Name: investigating the deployment of visual attention before accurate and averaging saccades via eye tracking and assessment of visual sensitivity
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Description: Watch this Scientific Journal Video about Investigating the Deployment of Visual Attention Before Accurate and Averaging Saccades via Eye Tracking and Assessment of Visual Sensitivity at JoVE.com

This research was supported by grants of the Deutsche Forschungsgemeinschaft to H.D. (DE336/5-1 and RTG 2175 &#34;Perception in context and its neural basis&#34;) and to M.S. (SZ343/1) and a Marie Sklodowska-Curie Action Individual Fellowship to M.S. (704537).

This protocol was designed according to the ethical requirement specified by the Ludwig-Maximilians-Universit&#228;t M&#252;nchen and with the approval of the ethics board of the department.
1. Participants
<ol>
	<li>Recruit a sufficient number of naive participants with normal or corrected-to-normal vision and without neurological or psychiatric disorders. 10 participants are recommended based on similar, recent protocols21,22. 
	NOTE: Overall, we recruited 13 participants (aged 20-28, 7 females, 12 right-eye dominant, 1 author) from which 3 were excluded from final analysis since their orientation discrimination performance remained at chance level for all tested locations.</li>
</ol>
2. Experimental Setup
<ol>
	<li>Conduct the experiment in a quiet and dimly illuminated room under the supervision of an experienced experimenter familiar with eye tracking and all other experimental components.</li>
	<li>Prepare an experimental setup consisting of a computer, a cathode-ray tube (CRT) monitor, a standard keyboard, two loudspeakers, and an eye tracker (see Table of Materials).
	<ol>
		<li>Sequence and control the experiment using an appropriate software (see Table of Materials). Write a script which can be run on the software to load and launch the experiment automatically for each participant (https://github.com/mszinte/CompAttExo). Ensure that the script encodes all necessary experimental parameters and implements stimulus presentation as well as behavioral and eye data collection.</li>
		<li>Display all visual stimuli on a CRT screen with a minimum vertical refresh rate of 120 Hz. Ensure the proper display of visual Gabors via gamma linearization of the experimental screen.</li>
		<li>Assess participants&#39; evaluation of the discrimination target orientation (counterclockwise vs. clockwise) via the left and right arrow keys on a standard keyboard.</li>
		<li>Provide auditory feedback via loudspeakers upon incorrect manual responses.</li>
	</ol>
	</li>
</ol>
3. Eye Tracking
<ol>
	<li>Record the gaze of participants&#39; dominant eye at a sampling rate of at least 1 kHz throughout the entire experiment via an eye tracker.</li>
	<li>Ask the participant to sit down comfortably on a chair, place their chin on a chinrest, and lean their forehead against a bar to restrain head movement&#160;during the experiment. Individually adjust the height of the chair, the chinrest and the forehead bar such that participants&#39; eyes align with the center of the experimental monitor.</li>
	<li>Individual Eye Tracker Calibration
	<ol>
		<li>Before each experimental block (duration: approximately 10 min) and whenever necessary (e.g. after noticeable head movements and resulting shifts of the estimated fixation), run a calibration procedure to guarantee that participants&#39; gaze can be accurately tracked within a radius of 1&#176;. 
		NOTE: Here, we used a 13-point calibration procedure to get an accurate estimate of the characteristic light reflections (pupil and corneal reflection) of the tracked eye as a function of the gaze.
		<ol>
			<li>Ask the participant to follow a dot moving across different locations on the screen with their eyes to estimate their gaze position.</li>
			<li>Repeat the procedure with a dot rotation of 30&#176; and compare the measured gaze position to the estimated gaze position to validate the initial calibration. The calibration can be considered accurate when the averaged difference between the estimated gaze position following the calibration stage and the measured gaze position in the validation stage is below 1&#176;.</li>
			<li>Repeat the calibration procedure whenever the participant breaks fixation repetitively to guarantee high tracking accuracy throughout the experiment.</li>
		</ol>
		</li>
	</ol>
	</li>
	<li>During the experiment, monitor correct fixation at the screen center at the beginning of each trial. Only start a trial if the gaze stays within a radius of 2&#176; around the central fixation target for at least 200 ms.</li>
</ol>
4. Instructions
<ol>
	<li>Provide participants with clear task instructions. Present the task instructions at least once at the beginning of each experimental session in the form of a written text, together with a visualization of the trial chronology. Encourage participants to carefully read through the instructions and to ask remaining questions to the experimenter. 
	NOTE: The instructions, as presented to the participants before each block, are shown in Figure 1.
	<ol>
		<li>Instruct the participant to fixate at the center of the screen at the beginning of each trial.</li>
		<li>Inform the participant that 24 flickering distractor streams will appear on the screen and that two of them will be cued by white frames, which will either be flashed shortly or remain on the screen until the trial end.</li>
		<li>Ask the participant to execute a saccade towards the center of one of the two cued distractor streams at free choice. Emphasize that participants should move their eyes as fast and as accurately as possible upon the onset of the cues.</li>
		<li>Inform the participant that, for a short duration during the trial, a tilted Gabor will be presented randomly at one of the 24 distractor streams.</li>
		<li>Ask the participant to manually report whether the tilted Gabor was rotated clockwise or counterclockwise relative to the vertical by pressing the right or left arrow on the keyboard, respectively. Explain that a sound will be played if the orientation of the tilted Gabor is being reported incorrectly.</li>
	</ol>
	</li>
</ol>
5. Experimental Design, Stimuli, and Trial Chronology
<ol>
	<li>Ensure to partition the experiment into at least two experimental sessions on different days to guarantee participants&#39; concentration across the entire duration of the experiment. Within an experimental session, prompt participants to take short breaks in between consecutive blocks. 
	NOTE: This experiment consisted of 24 blocks, each including 290 online correct trials (all trials without fixation breaks and with a saccade onset between 50 and 350 ms after the saccade targets onset; incorrect trials were repeated at the end of a block), amounting to a total duration of about 5 h.</li>
	<li>Deliberately predefine stimulus features (color, luminance, and size), stimulus timing, and a viewing distance which ensures the desired angular stimulus size. While most features of the visual stimuli (e.g., size, luminance, and contrast) can be adjusted to account for specific experimental purposes based on piloting, precise stimulus timing is crucial to assess visual attention during the presaccadic interval.</li>
	<li>Stimuli and Trial Chronology
	<ol>
		<li>Present all stimuli on a gray (~19.5 cd/m2) background in order to minimize visual and screen aftereffects. 
		NOTE: A visualization of the experimental procedure can be found in Figure 2.</li>
		<li>Present a fixation target (FT) in the form of a black (~0 cd/m2) and white (~57 cd/m2) &#34;bull&#39;s eye&#34; (0.4&#176; radius) at the screen center at trial start. Remove the fixation target from the screen together with the onset of the saccade targets.</li>
		<li>Display 24 evenly spaced distractor streams (DS) at a radius of 10&#176; from the fixation target at the trial start. Use dynamic stimuli, alternating every 25 ms (40 Hz) between a vertical Gabor patch (frequency: 2.5 cpd; 100 % contrast; random phase selected each stream refresh; SD of the Gaussian window: 1.1&#176;; mean luminance: ~28.5 cd/m2) and a Gaussian pixel noise mask (made of approximately 0.22&#176; width pixels with the same Gaussian envelope as the Gabors). 
		NOTE: The use of flickering noise helps to minimize attentional capture due to sudden onsets that are normally associated with static stimuli and thus reduces discrimination target detectability without concurrent selective deployment of attention21.</li>
		<li>Between 300 and 600 ms (in steps of the screen refresh rate of ~8 ms) after the onset of the fixation target, present two saccade targets (ST1 and ST2) in the form of gray circles (~39 cd/m2; 1.1&#176; radius; 0.2&#176; width) surrounding two randomly chosen distractor streams. Ensure to vary the time of saccade target onset from trial to trial to avoid that participants adopt a predictive saccade execution pattern.
		<ol>
			<li>Randomly present the two saccade targets at an angular distance of either 30&#176; or 90&#176; across trials.</li>
			<li>Randomly display the saccade targets for either 50 ms (transient cueing condition: tST1+2) or until the end of the trial (continuous cueing condition: cST1+2) across trials.</li>
		</ol>
		</li>
		<li>Randomly present a discrimination target (DT) at one of the 24 distractor streams and between 75 and 175 ms after the onset of the saccade targets. Display the discrimination target, a tilted Gabor patch, rotated clockwise or counterclockwise by 12 &#176; relative to the vertical, for 25 ms to replace the vertical Gabor patch within the randomly selected distractor stream. Select the time window for discrimination target presentation to maximize the number of trials in which the discrimination target offset occurred before saccade onset. 
		NOTE: The applied tilt level of the discrimination target was derived from pretests with the objective of producing visual discrimination performance above chance level at attended locations. The tilt level can be generally changed but experimenters should first test whether participants can properly discriminate the target angle at least at the cued locations.</li>
		<li>Erase all stimuli from the screen 500 ms after the onset of the saccade targets such that only the gray background remains.</li>
		<li>Wait for the participant to indicate the orientation of the discrimination target via the keyboard (by pressing the left arrow for counterclockwise orientations and the right arrow for clockwise orientations) and play a feedback sound whenever participants report the discrimination target orientation incorrectly. Automatically launch the next trial once a manual response was given.</li>
	</ol>
	</li>
</ol>
6. Data Preprocessing and Analysis
<ol>
	<li>Process the recorded eye data before proceeding to final data analysis. Only include trials in which the participant maintained fixation within a 2&#176; radius around the fixation target without blinking and initiated a saccade landing between 7&#176; and 13&#176; from the fixation target (i.e. within &#177; 30 % of the instructed saccade size). Ensure that any measure of visual sensitivity was collected during the presaccadic interval by including only those trials in which the discrimination target offset occurred before the saccade onset. 
	NOTE: In total, 75.7% of all trials were included in the final analyses after eye data preprocessing.</li>
	<li>In order to analyze data as a function of the location of the discrimination target relative to the location of the saccade targets, rotate the stimulus configuration of each trial as to align the saccade target locations symmetrically around the geometrical angle 0 of the stimulus stream orbit.</li>
	<li>Split trials as a function of the saccade landing direction. To do so, divide the entire stimulus stream orbit into 24 even angular sectors of 15&#176; (&#177;7.5&#176;) centered on each distractor stream and combine trials entailing saccades directed towards the same respective sector.</li>
	<li>Define visual sensitivity as: d&#39; = z(hit rate) &#8722; z(false alarm rate). Count clockwise responses to clockwise discrimination targets as hits and clockwise responses to counterclockwise discrimination targets as false alarms (and vice versa). Substitute discrimination performance values of 100% and 0% by values of 99% and 1%, respectively, before transforming them into d&#39;. Transform discrimination performance values below the chance level (50% or d&#39; = 0) into negative d&#39; values.</li>
</ol>

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The authors have declared that no competing interests exist.

This experimental protocol employed the concurrent assessment of gaze behavior and presaccadic visual sensitivity in a free choice saccade task. It allowed us to analyze whether visual attention is indeed obligatorily coupled to oculomotor programming at the behavioral level and therefore systematically deployed at the endpoint of saccades. Two saccade targets were presented in close proximity (30&#176;)&#160;on half of the trials in which we observed a distinct global effect, reflected in a saccade landing distribution consisting of both, accurate and averaging saccades. To conclude on the spatial coupling between visual attention and the saccadic endpoint, visual sensitivity was analyzed and compared across different locations as a function of the saccade landing direction. While we observed a consistent and selective enhancement of visual sensitivity at the endpoint of accurate saccades, visual sensitivity was not enhanced at the endpoint of averaging saccades. Rather, visual sensitivity was equally facilitated at the two saccade targets before the execution of averaging saccades, suggesting that saccade averaging arises from unresolved attentional selection among the saccade targets. Our results, therefore, demonstrate that visual attention is not obligatorily deployed at the endpoint of the executed oculomotor program. A corrective saccade analysis, which demonstrated that the even deployment of visual sensitivity across the two saccade targets before averaging saccades did not systematically vary as a function the corrective saccade direction, further confirmed this interpretation. In this regard, our data are consistent with a recent model by Zirnsak et al.25 which assumes a target selection process that gradually builds up over time.

Importantly, our protocol differs from other behavioral studies that reported evidence for a dissociation between attention and saccades in several aspects. While some studies based their conclusion on saccadic reaction times14,15,16, we used a direct measure of visual spatial attention, namely visual sensitivity during saccade preparation. The specific parameters used throughout this protocol were effective in replicating the classical presaccadic shift of attention8,9 as evident in the consistent enhancement of visual sensitivity at the endpoint of accurate saccades. Thus, the protocol allowed for reliable detection of systematic modulations of visual attention specific to saccade preparation. This is an important prerequisite to validly interpret presaccadic attentional effects, and in particular, the observed absence of attentional enhancement at the endpoint of averaging saccades.
A central and distinct aspect of this protocol was the random presentation of the discrimination target among various locations. Thereby, we could sample visual sensitivity across the entire visual field, which consequently allowed us to not only determine whether attention is facilitated at the endpoint of saccades but also to investigate the spread of attention around this area including adjacent locations. The discrete allocation of attention at the two saccade targets (limited to less than ~2.6&#176;, the distance between two of our adjacent stimuli) we observed before averaging saccades contradicts an early account which suggested that averaging saccades may reflect a coarse processing of the visual scene17 and argues for&#160;an enhancement of local rather than global visual information processing. Further, the random presentation of the discrimination target rendered its location completely unpredictable to participants. Thus, our protocol generally facilitated an even deployment of visual attention across the visual field with respect to the discrimination task. We consider this fact important with regard to any potential attentional effects and conclusions related to saccade preparation.
However, since eye movements are not typically performed while trying to discriminate stimuli across the entire visual field in natural vision, the results obtained in this protocol can not unrestrictedly account for oculomotor behavior in every day life. Furthermore, the oculomotor task did inevitably bias the deployment of attention via the saccade target cueing. The saccade targets did not only introduce relevant oculomotor goals but also salient exogenous cues that likely attracted attention. Thus, it is possible that visual discrimination performance at the intermediate location was generally deteriorated due to some masking elicited by the two surrounding saccade targets. In order to decrease the impact of the saccade targets with respect to discrimination performance at the intermediate location and to evaluate potential masking effects, we decided to present the saccade targets only transiently (for 50 ms) instead of continuously (until the trial end) on half of the trials. Consequently, even though both cueing conditions introduced visual onsets at the saccade target locations, the saccade targets had always disappeared before the onset of the discrimination target in the transient cueing condition. While the majority of results were very consistent across both cueing conditions and were therefore combined in the final analysis, we indeed observed an indication of a masking effect in the continuous cueing condition relative to the transient cueing condition. Overall, irrespective of the saccade direction, visual sensitivity at the intermediate location was slightly decreased in the continuous compared to the transient cueing condition. Given the notion that transient saccade target cueing apparently minimizes masking of the intermediate location while still being effective in eliciting averaging saccades, future studies using a protocol similar to ours should consider employing transient cueing of targets. However, despite our efforts to minimize masking effects via the transient cueing of targets, we can not rule out that the transient cueing still introduced a forward masking effect, which might potentially account for the poor discrimination performance at the intermediate location to some extent.
Taken together, our protocol allowed to directly address the coupling between visual attention and oculomotor programming, and to reveal a distinct spatial dissociation between attention and the endpoint of averaging saccades at the behavioral level. Our results argue against a mandatory coupling between visual attention and oculomotor programming suggested in the premotor theory of attention. Future studies should employ paradigms including concurrent neurophysiological recordings within areas such as the FEF and SC to further resolve the coupling between visual attention and oculomotor programming.

Accumulated evidence argues for strong coupling between oculomotor and attentional control. The influential premotor theory of attention1,2 provides a particularly strict account regarding this coupling, suggesting that covert shifts of visual attention correspond to saccade programming without subsequent execution. Indeed, shared neuronal correlates of attentional and oculomotor control have been identified via functional magnetic resonance imaging (fMRI)3 and sub-threshold micro-stimulation of the&#160;Frontal Eye Fields (FEF) and the Superior Colliculi (SC) produces attentional benefits measured both behaviorally and electrophysiologically at the stimulated movement field position, even if no eye movements are induced4,5,6,7. Psychophysical experiments furthermore revealed that visual attention is consistently shifted towards the target of a saccade during oculomotor preparation8,9. However, dissociations at the neuronal level10,11,12 and observations that saccade preparation does not necessarily entail a corresponding shift of attention13,14,15,16 cast some doubt on an obligatory coupling between saccade programming and visual spatial attention.
Here, we revisited the nature of the coupling between attention and oculomotor programming at the behavioral level using a dual task which entailed a free choice saccade task and a visual discrimination task. Crucially, two saccade targets were presented at an angular distance of 30&#176; on half of the trials, producing a distinct global effect17,18,19,20 associated with a substantial number of saccades landing in between the two targets (averaging saccades). Since we randomly presented a discrimination target shortly before saccade onset at one out of 24 equidistant locations (including the two saccade target locations, the location in between them and 21 control locations), we were able to assess and compare the presaccadic deployment of visual attention when saccade goal and saccade endpoint were either spatially associated (accurate saccades) or dissociated (averaging saccades).
To test whether visual attention is an obligatory consequence of oculomotor programming, and, therefore, always shifted towards the saccade endpoint, we analyzed visual sensitivity for all 24 locations as a function of the saccade landing direction. While accurate saccades were associated with a consistent presaccadic enhancement of visual sensitivity at their endpoint, we found no such enhancement at the endpoint of averaging saccades. This dissociation rules out an obligatorily coupling of visual attention to the executed oculomotor program at the behavioral level and suggests that attentional and oculomotor control are dissociable at some cortical or subcortical processing stage. Importantly, we observed an equal enhancement of visual sensitivity at the two saccade targets before averaging saccades, suggesting that the global effect arises from unresolved saccade target selection before saccade onset.

<table><tbody><tr><td>Computer</td><td>Apple iMac (Cupertino, CA)&amp;nbsp;</td><td></td><td></td></tr><tr><td>CRT Screen</td><td>Sony GDM F900 (Tokyo, Japan)&amp;nbsp;</td><td></td><td>24 inch screen with a spatial resolution of 1024 x 640 pixels and&amp;nbsp; a vertical refresh rate of 120 Hz</td></tr><tr><td>Eye Tracker</td><td>EyeLink 1000 Desktop Mount (SR Research, Osgoode, Ontario, Canada)</td><td></td><td>operating at a sampling rate of 1 kHz</td></tr><tr><td>Software</td><td>Matlab (The MathWorks, Natick, MA) / toolboxes: Psychophics, EyeLink</td><td></td><td></td></tr></tbody></table>

investigating the deployment of visual attention before accurate and averaging saccades via eye tracking and assessment of visual sensitivity

This experimental protocol was designed to investigate whether visual attention is obligatorily deployed at the endpoint of saccades. To this end, we recorded the eye position of human participants engaged in a saccade task via eye tracking and assessed visual orientation discrimination performance at various locations during saccade preparation. Importantly, instead of using a single saccade target paradigm for which the saccade endpoint typically coincides roughly with the target, this protocol comprised the presentation of two nearby saccade targets, leading to a distinct spatial dissociation between target locations and saccade endpoint on a substantial number of trials. The paradigm allowed us to compare presaccadic visual discrimination performance at the endpoint of accurate saccades (landing at one of the saccade targets) and of averaging saccades (landing at an intermediate location in between the two targets). We observed a selective enhancement of visual sensitivity at the endpoint of accurate saccades but not at the endpoint of averaging saccades. Rather, before the execution of averaging saccades, visual sensitivity was equally enhanced at both targets, suggesting that saccade averaging follows from unresolved attentional selection among the saccade targets. These results argue against a mandatory coupling between visual attention and saccade programming based on a direct measure of presaccadic visual sensitivity rather than saccadic reaction times, which have been used in other protocols to draw similar conclusions. While our protocol provides a useful framework to investigate the relationship between visual attention and saccadic eye movements at the behavioral level, it can also be combined with electrophysiological measures to extend insights at the neuronal level.

Here, we only present some central, representative results. The entirety of results can be found in our recent publication23. Note that data were mainly analyzed irrespective of the duration of the saccade targets (i.e. transient and continuous cueing conditions were combined for the final analyses). For statistical comparisons, we drew 10,000 bootstrap samples (with replacement) from the distribution of single subject means and derived two-tailed p values from the distribution of differences between the bootstrapped samples.
The detection of saccade onsets and offsets was based on the velocity distribution of the gaze24. We used a moving average over 20 subsequent eye-position samples to determine saccade onsets/offsets whenever the velocity of the eye exceeded/fell below the median of the moving average by 3 SDs for at least 20 ms. Corrective saccades were defined as eye movements executed after the offline selected main saccade sequence and were only included in the respective corrective saccade analysis if they landed between 7&#176; and 13&#176; from the fixation target and were initiated within the first 500 ms following the main saccade sequence as well as before the participant&#39;s manual response.
Before proceeding to final data analysis, data were rotated (see 6.2). Consequently, after data rotation, the most counterclockwise saccade target ST1 was always represented at +45&#176;/+15&#176; (in the 90&#176; and 30&#176; conditions, respectively), the location BTW in between the saccade targets at 0&#176; (in both the 90&#176; and 30&#176; conditions), and the most clockwise saccade target ST2 at -45&#176;/-15&#176; (in the 90&#176; and 30&#176; conditions, respectively) relative to the angle 0. Locations other than ST1, ST2, and BTW were considered as control locations (CTRL) in both, the 90&#176; and 30&#176; conditions.
Our protocol allowed us to evaluate saccades in response to oculomotor competition among two saccade targets presented at different angular distances based on the recorded eye data. As expected, the saccade endpoint distributions associated with the 90&#176; (Figure 3A and 3C) and 30&#176; (Figure 3B and 3D) conditions differed substantially. We observed mostly accurate saccades towards one of the saccade targets in the 90 &#176; condition, where 41.0% &#177; 1.0% of saccades ended within the sector including the most counterclockwise saccade target ST1 and 41.8% &#177; 1.9% within the sector including the most clockwise saccade target ST2 (Figure 3C). In the 30&#176; condition, in contrast, participants executed a substantial number of averaging saccades. Here, 33.6% &#177; 2.4% of the saccades ended within the sector in between the 2 saccade targets BTW, 29.95% &#177; 1.6% ended within the sector including ST1, and 32.0% &#177; 1.8% within the sector including ST2 (Figure 3D).
Furthermore, the assessment of visual sensitivity at all 24 locations distributed across the visual field allowed us to analyze the spatial deployment of attention during oculomotor programming in detail. Overall, taking into account saccades of all directions, we observed a selective facilitation of visual sensitivity at the two saccade targets relative to the control locations CTRL (corresponding to the average across all positions except for ST1, ST2, and BTW) in both the 90&#176; (ST1: d&#39; = 2.2 &#177; 0.3 versus CTRL: d&#39; = 0.3 &#177; 0.1, p &#60; 0.0001; ST2: d&#39; = 2.2 &#177; 0.4 versus CTRL, p &#60; 0.0001; ST1 versus ST2, p = 0.8964; Figure 4A) and 30 &#176; (ST1: d&#39; = 2.2 &#177; 0.3 versus CTRL: d&#39; = 0.3 &#177; 0.1, p &#60; 0.0001; ST2: d&#39; = 2.1 &#177; 0.3 versus CTRL, p &#60; 0.0001; ST1 versus ST2, p = 0.6026; Figure 4B) conditions. While visual sensitivity at the intermediate location was significantly lower than at the saccade target locations (BTW: d&#39; = 0.6 &#177; 0.2 versus ST1, p &#60; 0.0001; BTW versus ST2, p &#60; 0.0001; Figure 4B), it was, however, slightly increased relative to the control locations in the 30&#176; condition (BTW versus CTRL, p = 0.0010).
In order to disentangle whether visual attention is obligatorily deployed at the endpoint of saccades, we analyzed visual sensitivity at all locations as a function of the saccade landing direction (see step 6.3 in the protocol). Crucially, the specific saccade landing distribution observed in the 30&#176; condition of this protocol made it possible to analyze the deployment of visual attention before saccades associated with spatially distinct endpoints in response to identical visual input. More specifically, by analyzing visual sensitivity before averaging saccades, we could determine whether or not attention shifts towards the endpoint of saccades even when it does not spatially coincide with a saccade goal. We observed that visual sensitivity was significantly enhanced at the endpoint of accurate saccades in both the 90&#176; (ST1+2 saccaded: d&#39; = 3.0 &#177; 0.4 versus ST1+2 non-saccaded: d&#39; = 1.7 &#177; 0.4, p &#60; 0.0001; Figure 4E) and the 30&#176; (ST1+2 saccaded: d&#39; = 2.7 &#177; 0.4 versus ST1+2 non-saccaded: d&#39; = 2.0 &#177; 0.3, p = 0.0080; Figure 4F) condition. In contrast, before averaging saccades, visual sensitivity was not enhanced at the saccade endpoint but slightly reduced (BTW saccaded: d&#39; = 0.4 &#177; 0.2 versus BTW non-saccaded: d&#39; = 0.7 &#177; 0.2, p &#60; 0.0001; Figure 4F). Thus, visual attention was not obligatorily shifted towards the endpoint of the upcoming saccade. Interestingly, averaging saccades were associated with an equal enhancement of visual sensitivity at the two surrounding saccade targets (ST1: d&#39; = 2.2 &#177; 0.4 versus ST2: d&#39; = 2.2 &#177; 0.4, p = 0.8402; Figure 4D), suggesting that attentional selection among the saccade targets was not readily resolved before the onset of averaging saccades.
To further evaluate a potential correlate of attentional selection before averaging saccades, data were analyzed as a function of the landing direction of corrective saccades, which can be frequently observed upon the execution of averaging saccades. We did not observe a significant benefit at the endpoint of corrective saccades following an averaging saccade (corrective saccade directed towards ST1+2: d&#39; = 2.8 &#177; 0.5 versus corrective saccade not directed towards ST1+2: d&#39; = 2.5 &#177; 0.8, p = 0.68300; Figure 5C), which supports the interpretation that attentional selection was not resolved before averaging saccades.
<img alt="Figure 1" class="xfigimg" src="/files/ftp_upload/59162/59162fig1.jpg" /> 
Figure 1: Instructions as presented to the participants. Visualization of the experimental instructions as presented to the participants at the beginning of each block. <a href="https://www.jove.com/files/ftp_upload/59162/59162fig1large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<img alt="Figure 2" class="xfigimg" src="/files/ftp_upload/59162/59162fig2.jpg" /> 
Figure 2: Experimental procedure and normalized saccade landing frequency maps.&#160;(A)&#160;Stimulus timing and display. Participants prepared a saccade from the fixation target (FT) to one of the two potential saccade targets (ST1 and ST2), presented simultaneously at two randomly chosen stimulus streams with an inter-target angular distance of either 90&#176; (top panels) or 30&#176; (bottom panels). The saccade targets were either shown continuously (cST1+2) or transiently (tST1+2). Stimulus streams could either be distractor streams (DS), composed of alternating vertical Gabors and masks (40 Hz) or discrimination target streams (DTS) which included the presentation of a brief discrimination target (DT, 25 ms), a clockwise or counterclockwise tilted Gabor, shown between 75 and 175 ms after the saccade targets onset. Participants saccaded towards one of the saccade targets and had to report the orientation of the discrimination target, appearing randomly at one of the 24 stimulus stream locations. Note that stimuli are sketched in order to increase their visibility. Actual stimuli match those shown in the stimulus streams depiction. (B)&#160;Normalized saccade landing frequency maps averaged across participants (n = 10) for the 90&#176; (top) and 30&#176; (bottom) conditions (collapsed across the transient and continuous ST presentation). This figure has been reprinted from Wollenberg et al. (2018)23. <a href="https://www.jove.com/files/ftp_upload/59162/59162fig2large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<img alt="Figure 3" class="xfigimg" src="/files/ftp_upload/59162/59162fig3.jpg" /> 
Figure 3: Saccade metrics.&#160;(A-B)&#160;Circular plots show the averaged frequency distribution of the saccade landing direction binned in evenly distributed angular sectors of 5&#176;, in the 90&#176; (A) and 30&#176; conditions (B). Stimulus configuration is rotated as to align the two saccade targets symmetrically around the geometrical angle zero (see central insets).&#160;(C-D)&#160;Bar graphs illustrate averaged frequency of trials as a function of the saccade landing direction binned in 24 evenly distributed angular sectors of 15&#176;. Data are shown for the three positions of interest (ST1, BTW and ST2) in the 90&#176; (C) and 30&#176; conditions (D). (E-H) Averaged saccade latency (E, F) and amplitude (G, H) observed for the same three positions of interest in the 90&#176; (E, G) and 30&#176; conditions (F, H). All data are shown irrespective of the duration (continuously or transiently) of the saccade targets. Light gray areas and error bars represent SEM. Polar plot black lines and corresponding light gray areas show linear interpolation between data points. This figure has been reprinted from Wollenberg et al. (2018)23. <a href="https://www.jove.com/files/ftp_upload/59162/59162fig3large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<img alt="Figure 4" class="xfigimg" src="/files/ftp_upload/59162/59162fig4.jpg" /> 
Figure 4: Visual sensitivity. (A-B). Circular plots show averaged visual sensitivity (d&#39;) as a function of the DT position in the 90&#176; (A) and 30&#176; conditions (B), irrespective of the duration of the saccade targets and across all saccade directions observed. Bar graphs illustrate visual sensitivity for four positions of interest (ST1, BTW, ST2, CTRL). (C-D) Visual sensitivity as a function of the DT position relative to the saccade landing direction in the 90&#176; (C) and 30&#176; conditions (D), irrespective of the duration of the saccade targets (blue: saccade to ST1; green: saccade to BTW; red: saccade to ST2). For each saccade direction, we took the average sensitivity for each discrimination target location. For example, the blue line plots visual sensitivity when saccades were made towards ST1 and the discrimination target was either at ST1 (+15&#176; on the polar plot), BTW (15&#176; counterclockwise to ST1; 0&#176; on the polar plot) or ST2 (30&#176; counterclockwise to ST1; + 345&#176; on the polar plot), and so on. (E-F) Bar graphs illustrate sensitivity observed for DT shown at the saccaded (purple: e.g., DT at ST1 and saccade to ST1) and the non-saccaded positions (light-purple: e.g. DT at ST1 and saccade to ST2 or BTW) in the 90&#176; (E) and the 30&#176; (F) conditions. Conventions are as in Figure 3. This figure has been reprinted from Wollenberg et al. (2018)23. <a href="https://www.jove.com/files/ftp_upload/59162/59162fig4large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<img alt="Figure 5" class="xfigimg" src="/files/ftp_upload/59162/59162fig5.jpg" /> 
Figure 5: Corrective saccades. (A) Circular plot shows averaged frequency distribution of the corrective saccade landing direction following an averaging saccade. (B)&#160;The bar graph illustrates averaged frequency of trials as a function of the corrective saccade landing direction following an averaging saccade for three positions of interest (ST1, BTW and ST2). (C) The bar graph illustrates visual sensitivity as a function of the direction of the first corrective saccade for all trials in which an averaging saccade was executed. Purple bars show visual sensitivity for trials in which the corrective saccade was directed towards the location at which the DT appeared (e.g. DT at ST1 and corrective saccade towards ST1). Light purple bars show visual sensitivity for trials in which the corrective saccade was directed towards a different location than the location at which the DT appeared (e.g. DT at ST1 and corrective saccade towards ST2 or BTW). Conventions are as in Figure 3-4. This figure has been reprinted from Wollenberg et al. (2018)23.&#160;<a href="https://www.jove.com/files/ftp_upload/59162/59162fig5large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>

Watch this Scientific Journal Video about Investigating the Deployment of Visual Attention Before Accurate and Averaging Saccades via Eye Tracking and Assessment of Visual Sensitivity at JoVE.com

Investigating the Deployment of Visual Attention Before Accurate and Averaging Saccades via Eye Tracking and Assessment of Visual Sensitivity

This experimental protocol combined eye tracking and the assessment of presaccadic visual sensitivity in a dual task paradigm, consisting of a free choice saccade task and a visual discrimination task, to investigate the deployment of visual spatial attention before both, accurate and averaging saccades.

This experimental protocol was designed to investigate whether visual attention is obligatorily deployed at the endpoint of saccades. To this end, we ...

investigating-deployment-visual-attention-before-accurate-averaging

Research

JoVE Journal

Behavior

7.0K Views.  Ludwig-Maximilians-Universität München. This experimental protocol combined eye tracking and the assessment of presaccadic visual sensitivity in a dual task paradigm, consisting of a free choice saccade task and a visual discrimination task, to investigate the deployment of visual spatial attention before both, accurate and averaging saccades.

Video: Investigating the Deployment of Visual Attention Before Accurate and Averaging Saccades via Eye Tracking and Assessment of Visual Sensitivity

VisualEyes: A Modular Software System for Oculomotor Experimentation

Eye movement studies have provided a strong foundation forming an understanding of how the brain acquires visual information in both the normal and dysfunctional brain.1 However, development of a platform to stimulate and store eye movements can require substantial programming, time and costs. Many systems do not offer the flexibility to program numerous stimuli for a variety of experimental needs. However, the VisualEyes System has a flexible architecture, allowing the operator to choose any background and foreground stimulus, program one or two screens for tandem or opposing eye movements and stimulate the left and right eye independently. This system can significantly reduce the programming development time needed to conduct an oculomotor study. The VisualEyes System will be discussed in three parts: 1) the oculomotor recording device to acquire eye movement responses, 2) the VisualEyes software written in LabView, to generate an array of stimuli and store responses as text files and 3) offline data analysis. Eye movements can be recorded by several types of instrumentation such as: a limbus tracking system, a sclera search coil, or a video image system. Typical eye movement stimuli such as saccadic steps, vergent ramps and vergent steps with the corresponding responses will be shown. In this video report, we demonstrate the flexibility of a system to create numerous visual stimuli and record eye movements that can be utilized by basic scientists and clinicians to study healthy as well as clinical populations.

Neural control and cognitive processes can be studied through eye movements. The VisualEyes software allows an operator to program stimuli on two computer screens independently using a simple, custom scripting language. The system can stimulate tandem eye movements (saccades and smooth pursuit) or opposing eye movements (vergence) or any combination.

Eye movement studies have provided a strong foundation forming an understanding of how the brain acquires visual information in both the normal and ...

Neuroscience

Eye Tracking Young Children with Autism

The rise of accessible commercial eye-tracking systems has fueled a rapid increase in their use in psychological and psychiatric research. By providing a direct, detailed and objective measure of gaze behavior, eye-tracking has become a valuable tool for examining abnormal perceptual strategies in clinical populations and has been used to identify disorder-specific characteristics1, promote early identification2, and inform treatment3. In particular, investigators of autism spectrum disorders (ASD) have benefited from integrating eye-tracking into their research paradigms4-7. Eye-tracking has largely been used in these studies to reveal mechanisms underlying impaired task performance8 and abnormal brain functioning9, particularly during the processing of social information1,10-11. While older children and adults with ASD comprise the preponderance of research in this area, eye-tracking may be especially useful for studying young children with the disorder as it offers a non-invasive tool for assessing and quantifying early-emerging developmental abnormalities2,12-13. Implementing eye-tracking with young children with ASD, however, is associated with a number of unique challenges, including issues with compliant behavior resulting from specific task demands and disorder-related psychosocial considerations. In this protocol, we detail methodological considerations for optimizing research design, data acquisition and psychometric analysis while eye-tracking young children with ASD. The provided recommendations are also designed to be more broadly applicable for eye-tracking children with other developmental disabilities. By offering guidelines for best practices in these areas based upon lessons derived from our own work, we hope to help other investigators make sound research design and analysis choices while avoiding common pitfalls that can compromise data acquisition while eye-tracking young children with ASD or other developmental difficulties.

Eye tracking has long been used to study gaze patterns in typically-developing individuals, but recent technological advancements have made its use with clinical populations, including autism, more feasible. While eye-tracking young children with autism can offer insight into early symptom manifestations, it involves methodological challenges. Suggestions for best practices are provided.

The rise of accessible commercial eye-tracking systems has fueled a rapid increase in their use in psychological and psychiatric research. By providing a ...

Medicine

A Method to Quantify Visual Information Processing in Children Using Eye Tracking

Visual problems that occur early in life can have major impact on a child's development. Without verbal communication and only based on observational methods, it is difficult to make a quantitative assessment of a child's visual problems. This limits accurate diagnostics in children under the age of 4 years and in children with intellectual disabilities. Here we describe a quantitative method that overcomes these problems. The method uses a remote eye tracker and a four choice preferential looking paradigm to measure eye movement responses to different visual stimuli. The child sits without head support in front of a monitor with integrated infrared cameras. In one of four monitor quadrants a visual stimulus is presented. Each stimulus has a specific visual modality with respect to the background, e.g., form, motion, contrast or color. From the reflexive eye movement responses to these specific visual modalities, output parameters such as reaction times, fixation accuracy and fixation duration are calculated to quantify a child's viewing behavior. With this approach, the quality of visual information processing can be assessed without the use of communication. By comparing results with reference values obtained in typically developing children from 0-12 years, the method provides a characterization of visual information processing in visually impaired children. The quantitative information provided by this method can be advantageous for the field of clinical visual assessment and rehabilitation in multiple ways. The parameter values provide a good basis to: (i) characterize early visual capacities and consequently to enable early interventions; (ii) compare risk groups and follow visual development over time; and (iii), construct an individual visual profile for each child.

A method is described to quantify the quality of visual information processing based on reflexive eye movements in response to specific visual modalities. Reaction times and fixation output parameters are used to characterize visual performance in children with and without visual impairments from 6 months of age.

Visual problems that occur early in life can have major impact on a child's development. Without verbal communication and only based on observational ...

Recording Horizontal Saccade Performances Accurately in Neurological Patients Using Electro-oculogram

Electro-oculogram (EOG) has been widely used for clinical eye movement recording, especially horizontal saccades, although the video-oculography (VOG) has largely taken the place of it nowadays due to its higher spatial accuracy. However, there are situations in which EOG has clear advantages over VOG, e.g., subjects with narrow eye clefts or having cataract lenses, and patients with movement disorders. The present article shows that if properly implemented, EOG can achieve an accuracy almost as good as VOG with substantial stability for recording, while circumventing problems associated with VOG recording. The present paper describes a practical method for recording horizontal saccades using oculomotor paradigms with high accuracy and stability by EOG in neurological patients. The necessary measures are to use an Ag-AgCl electrode with a wide plastic fringe capable of reducing noise, and to wait for sufficient light adaptation to occur. This waiting period also helps to lower the impedance between the electrodes and the skin, thereby ensuring stable signal recorded as time goes by. Furthermore, re-calibration is performed as needed during the task performance. Using this method, the experimenter can avoid drifts of signals, as well as contamination of artifacts or noise from the electromyogram and electroencephalogram, and can collect sufficient data for clinical evaluation of saccades. Thus when implemented, EOG can still be a method of high practicability that can be widely applied to neurological patients, but may be effective also for studies in normal subjects.

The article describes a practical method for recording horizontal eye movements with high accuracy by electro-oculogram in neurological patients, using a cup Ag-AgCl electrode with a wide plastic fringe. Stable measurement requires proper selection and fixation of electrodes, taking sufficient time for light adaptation to occur, and re-calibration as needed.

Electro-oculogram (EOG) has been widely used for clinical eye movement recording, especially horizontal saccades, although the video-oculography (VOG) has ...

Exploring Infant Sensitivity to Visual Language using Eye Tracking and the Preferential Looking Paradigm

We discuss the use of the preferential looking paradigm in eye tracking studies in order to study how infants develop, understand, and attend to the world around them. Eye tracking is a safe and non-invasive way to collect gaze data from infants, and the preferential looking paradigm is simple to design and only requires the infant to be attending to the screen. By simultaneously showing two visual stimuli that differ in one dimension, we can assess whether infants show different looking behavior for either stimulus, thus demonstrating sensitivity to that difference. The challenges in such experimental approaches are that experiments must be kept brief (no more than 10 min) and be carefully controlled such that the two stimuli differ in only one way. The interpretation of null results must also be carefully considered. In this paper, we illustrate a successful example of an infant eye tracking study with a preferential looking paradigm to discover that 6-month-olds are sensitive to linguistic cues in a signed language despite having no prior exposure to signed language, suggesting that infants possess intrinsic or innate sensitivities to these cues.

Eye tracking studies using a preferential looking paradigm can be used to study infants&#39;&#160;emerging understanding of, and attention to, their external visual world.

We discuss the use of the preferential looking paradigm in eye tracking studies in order to study how infants develop, understand, and attend to the world ...

Assessing Binocular Central Visual Field and Binocular Eye Movements in a Dichoptic Viewing Condition

Macular degeneration typically results in heterogeneous binocular central visual defects. Currently available approaches to assess central visual field, like the microperimetry, can test only one eye at a time. Therefore, they cannot explain how the defects in each eye affect the binocular interaction and real-world function. Dichoptic stimulus presentation with a gaze-controlled system could provide a reliable measure of monocular/binocular visual fields. However, dichoptic stimulus presentation and simultaneous eye-tracking are challenging because optical devices of instruments that present stimulus dichoptically (e.g., haploscope) always interfere with eye-trackers (e.g., infrared video-based eye-trackers). Therefore, the goals were 1) to develop a method for dichoptic stimulus presentation with simultaneous eye-tracking, using 3D-shutter glasses and 3D-ready monitors, that is not affected by interference and 2) to use this method to develop a protocol for assessing central visual field in subjects with central vision loss. The results showed that this setup provides a practical solution for reliably measuring eye-movements in dichoptic viewing condition. In addition, it was also demonstrated that this method can assess gaze-controlled binocular central visual field in subjects with central vision loss.

Presented here is a protocol for assessing binocular eye movements and gaze-controlled central visual field screening in participants with central vision loss.

Macular degeneration typically results in heterogeneous binocular central visual defects. Currently available approaches to assess central visual field, ...

Eye Tracking During A Complex Aviation Task For Insights Into Information Processing

Eye tracking has been used extensively as a proxy to gain insight into the cognitive, perceptual, and sensorimotor processes that underlie skill performance. Previous work has shown that traditional and advanced gaze metrics reliably demonstrate robust differences in pilot expertise, cognitive load, fatigue, and even situation awareness (SA).
This study describes the methodology for using a wearable eye tracker and gaze mapping algorithm that captures naturalistic head and eye movements (i.e., gaze) in a high-fidelity flight motionless simulator. The method outlined in this paper describes the area of interest (AOI)-based gaze analyses, which provides more context related to where participants are looking, and dwell time duration, which indicates how efficiently they are processing the fixated information. The protocol illustrates the utility of a wearable eye tracker and computer vision algorithm to assess changes in gaze behavior in response to an unexpected in-flight emergency.
Representative results demonstrated that gaze was significantly impacted when the emergency event was introduced. Specifically, attention allocation, gaze dispersion, and gaze sequence complexity significantly decreased and became highly concentrated on looking outside the front window and at the airspeed gauge during the emergency scenario (all p values &#60; 0.05). The utility and limitations of employing a wearable eye tracker in a high-fidelity motionless flight simulation environment to understand the spatiotemporal characteristics of gaze behavior and its relation to information processing in the aviation domain are discussed.

Eye tracking is a non-invasive method to probe information processing. This article describes how eye tracking can be used to study gaze behavior during a flight simulation emergency task in low-time pilots (i.e., &lt;350 flight hours).

Eye tracking has been used extensively as a proxy to gain insight into the cognitive, perceptual, and sensorimotor processes that underlie skill ...

Using Saccadometry with Deep Brain Stimulation to Study Normal and Pathological Brain Function

The oculomotor system involves a large number of brain areas including parts of the basal ganglia, and various neurodegenerative diseases including Parkinson's and Huntington's can disrupt it. People with Parkinson's disease, for example, tend to have increased saccadic latencies. Consequently, the quantitative measurement of saccadic eye movements has received considerable attention as a potential biomarker for neurodegenerative conditions. A lot more can be learned about the brain in both health and disease by observing what happens to eye movements when the function of specific brain areas is perturbed. Deep brain stimulation is a surgical intervention used for the management of a range of neurological conditions including Parkinson's disease, in which stimulating electrodes are placed in specific brain areas including several sites in the basal ganglia. Eye movement measurements can then be made with the stimulator systems both off and on and the results compared. With suitable experimental design, this approach can be used to study the pathophysiology of the disease being treated, the mechanism by which DBS exerts it beneficial effects, and even aspects of normal neurophysiology.

This paper describes the use of quantitative measurement of eye movements in conjunction with stimulation of focal areas of the deep brain in order to study physiology, pathophysiology, and the mechanisms of deep brain stimulation.

The oculomotor system involves a large number of brain areas including parts of the basal ganglia, and various neurodegenerative diseases including ...

Characterizing the Relationship Between Eye Movement Parameters and Cognitive Functions in Non-demented Parkinson's Disease Patients with Eye Tracking

Cognitive impairment is a common phenomenon in Parkinson&#8217;s disease that has implications on the prognosis. A simple, noninvasive and objective proxy measurement of cognitive function in Parkinson&#8217;s disease will be helpful in detecting early cognitive decline. As a physiological metric, eye movement parameter is not confounded by the subject&#39;s attributes and intelligence and can function as a proxy marker if it correlates with cognitive functions. To this end, this study explored the relationship between the eye movement parameters and performance in cognitive tests in multiple domains. In the experiment, a visual search task with eye tracking was set up, where subjects were asked to look for a number embedded in an array of alphabets scattered randomly on a computer screen. The differentiation between the number and the alphabet is an overlearned task such that the confounding effect of cognitive ability on the eye movement parameters is minimized. The average saccadic amplitude and fixation duration were captured and calculated during the visual search task. The cognitive assessment battery covered domains of frontal-executive functions, attention, verbal and visual memory. It was found that prolonged fixation duration was associated with poorer performance in verbal fluency, visual and verbal memory, allowing further exploration on the use of eye movement parameters as proxy markers for cognitive function in Parkinson&#8217;s disease patients. The experimental paradigm has been found to be highly tolerable in our group of Parkinson&#39;s disease patients and could be applied transdiagnostically to other disease entities for similar research questions.

Here, we present a protocol to study the relationship between the eye movement parameters and cognitive functions in non-demented Parkinson&#39;s disease patients. The experiment used an eye tracker to measure the saccadic amplitude and fixation duration in a visual search task. The correlation with performance in multi-domain cognitive tasks was subsequently measured.

Cognitive impairment is a common phenomenon in Parkinson&#8217;s disease that has implications on the prognosis. A simple, noninvasive and objective proxy ...

A Visuospatial Planning Task Coupled with Eye-Tracker and Electroencephalogram Systems

The planning process, characterized by the capability to formulate an organized plan to reach a goal, is essential for human goal-directed behavior. Since planning is compromised in several neuropsychiatric disorders, the implementation of proper clinical and experimental tests to examine planning is critical. Due to the nature of the deployment of planning, in which several cognitive domains participate, the assessment of planning and the design of behavioral paradigms coupled with neuroimaging methods are current challenges in cognitive neuroscience. A planning task was evaluated in combination with an electroencephalogram (EEG) system and eye movement recordings in 27 healthy adult participants. Planning can be separated into two stages: a mental planning stage in which a sequence of steps is internally represented and an execution stage in which motor action is used to achieve a previously planned goal. Our protocol included a planning task and a control task. The planning task involved solving 36 maze trials, each representing a zoo map. The task had four periods: i) planning, where the subjects were instructed to plan a path to visit the locations of four animals according to a set of rules; ii) maintenance, where the subjects had to retain the planned path in their working memory; iii) execution, where the subjects used eye movements to trace the previously planned path as indicated by the eye-tracker system; and iv) response, where the subjects reported the order of the visited animals. The control task had a similar structure, but the cognitive planning component was removed by modifying the task goal. The spatial and temporal patterns of the EEG revealed that planning induces a gradual and lasting rise in frontal-midline theta activity (FM&#952;) over time. The source of this activity was identified within the prefrontal cortex by source analyses. Our results suggested that the experimental paradigm combining EEG and eye-tracker systems was optimal for evaluating cognitive planning.

The study of cognitive planning combining EEG and eye-tracking systems provides a multimodal approach to investigate the neural mechanisms that mediate cognitive control and goal-directed behavior in humans. Here, we describe a protocol for investigating the role of brain oscillations and eye movements in planning performance.

The planning process, characterized by the capability to formulate an organized plan to reach a goal, is essential for human goal-directed behavior. Since ...