequency; hence the stimulus is said to be ‘‘tagged’’
field while visual information is concurrently processed from a with a frequency. The amplitude of SSVEP is modulated by
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
mean illuminance of the checkered pattern was 150 cd/m2. entire trial or when a blink occurred during the last 5 seconds
The thickness of the ring spanned between 3.58 and 78 from of the baseline or activity phase.
the fixation cross center, leaving a center gray zone extending
from the fixating point to the inner edge of the ring. The Experiment 2: Central–Peripheral Dual Task
baseline phase lasted for 10 seconds, followed by the activity
phase, which was the same as the baseline phase except for The purpose of this task was to investigate the participant’s
two aspects. Firstly, just outside and around the annulus ring ability to direct simultaneous attention to both central and
were eight equally distributed small peripheral rings (1.48 peripheral stimulus. In other words, it measured the likelihood
visual angle in size). Only one of these circles was randomized of detecting a target at a given eccentricity while attending to a
to be filled black for 100 ms (onset of peripheral stimulus) central stimulus, thus assessing the breadth of allocated
every 1.2 seconds in synchrony with the fixation cross. attention in space (i.e., UFOV performance). The trial design
Secondly, the activity phase was randomized to last for 16 to was the same as for experiment 1 except that during activity
phase, the center fixating stimulus was a small circular ring,
32 seconds to allow sufficient time to adapt to the peripheral
0.1678 (10 arcmin) in size (Fig. 2). The circular ring presented a
stimuli. The end of the activity phase was indicated by a white-
0.0838 (5 arcmin) broken gap every 1.2 seconds in synchrony
noise screen, which was presented for 2 seconds; then
with the peripheral stimulus onset. The presentation of the gap
participants had to indicate which one of the peripheral
was randomized to occur at either the up, down, left, or right
circles last seen was filled black by pressing a response button part of the circular ring. The participant had to actively
corresponding to the peripheral circle position (e.g., numeric respond in real time to the gap direction using keyboard arrow
keypad number 1 ¼ bottom left circle, 9 ¼ top right circle). The buttons, while response to the peripheral stimulus occurred
purpose was to exclude anticipatory deployment of attention after the white noise when each trial ended. There were a total
to the periphery. Participants were told to hold their blink of 20 trials. The UFOV performance scores were recorded as
during the baseline and activity phase but were encouraged to the percentage of correct responses for the peripheral stimulus
blink to their satisfaction during the time when they made that occurred just before the white-noise onset. Note that trial
their response for the peripheral target after the white noise. results were excluded from score calculations if a participant
Participants were also told to take their time to make this did not make a correct response to the last central stimulus
response so as to have ample time for blinking and sufficient during its simultaneous onset with the last peripheral stimulus
rewetting of their eyes. Scores were recorded as the just before the white noise.
percentage of correct responses for the peripheral stimulus
that occurred just before the white-noise onset. There were a Experiment 3: Central–Peripheral Dual Task With
total of 20 trials. An eye tracker (SMI RED 250; SensoMotoric
Active Distractors
Instruments Gmb, Teltow, Germany) was used in this study to
ensure that participants’ eyes were fixating on the central The purpose of this task was to investigate that participant’s
stimulus. Trial results were discarded if a subject was found to ability to perform a central–peripheral attention task in the
fixate beyond 18 away from the central stimulus during the presence of peripheral distractors. The trial design was the
same as for experiment 2 except that during the activity phase, normalized SSVEP (nSSVEP) power for each experiment was
extra distractors between the peripheral circles in the form of calculated by taking the average 7.5-Hz power of the
black spots (1.48 visual angle in size) were presented along accumulated activity phase minus its accumulated preceding
with the onset of peripheral stimulus (Fig. 3). baseline phase’s power of the same frequency. Statistical
analyses on psychophysical and nSSVEPs were conducted
Experiment 4: Single-Trial Central Task using GraphPad Prism 7.0 (La Jolla, CA, USA).
DISCUSSION
The first experiment demonstrated that all participants had
good peripheral vision to start with. The second experiment
FIGURE 6. Percentage accuracy versus normalized SSVEPs in experi-
ment 1 (a), 2 (b), and 3 (c). demonstrated that all participants could perform the central–
peripheral task well. The third experiment increased periph-
eral task difficulty by throwing in peripheral distractors on
top of the central–peripheral dual attention task to examine
strong indicator of performance and there is a high chance how individuals handle multiple pieces of information closer
that different peripheral target difficulties (with or without to the boundaries of UFOV. The peripheral distractors in
distractors) have a small effect on nSSVEP as seen in Figure 5 experiment 3 were shown to be effective in increasing
(experiment 2 versus experiment 3), can nSSVEPs derived peripheral task difficulty, providing a wider spread of
from a simple central stimulus task approximate dual-task performance differences between participants. Noticeably,
performance in experiment 3? And given the stability of the the relationship between UFOV performance and nSSVEP in
FIGURE 7. Mean SSVEPs for ‘‘empty,’’ baseline, and activity phase for experiment 4. Error bar: SE.
experiment 3 is driven by two clusters of data in the current increased SSVEPs for attended flashing stimuli accompanied
small sample size. Hence, at the moment, implementing by an increased detection accuracy in a multiregion visual
peripheral distractors in experiment 3 could differentiate the search task. Hence, they are thought to be deploying some
participants’ performance into only two different levels. form of attention enhancement. Findings for the participant
Interestingly, peripheral task difficulty was not accompanied in experiment 3 who was a frequent RPG player seem to
by a corresponding significant difference in nSSVEPs when concur with the findings of Krishnan et al.29 as her relatively
comparing experiments 3 and 2 (with and without peripheral higher nSSVEP is accompanied by better peripheral detection
distractor comparison) and experiments 3 and 4 (with and accuracy than most of the other participants. Unfortunately,
without peripheral task comparison). This could be a case of this preliminary study did not have participants who were
a small difference in nSSVEPs between experiments 2 and 4 active/frequent action video game players. It is known that
compared to a larger difference in their UFOV performances; action video gamers perform better in UFOV tasks,30,31 and
this small difference could not reach significance due to small they probably ignore distractors better using a unique neural
sample size. Nevertheless, experiment 4, a case of an strategy revealed by the suppression of SSVEPs from
extremely easy single-trial central task without any peripheral irrelevant flashing stimuli.7 Therefore, it will certainly be of
task, produced nSSVEPs similar to those in experiment 3 in interest to repeat experiments 3 and 4 with action video
identifying good UFOV performers over poorer ones for a gamers.
difficult peripheral task. This suggested that the single-trial On the other hand, the influence of sports training on
nSSVEP has applicable value as a screening tool. Another SSVEPs is less well studied. Also, the findings in the literature
strong contributing factor to the success of experiment 4 is regarding better UFOV in ball sport athletes are rather
how the baseline was designed. Both SSVEPs were stimulated mixed. Matos and Godinho32 and Memmert et al.33 high-
and acquired during baseline phase (no task) and activity lighted that UFOV for these sportsmen is not significantly
phase (task). Taking the signal differences between them to better than in nonsportsmen. Memmert et al. suggested that
associate with effects arising from the corresponding task the commercial version of the UFOV test is designed for
performance is more meaningful than purely having an SSVEP screening elderly persons for risk of driving accidents and
extracted and baselined to a controlled condition without any may not have the sensitivity to find differences between
checkered stimulus. sportsmen and nonsportsmen among healthy young individ-
Another observation in experiment 3 was that most uals. However, Schwab and Memmert34 found that sports
nSSVEPs in this study were negative in value, and those with vision training improves UFOV for hockey players but did
good UFOV had positive nSSVEP values. This may be attributed not report sports performance to suggest any corresponding
to the fact that good UFOV performers in experiment 3 improvement in actual sports activity. A study by Störmer et
maintained their attention better under the stress of a difficult al.27 suggested that individuals who are better at tracking
peripheral task, hence suffered less peripheral field SSVEP multiple flashing moving targets within their visual field
attrition when executing central–periphery dual detection exhibit higher SSVEPs than those elicited by the frequency-
during the activity phase. Given that SSVEP strength is tagged targets. If these individuals are analogous to ball game
relatively stronger for attended stimuli,5,6 this explanation is sportsmen, then there is a good possibility that better UFOV
plausible. in sportsmen could be accompanied by higher levels of
The last observation worth noting concerns the top three SSVEPs.
performers in experiment 3 (mentioned earlier) who included In conclusion, in this preliminary study, we have demon-
two sportsmen and a video gamer. The effect of video gaming strated that changes in peripheral field SSVEP can potentially
has previously been demonstrated, with specific differences be used to identify an individual with good UFOV perfor-
in the SSVEPs of video gamers compared to normal mance in the presence of distractors. Particularly, as
individuals.7,29 Krishnan et al.29 found that RPG players have demonstrated in experiment 4, it is possible that a short 30-
FIGURE 8. Percentage accuracy in experiments 1 (a), 2 (b), 3 (c) versus normalized SSVEPs in experiment 4.
second objective SSVEP test can differentiate those individu- impedance quality. This setup time can be reduced in the
als with good UFOV from those with poor UFOV. For the future when dry electrodes with conductivity nearly equiv-
purpose of a quick screening test, this could be a reasonable alent to that of wet types are available. Future work should
trade-off of assessment accuracy for shorter testing time. look at larger sample size to avoid the possibility of type 1
While the testing time is short, the setup time for experiment error, as well as various eccentricities of peripheral stimulus
4 requires approximately 3 minutes to place the six to estimate the distribution of attentional performance
electrodes (O1, O2, Oz, M1, M2, GND) and to ensure their toward the periphery. Extensive efforts in testing and
retesting of the screening task in experiment 4 must be made index of amblyopic deficits. Invest Ophthalmol Vis Sci. 2015;
to ascertain its reliability in predicting UFOV performance. It 56:1208–1216.
will also be worthwhile to recruit sportsmen and video 16. Johansson B, Jakobsson P. Fourier analysis of steady-state visual
gamers to study their differences using current experimental evoked potentials in subjects with normal and defective stereo
paradigms. vision. Doc Ophthalmol. 2000;101:233–246.
17. Zhang P, Jamison K, Engel S, He B, He S. Binocular rivalry
Acknowledgments requires visual attention. Neuron. 2011;71:362–369.
18. Sutoyo D, Srinivasan R. Nonlinear SSVEP responses are
Supported by Future Systems and Technology Directorate (FSTD),
sensitive to the perceptual binding of visual hemifields during
Singapore. Grant number 9012102527.
conventional ‘‘eye’’ rivalry and interocular ‘‘percept’’ rivalry.
Disclosure: S.T. Lin, None; L.K. Tey, None Brain Res. 2009;1251:245–255.
19. Jamison KW, Roy AV, He S, Engel SA, He B. SSVEP signatures of
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