Name: eye-tracking control to assess cognitive functions in patients with amyotrophic lateral sclerosis
Uploaded: 2016-10-13T15:00:00.000+00:00
Duration: 7 min
Description: Watch this Scientific Journal Video about Eye-Tracking Control to Assess Cognitive Functions in Patients with Amyotrophic Lateral Sclerosis at JoVE.com

The authors would like to thank Ralf K&#252;hne for technical support. This work was funded by the Deutsche Forschungsgemeinschaft (DFG) and the Bundesministerium f&#252;r Bildung und Forschung (BMBF #01GM1103A). This is an EU Joint Programme-Neurodegenerative Disease Research (JPND) project. The project is supported through the following organizations under the aegis of JPND-e.g., Germany, Bundesministerium f&#252;r Bildung und Forschung (BMBF, FKZ), Sweden, Vetenskapr&#229;det Sverige, Poland, Narodowe Centrum Bada&#324; i Rozwoju (NCBR).

The study was approved by the Ethics Committee of the University of Ulm (Statement No. 19/12) and the protocol described therefore follows their guidelines. All participants gave written informed consent.
1. Stimuli and Testing Environment
<ol>
	<li>To keep distractions to a minimum perform the research in a dark or a very dimly lit and quiet room.</li>
	<li>Use an appropriate eye tracking device. 
	NOTE: There are a wide variety of devices available to perform eye movement studies. In the present research a portable eye movement recording device with goggles was used, which synchronously measure binocular eye positions, using two integrated cameras with an infrared light emitting diode (IR LEDs), one for each eye18.
	<ol>
		<li>To ensure optimal eye-tracking, adjust the cameras manually by tilting them in all 6 degrees of freedom (3 translational, 3 rotational) until eye movement detection is optimal. 
		NOTE: The measurements of the system are displayed in real-time on an experimenter&#39;s screen to monitor recording quality and participants&#39; response behavior. The key features of the system are described below and detailed specifications are given in Table 1.</li>
	</ol>
	</li>
	<li>Implement a standardized oculomotor testing paradigm, which is able to detect deficits in eye movement control. 
	NOTE: This can be a series of tasks like smooth pursuit or saccade tasks, in which participants with impaired eye movement control perform badly (e.g., the methods described by Gorges et al. 201511). These participants have to be excluded from further testing.</li>
	<li>Present tasks using appropriate software that projects the stimuli on a hemi-cylindrical screen via a projector mounted above the subject&#39;s head11. Additionally, ensure that a red laser spot (diameter: 0.3&#176;, position: 10&#176; vertical) is present for the D2-test.</li>
	<li>Seat the participants on an elevated chair with an adjustable chin rest, so that eye-to-screen distance is approximately 150 cm.</li>
	<li>Use set A and B of the CPM (12 stimuli for each set) for the first part of the experiment. Show these stimuli as 22&#176; long/15&#176; high matrices with six possible alternatives depicted below, which might fit in a 6&#176; wide and 5&#176; high blank space cut out from the matrix.</li>
	<li>For the D2-test, use the five blocks with 47 stimuli, corresponding to line 2 - 6 of the standard D2-test15, and depict them one stimulus after another in the middle of the screen with a height of 11&#176; and a width of 2.5&#176;. Make sure each stimulus lasts for 2,000 msec.</li>
</ol>
2. Running the Experiment
<ol>
	<li>Before the experiment starts, ask participants to fill out a written informed consent form to ensure the study is in accordance with ethical standards.</li>
	<li>Give general instructions concerning the purpose and procedure of the experiment and control for CNS-active drugs, i.e., ask the participant if he/she is currently taking any medication which affects alertness and therefore cognitive performance.</li>
	<li>Turn off all devices which might be a potential disturbance, such as mobile phones or pagers.</li>
	<li>Seat participants comfortably with the chin rest in optimal position. Ensure that the whole screen is visible and ask the participant to maintain posture during the whole experiment.</li>
	<li>Ask participants to place their head on the chin rest and place the videooculography goggles onto their head. Adjust them to individual head size/shape. 
	NOTE: Thereby, the best possible compromise between comfort for the participant and minimal risk of unwanted slipping during measurement must be made.</li>
	<li>Make sure that both eyes are visible on the experimenter&#39;s screen, where the images of the two eye movement recording cameras within the goggles are displayed and then focus the cameras to center the images on the screen. 
	NOTE: This is important for optimal detection and tracking of the pupil as an improper acuity can lead to a disturbed signal.</li>
	<li>To ensure continuous recording of eye movements at all times, start calibration of the system by instructing the participant to look in each corner of the hemi-cylindrical screen. In case the signal is lost, change the angle of the camera tracking the respective pupil of the eye to resolve the problem.</li>
	<li>Start the standardized oculomotor testing paradigm described above and exclude all patients with substantial visual impairments as these will cause corrupted task performance.</li>
	<li>Instruct the participant to track a single spot on the screen, oscillating horizontally (&#177; 20&#176;) and then vertically (&#177; 15&#176;) with a frequency of 0.125 Hz to map the non-calibrated orthogonalized &#39;raw&#39; data from the eye movement recording device with respect to the &#39;true&#39; orthogonalized eye position for calibration of the system.</li>
	<li>Check if calibration is acceptable, i.e., if the &#39;true&#39; eye movement and the &#39;raw&#39; data are spatially and temporally synchronized and then instruct the participant to not move the head as this might result in bad data quality. 
	NOTE: Position of the videooculography device and the subject is expected to be stationary during the course of the experiment, so that there is no need for re-calibration.</li>
	<li>Explain the procedure of the training session for the CPM:
	<ol>
		<li>Instruct the subjects to identify the missing pieces below the upcoming matrices displayed on the hemi-cylindrical screen for which they have infinite time. After making a choice, have the subject close their eyes for at least 250 msec to start off a green frame outlining all of the possible alternatives of missing pieces for 1,500 msec each.</li>
		<li>Have the participant choose the alternative they think is correct by closing their eyes for at least 250 msec while their choice is enframed.</li>
		<li>Project the choice separately on the hemi-cylindrical screen. Ask the participants to confirm. If the participant confirms, instruct them to close their eyes again for at least 250 msec.</li>
		<li>Instruct the participants that the next stimulus (matrix with 6 alternatives of missing pieces) will automatically (again, presented by the software described in step 2) appear and that this will be done four times with training stimuli taken from set AB of the CPM14.</li>
	</ol>
	</li>
	<li>Answer any questions subjects might have about the procedure. Then, instruct the participants to choose the missing piece of the matrix, as they have learned during the training session and start the CPM (Figure 1).</li>
	<li>Explain the procedure of the training session for the D2-test:
	<ol>
		<li>Instruct participants to direct their gaze to the center of the screen and observe 47 stimuli separately (47 d&#39;s corresponding to line 1 of the standard D2-test).</li>
		<li>Instruct the participants to look at the red laser spot positioned above the stimuli whenever a &#34;d&#34; with two dashes is presented until the next stimulus appears. NOTE: If no target stimulus is presented the gaze needs to be focused at the center of the screen where the next stimulus will be presented.</li>
	</ol>
	</li>
	<li>Answer any questions subjects might have about the procedure. Then, instruct the participant to proceed for the following five blocks of 47 stimuli, similar to the training session and start the D2-test.</li>
	<li>For quality control, inspect the data obtained from each session for each subject carefully (visually by a trained experimenter). Check if data quality is corrupted, for example due to technical difficulties, corrupted eye movements or misunderstandings.</li>
	<li>Thank subjects for their participation and answer all questions during the experiment.</li>
</ol>

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K., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+effects+of+executive+and+behavioral+dysfunction+in+the+course+of+ALS.">The effects of executive and behavioral dysfunction in the course of ALS.</a> Neurology. 65 (11), 1774-1777 (2005).</li><li>Donaghy, C., Thurtell, M. J., Pioro, E. P., Gibson, J. M., Leigh, R. J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Eye+movements+in+amyotrophic+lateral+sclerosis+and+its+mimics:+a+review+with+illustrative+cases.">Eye movements in amyotrophic lateral sclerosis and its mimics: a review with illustrative cases.</a> J. Neurol. Neurosurg. Psychiatry. 82 (1), 110-116 (2011).</li><li>Mizutani, T., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Development+of+ophthalmoplegia+in+amyotrophic+lateral+sclerosis+during+long-term+use+of+respirators.">Development of ophthalmoplegia in amyotrophic lateral sclerosis during long-term use of respirators.</a> J. Neurol. Sci. 99 (2-3), 311-319 (1990).</li><li>Khin Khin, E., Minor, D., Holloway, A., Pelleg, A. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Decisional+Capacity+in+Amyotrophic+Lateral+Sclerosis.">Decisional Capacity in Amyotrophic Lateral Sclerosis.</a> J. Am. Acad. Psychiatry Law. 43 (2), 210-217 (2015).</li><li>K&#252;bler, A., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Patients+with+ALS+can+use+sensorimotor+rhythms+to+operate+a+brain-computer+interface.">Patients with ALS can use sensorimotor rhythms to operate a brain-computer interface.</a> Neurology. 64 (10), 1775-1777 (2005).</li><li>Connolly, S., Galvin, M., Hardiman, O. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=End-of-life+management+in+patients+with+amyotrophic+lateral+sclerosis.">End-of-life management in patients with amyotrophic lateral sclerosis.</a> Lancet Neurol. 14 (4), 435-442 (2015).</li></ol>

The authors declare that they have no competing financial interests.

It is a challenging task to successfully assess the cognitive status of patients with ALS who are unable to speak and write. The use of videooculography systems provides a promising approach. The hereby presented technique is reliable in detecting cognitive deficits, which play a pivotal role in the context of carer burden and disease management20 in ALS patients. Also, the oculomotor versions of the CPM and the D2-test correlate significantly with their respective standard paper-pencil versions, but further support is needed to claim the usefulness in a clinical context.
The researcher needs to make sure that eye movement recordings are as noise free as possible to allow for sufficient data quality. Therefore, it is important for researchers to select an eye movement recording device with an appropriate sampling rate. Usually, sampling rates range between 50 Hz and 1,000 Hz. In general, the more subtle oculomotor measurements are required for the task, the higher temporal resolution needs to be used. It needs to be yielded that higher sampling rates usually require a larger restriction of head movement. Also, to allow for a higher sampling rate, researchers may record the movement of just one eye. Another important parameter is spatial accuracy, which is expressed in degrees of visual angle and in this work is 0.05&#176; - 0.1&#176;, depending on pupil size. Again, the higher the demands on visual accuracy in the task the better spatial resolution needs to be. Furthermore, a major issue in quality of the obtained oculomotor data is head movement, which has to be restricted to a tolerable minimum. Most eye-tracking studies use a chin rest and/or a head mounted device. If possible, combine both options as this restricts head movement and its accompanying confounds most. However, this is not possible in all patients, e.g., patients with very serious physical impairments, and might then be altered according to the subject&#39;s capacities. It should also be noted that newer devices, which calculate the eye position via a small stationary camera placed in front of the subject underneath the screen on which stimuli are presented, do not require goggles or a chin rest, while also sufficiently correcting for head movements.
The cognitive tests are interchangeable with other standard neuropsychological tests, depending on the cognitive domain one is interested in. To use other tests in ALS patients, they just need to be adapted to a format in which answers can be given using eye movements. Especially given the rapid technological advance in the field of eye-tracking, further increasing acuity, flexibility and handiness, this methodology might also be suited for a large variety of cognitive research questions in different clinical samples.
Some patients might be too impaired in their cognitive abilities to correctly understand the instructions of the tasks used in this study. One other serious limitation for the use of eye-tracking technologies in ALS patients are potential oculomotor abnormalities, or even complete loss of eye movement control, previously reported in patients with the disease21,22. These abnormalities are very subtle in early stages of the disease and sequentially impact more basic oculomotor functions in the progress of ALS pathology11.
The protocol presented here is therefore only suited for those ALS patients unable to speak and write but still able to control their eye movements. This however encompasses a comparably large group, for which reliable information about cognitive status is crucial23. For patients with no satisfactory eye movement control or ability to blink, this protocol is not suited. However, another hand and speech-motor free way to assess cognitive function in these cases is brain-computer interface control, as has been done in recent work24.
The technique presented here is fast, easy to administer, user-friendly and potentially allows clinicians and researchers to perform neuropsychological assessments with patients who are severely physically impaired and therefore not able to undergo paper-pencil based testing anymore, such as - but not necessarily limited to - patients with ALS, using an eye-tracking device.
It provides an opportunity to gain information about potential cognitive deficits in patients with complete paralysis, i.e., information which then plays a critical role in the context of life prolonging therapeutic treatments and end-of-life decision making in ALS6,25.
In the future, mobile devices with high acuity and head movement tolerability which can be handled more flexibly might be used to comfortably assess cognition in immobile patients at their bedside, eliminating the need for a special testing environment. Also, the use of other, possibly more sophisticated eye-tracking controlled experimental procedures is needed to assess more subtle cognitive deficits in severely impaired patients.

Amyotrophic lateral sclerosis (ALS) is a fatal neurodegenerative disorder usually leading to death within 3 to 5 years. In the course of the pathology, patients present with progressive loss of respiratory and bulbar functioning as well as impairments in movement abilities1. It shares some clinical, pathological, and genetic features with frontotemporal dementia2 and it is well documented that about 30% of ALS patients exhibit cognitive deficits3. These deficits are most prominent in the domains of executive function, verbal fluency and language4 and have an influence on survival5, compliance6 and carer burden7. Thus, reliable neuropsychological assessment is crucial in this disease.
Advancing impairments in motor and speech abilities are, however, a limiting factor for thorough evaluation of cognitive abilities in later stages of the disease8. Here, oculomotor based approaches seem to be very promising, as basic eye movement control remains intact for a comparably long time during the course of ALS for the majority of patients9. Eye-tracking parameters itself have been used to gain information about the cognitive status of patients with ALS10 and also correlate with the sequential spreading pattern of ALS11. Eye movement as a means to control cognitive tests in the context of ALS has also been studied in previous works. One study has successfully demonstrated its usability in healthy controls using an oculomotor based version of the Trail-Making Test12, whereas another found it suitable to distinguish between healthy controls and ALS patients based on cognitive performance and to discriminate between cognitively more and less impaired patients13.
The research described here used an oculomotor based methodology to study cognitive impairments in ALS patients, specifically in the domain of executive functioning. Two well validated and commonly used neuropsychological tests were adapted to eye movement control: the Raven&#39;s coloured progressive matrices (CPM)14 and the D2-test15. The CPM is a non-verbal instrument used to measure executive and visuospatial abilities as well as fluid intelligence. The D2-test is also a non-verbal tool used to uncover executive dysfunction in the domains of selective and sustained attention and visual processing speed. Both are widely used clinical tools which have been successfully employed in previous studies assessing potential cognitive decline during the course of the disease16 and the neuropsychological status of ALS patients compared to healthy controls17.
The goal of this work was to show the requirements for successful evaluation of cognitive deficits in ALS independent of movement and speech disabilities using a reliable, eye-tracking based version of the CPM and the D2-test. Importantly, the method described here has the potential to be expanded to study other populations of patients with severe motor impairments.

<table><tbody><tr><td>EyeSeeCam</td><td>EyeSeeTec GmbH; 82256 F&amp;uuml;rstenfeldbruck, Germany</td><td></td><td>Videooculography device</td></tr></tbody></table>

eye-tracking control to assess cognitive functions in patients with amyotrophic lateral sclerosis

Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disorder with pathological involvement of upper and lower motoneurons, subsequently leading to progressive loss of motor and speech abilities. In addition, cognitive functions are impaired in a subset of patients. To evaluate these potential deficits in severely physically impaired ALS patients, eye-tracking is a promising means to conduct cognitive tests. The present article focuses on how eye movements, an indirect means of communication for physically disabled patients, can be utilized to allow for detailed neuropsychological assessment. The requirements, in terms of oculomotor parameters that have to be met for sufficient eye-tracking in ALS patients are presented. The properties of stimuli, including type of neuropsychological tests and style of presentation, best suited to successfully assess cognitive functioning, are also described. Furthermore, recommendations regarding procedural requirements are provided. Overall, this methodology provides a reliable, easy to administer and fast approach for assessing cognitive deficits in patients who are unable to speak or write such as patients with severe ALS. The only confounding factor might be deficits in voluntary eye movement control in a subset of ALS patients.

For the purpose of the research presented here, i.e.,&#160;the development of a reliable oculomotor based neuropsychological assessment for ALS patients, in-house developed software stores the subject&#39;s choices of the CPM in a separate file, allowing for manual computation of the percentage of correct answers. For the D2-test, a record of the vertical eye movements is manually analyzed using a threshold of + 5&#176; for detection of a relevant response. Recordings are assigned to each stimulus presentation and percentage of correct answers can subsequently be computed. There are many options available of how data can be analyzed, either based on visual inspection of the eye movements or fully computerized, depending on the neuropsychological tasks used.
Figure 2 shows the good congruency between the oculomotor and the standard version (i.e., applied according to standard protocol using paper versions to be marked with a pencil) of the CPM, in a sample of ALS patients (R&#178; = 0.712; p = 0.001). Figure 3 depicts the results from a comparison between cognitively more and less impaired ALS patients, indicating statistically significant group differences in the CPM (p &#60; 0.001) and the D2-test (p = 0.024)13. This further confirms the usability of this technique as it reliably distinguishes between more and less cognitively impaired ALS patients.
<img alt="Figure 1" src="/files/ftp_upload/54634/54634fig1.jpg" /> 
Figure 1.&#160;Illustration of Eye-tracking Based CPM. Example of the CPM selection procedure as displayed on the participants screen (upper panel) with its corresponding traces of horizontal (upper line) and vertical (lower line) eye positions (lower panel); a scale bar indicating time is given on the bottom of the Figure. When the subject has mentally decided for a choice, movement of a green frame along the presented alternatives of missing pieces which is triggered by a prolonged blink of the subject (A). Selection of one alternative of a missing piece is performed by another prolonged blink of the subject (B). Subsequently, presentation of subject&#39;s choice appears separately and confirmation of the choice is done via closing the subject&#39;s eyes for at least 250 msec (C). Modified from Keller et al. 201513. <a href="https://www-jove-com.remotexs.ntu.edu.sg/files/ftp_upload/54634/54634fig1large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<img alt="Figure 2" src="/files/ftp_upload/54634/54634fig2.jpg" /> 
Figure 2:. Congruency between Oculomotor and Standard Version of the CPM. Correlation between results from the standard and the oculomotor condition of the CPM. Given is the percentage of correct answers in the oculomotor (x-axis) and the standard paper-pencil (y-axis) condition of the CPM in ALS patients (R&#178; = 0.712; p = 0.001). <a href="https://www-jove-com.remotexs.ntu.edu.sg/files/ftp_upload/54634/54634fig2large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<img alt="Figure 3" src="/files/ftp_upload/54634/54634fig3.jpg" /> 
Figure 3. Comparison Between More and Less Cognitively Impaired Patients. Subjects were divided into more and less cognitively impaired according to a median split on their results in the Edinburgh Cognitive and Behavioural ALS Screen (ECAS)19, a standard tool for neuropsychological assessment in ALS patients. Shown are boxplots depicting the percentage of correct answers in the eye-tracking versions of the CPM and the D2-test for both groups. The error bars indicate the highest and lowest percentage scored. Modified from Keller et al. 201513. <a href="https://www-jove-com.remotexs.ntu.edu.sg/files/ftp_upload/54634/54634fig3large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<table border="1" fo:keep-together.within-page="1" fo:keep-with-next.within-page="always">
	<tbody>
		<tr>
			<td>PARAMETER</td>
			<td>VALUE</td>
		</tr>
		<tr>
			<td>Cameras</td>
			<td>2</td>
		</tr>
		<tr>
			<td>IR LED Wavelength</td>
			<td>&#62; 850 nm</td>
		</tr>
		<tr>
			<td>Total Head Mount Weight</td>
			<td>60 g</td>
		</tr>
		<tr>
			<td>Sampling Rate</td>
			<td>220 Hz</td>
		</tr>
		<tr>
			<td>Spatial Resolution</td>
			<td>0.05&#176; -&#160; 0.1&#176;</td>
		</tr>
		<tr>
			<td>Noise Level</td>
			<td>0.015&#176;</td>
		</tr>
		<tr>
			<td>Accuracy</td>
			<td>1&#176;</td>
		</tr>
		<tr>
			<td>Distance Camera-Eye</td>
			<td>~ 50 mm</td>
		</tr>
	</tbody>
</table>
Table 1: Specifications of the Videooculography System. Important parameters and their respective values of the system used.

Watch this Scientific Journal Video about Eye-Tracking Control to Assess Cognitive Functions in Patients with Amyotrophic Lateral Sclerosis at JoVE.com

Eye-Tracking Control to Assess Cognitive Functions in Patients with Amyotrophic Lateral Sclerosis

Cognitive deficits are common in about one third of patients with amyotrophic lateral sclerosis, a neurological condition leading to progressive impairments in speech and movement abilities. To conduct cognitive tests in patients unable to speak or write a reliable and easy to administer eye-tracking paradigm was developed.

Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disorder with pathological involvement of upper and lower motoneurons, subsequently leading to ...

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Nanyang Technological University

Research

JoVE Journal

Behavior

8.1K Views.  Ulm University. Cognitive deficits are common in about one third of patients with amyotrophic lateral sclerosis, a neurological condition leading to progressive impairments in speech and movement abilities. To conduct cognitive tests in patients unable to speak or write a reliable and easy to administer eye-tracking paradigm was developed.

Video: Eye-Tracking Control to Assess Cognitive Functions in Patients with Amyotrophic Lateral Sclerosis

Using Eye Movements to Evaluate the Cognitive Processes Involved in Text Comprehension

The present article describes how to use eye tracking methodologies to study the cognitive processes involved in text comprehension. Measuring eye movements during reading is one of the most precise methods for measuring moment-by-moment (online) processing demands during text comprehension. Cognitive processing demands are reflected by several aspects of eye movement behavior, such as fixation duration, number of fixations, and number of regressions (returning to prior parts of a text). Important properties of eye tracking equipment that researchers need to consider are described, including how frequently the eye position is measured (sampling rate), accuracy of determining eye position, how much head movement is allowed, and ease of use. Also described are properties of stimuli that influence eye movements that need to be controlled in studies of text comprehension, such as the position, frequency, and length of target words. Procedural recommendations related to preparing the participant, setting up and calibrating the equipment, and running a study are given. Representative results are presented to illustrate how data can be evaluated. Although the methodology is described in terms of reading comprehension, much of the information presented can be applied to any study in which participants read verbal stimuli.

The present article describes how to use eye tracking methodologies to study the cognitive processes involved in text comprehension. Descriptions of eye tracking equipment, how to develop experimental stimuli, and procedural recommendations are included. The information presented can be applied to most any study using verbal stimuli.

The present article describes how to use eye  tracking methodologies to study the cognitive processes involved in text  comprehension. Measuring eye ...

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

Driving Simulation in the Clinic: Testing Visual Exploratory Behavior in Daily Life Activities in Patients with Visual Field Defects

Patients suffering from homonymous hemianopia after infarction of the posterior cerebral artery (PCA) report different degrees of constraint in daily life, despite similar visual deficits. We assume this could be due to variable development of compensatory strategies such as altered visual scanning behavior. Scanning compensatory therapy (SCT) is studied as part of the visual training after infarction next to vision restoration therapy. SCT consists of learning to make larger eye movements into the blind field enlarging the visual field of search, which has been proven to be the most useful strategy1, not only in natural search tasks but also in mastering daily life activities2. Nevertheless, in clinical routine it is difficult to identify individual levels and training effects of compensatory behavior, since it requires measurement of eye movements in a head unrestrained condition. Studies demonstrated that unrestrained head movements alter the visual exploratory behavior compared to a head-restrained laboratory condition3. Martin et al.4 and Hayhoe et al.5 showed that behavior demonstrated in a laboratory setting cannot be assigned easily to a natural condition. Hence, our goal was to develop a study set-up which uncovers different compensatory oculomotor strategies quickly in a realistic testing situation: Patients are tested in the clinical environment in a driving simulator. SILAB software (Wuerzburg Institute for Traffic Sciences GmbH (WIVW)) was used to program driving scenarios of varying complexity and recording the driver's performance. The software was combined with a head mounted infrared video pupil tracker, recording head- and eye-movements (EyeSeeCam, University of Munich Hospital, Clinical Neurosciences).
The positioning of the patient in the driving simulator and the positioning, adjustment and calibration of the camera is demonstrated. Typical performances of a patient with and without compensatory strategy and a healthy control are illustrated in this pilot study. Different oculomotor behaviors (frequency and amplitude of eye- and head-movements) are evaluated very quickly during the drive itself by dynamic overlay pictures indicating where the subjects gaze is located on the screen, and by analyzing the data. Compensatory gaze behavior in a patient leads to a driving performance comparable to a healthy control, while the performance of a patient without compensatory behavior is significantly worse. The data of eye- and head-movement-behavior as well as driving performance are discussed with respect to different oculomotor strategies and in a broader context with respect to possible training effects throughout the testing session and implications on rehabilitation potential.

Patients with visual deficits after stroke report about different constraints in daily life most likely due to variable compensatory strategies, which are difficult to differentiate in clinical routine. We present a clinical set-up which allows measurement of different compensatory head- and eye-movement-strategies and evaluating their effects on driving performance.

Patients suffering from homonymous hemianopia after infarction of the posterior cerebral artery (PCA) report different degrees of constraint in daily ...

Medicine

Eye-tracking to Distinguish Comprehension-based and Oculomotor-based Regressive Eye Movements During Reading

Regressive eye movements are eye movements that move backwards through the text and comprise approximately 10-25% of eye movements during reading. As such, understanding the causes and mechanisms of regressions plays an important role in understanding eye movement behavior. Inhibition of return (IOR) is an oculomotor effect that results in increased latency to return attention to a previously attended target versus a target that was not previously attended. Thus, IOR may affect regressions. This paper describes how to design materials to distinguish between regressions caused by comprehension-related and oculomotor processes; the latter is subject to IOR. The method allows researchers to identify IOR and control the causes of regressions. While the method requires tightly controlled materials and large numbers of participants and materials, it allows researchers to distinguish and control the types of regressions that occur in their reading studies.

The method was designed to investigate the role of inhibition of return (IOR) in regressive eye movements during reading. The focus is on differentiating between regressions triggered as a result of comprehension difficulty versus those triggered from oculomotor error, including the role of IOR in the two types of regressions.

Regressive eye movements are eye movements that move backwards through the text and comprise approximately 10-25% of eye movements during reading. As ...

Efficiently Recording the Eye-Hand Coordination to Incoordination Spectrum

The objective analysis of eye movements has a significant history and has been long proven to be an important research tool in the setting of brain injury. Quantitative recordings have a strong capacity to screen diagnostically. Concurrent examinations of the eye and upper limb movements directed toward shared functional goals (e.g., eye-hand coordination) serve as an additional robust biomarker-laden path to capture and interrogate neural injury, including acquired brain injury (ABI). While quantitative dual-effector recordings in 3-D afford ample opportunities within ocular-manual motor investigations in the setting of ABI, the feasibility of such dual recordings for both eye and hand is challenging in pathological settings, particularly when approached with research-grade rigor. Here we describe the integration of an eye tracking system with a motion tracking system intended primarily for limb control research to study a natural behavior. The protocol enables the investigation of unrestricted, three-dimensional (3D) eye-hand coordination tasks. More specifically, we review a method to assess eye-hand coordination in visually guided saccade-to-reach tasks in subjects with chronic middle cerebral artery (MCA) stroke and compare them to healthy controls. Special attention is paid to the specific eye- and limb-tracking system properties in order to obtain high fidelity data from participants post-injury. Sampling rate, accuracy, permissible head movement range given anticipated tolerance and the feasibility of use were several of the critical properties considered when selecting an eye tracker and an approach. The limb tracker was selected based on a similar rubric but included the need for 3-D recording, dynamic interaction and a miniaturized physical footprint. The quantitative data provided by this method and the overall approach when executed correctly has tremendous potential to further refine our mechanistic understanding of eye-hand control and help inform feasible diagnostic and pragmatic interventions within the neurological and rehabilitative practice.&#160;

Cerebral injury can damage both ocular and somatic motor systems. Characterization of motor control post-injury affords biomarkers that assist in disease detection, monitoring, and prognosis. We review a method to measure eye-hand movement control in health and in pathologic incoordination, with look-and-reach paradigms to assess coordination between eye and hand.

The objective analysis of eye movements has a significant history and has been long proven to be an important research tool in the setting of brain ...

Simultaneous Eye Tracking and Single-Neuron Recordings in Human Epilepsy Patients

Intracranial recordings from patients with intractable epilepsy provide a unique opportunity to study the activity of individual human neurons during active behavior. An important tool for quantifying behavior is eye tracking, which is an indispensable tool for studying visual attention. However, eye tracking is challenging to use concurrently with invasive electrophysiology and this approach has consequently been little used. Here, we present a proven experimental protocol to conduct single-neuron recordings with simultaneous eye tracking in humans. We describe how the systems are connected and the optimal settings to record neurons and eye movements. To illustrate the utility of this method, we summarize results that were made possible by this setup. This data shows how using eye tracking in a memory-guided visual search task allowed us to describe a new class of neurons called target neurons, whose response was reflective of top-down attention to the current search target. Lastly, we discuss the significance and solutions to potential problems of this setup. Together, our protocol and results suggest that single-neuron recordings with simultaneous eye tracking in humans are an effective method to study human brain function. It provides a key missing link between animal neurophysiology and human cognitive neuroscience.

We describe a method to conduct single-neuron recordings with simultaneous eye tracking in humans. We demonstrate the utility of this method and illustrate how we used this approach to obtain neurons in the human medial temporal lobe that encode targets of a visual search.

Intracranial recordings from patients with intractable epilepsy provide a unique opportunity to study the activity of individual human neurons during ...

A Human-machine-interface Integrating Low-cost Sensors with a Neuromuscular Electrical Stimulation System for Post-stroke Balance Rehabilitation

A stroke is caused when an artery carrying blood from heart to an area in the brain bursts or a clot obstructs the blood flow to brain thereby preventing delivery of oxygen and nutrients. About half of the stroke survivors are left with some degree of disability. Innovative methodologies for restorative neurorehabilitation are urgently required to reduce long-term disability. The ability of the nervous system to reorganize its structure, function and connections as a response to intrinsic or extrinsic stimuli is called neuroplasticity. Neuroplasticity is involved in post-stroke functional disturbances, but also in rehabilitation. Beneficial neuroplastic changes may be facilitated with non-invasive electrotherapy, such as neuromuscular electrical stimulation (NMES) and sensory electrical stimulation (SES). NMES involves coordinated electrical stimulation of motor nerves and muscles to activate them with continuous short pulses of electrical current while SES involves stimulation of sensory nerves with electrical current resulting in sensations that vary from barely perceivable to highly unpleasant. Here, active cortical participation in rehabilitation procedures may be facilitated by driving the non-invasive electrotherapy with biosignals (electromyogram (EMG), electroencephalogram (EEG), electrooculogram (EOG)) that represent simultaneous active perception and volitional effort. To achieve this in a resource-poor setting, e.g., in low- and middle-income countries, we present a low-cost human-machine-interface (HMI) by leveraging recent advances in off-the-shelf video game sensor technology. In this paper, we discuss the open-source software interface that integrates low-cost off-the-shelf sensors for visual-auditory biofeedback with non-invasive electrotherapy to assist postural control during balance rehabilitation. We demonstrate the proof-of-concept on healthy volunteers.

A novel low-cost human-machine interface for interactive post-stroke balance rehabilitation system is presented in this article. The system integrates off-the-shelf low-cost sensors towards volitionally driven electrotherapy paradigm. The proof-of-concept software interface is demonstrated on healthy volunteers.

A stroke is caused when an artery carrying blood from heart to an area in the brain bursts or a clot obstructs the blood flow to brain thereby preventing ...

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 ...

Brain-Computer Interface-controlled Upper Limb Robotic System for Enhancing Daily Activities in Stroke Patients

This study introduces a Brain-Computer Interface (BCI)-controlled upper limb assistive robot for post-stroke rehabilitation. The system utilizes electroencephalogram (EEG) and electrooculogram (EOG) signals to help users assist upper limb function in everyday tasks while interacting with a robotic hand. We evaluated the effectiveness of this BCI-robot system using the Berlin Bimanual Test for Stroke (BeBiTS), a set of 10 daily living tasks involving both hands. Eight stroke patients participated in this study, but only four participants could adapt to the BCI robot system training and perform the postBeBiTS. Notably, when the preBeBiTS score for each item was four or less, the BCI robot system showed greater assistive effectiveness in the postBeBiTS assessment. Furthermore, our current robotic hand does not assist with arm and wrist functions, limiting its use in tasks requiring complex hand movements. More participants are required to confirm the training effectiveness of the BCI-robot system, and future research should consider using robots that can assist with a broader range of upper limb functions. This study aimed to determine the BCI-robot system's ability to assist patients in performing daily living activities.

This study introduces a brain-computer interface (BCI) system for stroke patients, which combines electroencephalography and electrooculography signals to control an upper limb robotic hand, enhancing daily activities. The evaluation used the Berlin Bimanual Test for Stroke (BeBiTS).

Eye-Tracking Control to Assess Cognitive Functions in Patients with Amyotrophic Lateral Sclerosis

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