Dr. Terao was supported by a Research Project Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan [16K09709,16H01497]. YU was supported by a Research Project Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan [No.25293206, No. 22390181, 15H05881, 16H05322]; by grants from the Research Committee on the Best rTMS Treatment of Parkinson's Disease From the Ministry of Health and Welfare of Japan; and by the Research Committee on Dystonia of the Ministry of Health and Welfare of Japan.

All experimental procedures in this study were approved and conducted according to the guidelines of the institution&#39;s human research ethics committee after obtaining informed consent.
1. Prepare the Subject and the Room for Recoding
<ol>
	<li>Perform recording in a room with low ambient illumination, to allow sufficient light adaptation.</li>
	<li>Have subjects sit in front of a black, concave dome-shaped screen measuring 90-cm in diameter that contains light-emitting diodes (LEDs) embedded in pinholes, which serve as the fixation points and saccade targets used for the oculomotor paradigms. 
	NOTE: The LEDs are arranged in horizontal, vertical and oblique arrays in a black, concave dome-shaped screen, i.e., in 8 directions separated by 45 degrees from the center and at an interval of 5 degrees from the center, as was originally devised by Kato et al.20 for behavioral and physiological studies, and modified for human use by Hikosaka et al.21</li>
	<li>For controlling the oculomotor tasks, make each subject hold a microswitch button connected to a microcomputer, which allows the subject to initiate and terminate a task trial by pressing and releasing the button. 
	NOTE: Tasks and data acquisition are controlled by a custom-made program operating on a typical Windows PC.</li>
	<li>Stabilize the subject&#39;s head position by chin and forehead rests, as well as by a head band.</li>
</ol>
2. Place the Electrodes for EOG
<ol>
	<li>Use an Ag-AgCl cup electrode for recording EOG (Figure 1), which has a diameter of 1.8 cm and a thickness of 3.5 mm. The bottom of the cup comprises the Ag-AgCl electrode and the lateral wall is surrounded by a plastic fringe of 5 mm thickness, enabling wide contact with the skin.</li>
	<li>Wipe the skin with an alcohol swab.</li>
	<li>Fill the cup with electrode paste.</li>
	<li>Stably fixate the electrode on the skin by placing double-stick adhesive tape beneath the plastic and attach the fringe to the skin.</li>
	<li>For recording horizontal saccades by EOG, place the electrodes at the bilateral canthi of the eyes, whereas for recording vertical saccades, place the electrodes above and below one eye.</li>
</ol>
3. Set Up the Amplifiers for Recording
<ol>
	<li>Use a direct current (DC)-amplifier for recording the EOG, with the signal digitized at 500 Hz.</li>
	<li>Record VOG simultaneously, using the video-based eye tracking system, which records ocular fixation position data at a sampling rate of 500 - 1,000 Hz.</li>
	<li>Feed the analog output of the horizontal and vertical eye positions and set the filter of the data acquisition system, with the signal low-pass filter at 20 Hz.</li>
	<li>Also, set the filter to attenuate the high-intermediate frequency noise, such as electromyography and electroencephalography. 
	NOTE: For analysis, a further smoothing process is necessary for calculating saccade velocity profiles from the eye position data (here, 3-point smoothing was performed three times).</li>
	<li>If possible, measure the impedance between the electrode and the skin and keep it below 20 k&#937;.</li>
</ol>
4. Waiting Period after Placing the Electrodes for Light Adaptation
<ol>
	<li>Wait 10 - 20 min after placing the EOG electrode on the skin, until sufficient light adaptation takes place.</li>
	<li>Allow the recording to stabilize and the impedance between the electrode gel to decrease.</li>
</ol>
5. Calibrate the EOG and VOG Signals
<ol>
	<li>Perform eye movement calibration before each test session by having the subjects look at 5 pre-specified locations.</li>
	<li>More specifically, make subjects view visual targets in the center and those that appear 20 degrees to the left, right, upwards, and downwards of the fixation point, both for EOG and VOG.</li>
	<li>Adjust the gain of EOG as the subjects fixate on these spots, so that using the custom-built data acquisition system for monitoring the current eye position displayed on the computer screen matches the target position displayed on the screen.</li>
</ol>
6. Record Saccades Using the Oculomotor Paradigms and Recalibrate the Eye Positions as Needed During the Session
<ol>
	<li>Instruct the subjects about the oculomotor paradigms. 
	NOTE: Two oculomotor tasks are typically used for clinical studies, the visually guided saccade (VGS) and antisaccade (AS) tasks. Briefly, in VGS, when subjects press the button, a central spot is lit in the center of the dome, and the subjects are first required to fixate on this spot. 1.5 - 2 s later, a target is presented, randomly at a location 5, 10, 20, or 30 degrees horizontally to the left or right of it, at the same time as the central fixation spot is extinguished. The subjects are instructed to make a saccade toward that target. In the AS task, make the subjects first press the button and then require them to fixate on the central fixation point as it appears. 1.5 - 2 s later, the target jumps to the left or right of it, similar to above. The subjects are required to make a saccade towards a mirror-symmetrical position across the central fixation spot.</li>
	<li>Have the subjects press the button and begin the trials.</li>
	<li>During the session, adjust the gain of EOG during the task performance, so that the current eye position displayed on the monitor is always aligned with the target position simultaneously displayed on the same screen. Both for EOG and VOG, perform re-calibration for adjustment when necessary throughout the experiments.</li>
	<li>To compare the performances of the two methodologies, analyze the filtered and digitized EOG signals from the DC-amplifier and VOG by a custom-built computer program and show the EOG and VOG signals together in the same trace.</li>
</ol>

<ol><li>Braun, D., Weber, H., Mergner, T., Schulte-Mönting, J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Saccadic+reaction+times+in+patients+with+frontal+and+parietal+lesions%5BTitle%5D)+AND+%22Brain%22%5BJournal%5D)">Saccadic reaction times in patients with frontal and parietal lesions.</a> Brain. 115, (Pt 5) 1359-1386 (1992).</li>
<li>Sweeney, J. A., Levy, D., Harris, M. S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Commentary%3A+eye+movement+research+with+clinical+populations%5BTitle%5D)+AND+%22Prog+Brain+Res%22%5BJournal%5D)">Commentary: eye movement research with clinical populations.</a> Prog Brain Res. 140, 507-522 (2002).</li>
<li>Leigh, R. J., Kennard, C. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Using+saccades+as+a+research+tool+in+the+clinical+neurosciences%5BTitle%5D)+AND+%22Brain%22%5BJournal%5D)">Using saccades as a research tool in the clinical neurosciences.</a> Brain. 127, (Pt 3) 460-477 (2004).</li>
<li>Ramat, S., Leigh, R. J., Zee, D. S., Optican, L. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((What+clinical+disorders+tell+us+about+the+neural+control+of+saccadic+eye+movements%29%5BTitle%5D)+AND+%22Brain%22%5BJournal%5D)">What clinical disorders tell us about the neural control of saccadic eye movements).</a> Brain. 130, (Pt 1) 10-35 (2007).</li>
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<li>Kennard, D. W., Smyth, G. L. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((The+causes+of+downward+eyelid+movement+with+changes+of+gaze%2C+and+a+study+of+the+physical+factors+concerned%5BTitle%5D)+AND+%22J+Physiol%22%5BJournal%5D)">The causes of downward eyelid movement with changes of gaze, and a study of the physical factors concerned.</a> J Physiol. 166, 178-190 (1963).</li>
<li>Houben, M. M., Goumans, J., van der Steen, J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Recording+three-dimensional+eye+movements%3A+scleral+search+coils+versus+video+oculography%5BTitle%5D)+AND+%22Invest+Ophthalmol+Vis+Sci%22%5BJournal%5D)">Recording three-dimensional eye movements: scleral search coils versus video oculography.</a> Invest Ophthalmol Vis Sci. 47 (1), 179-187 (2006).</li>
<li>Eggert, T. <a target="_blank" href="https://www.ncbi.nlm.nih.gov/pubmed/17314477">Eye movement recordings: methods.</a> Dev Ophthalmol. 40, 15-34 (2007).</li>
<li>Frens, M. A., van der Geest, J. N. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Scleral+search+coils+influence+saccade+dynamics%5BTitle%5D)+AND+%22J+Neurophysiol%22%5BJournal%5D)">Scleral search coils influence saccade dynamics.</a> J Neurophysiol. 88 (2), 692-698 (2002).</li>
<li>Lappe-Osthege, M., Talamo, S., Helmchen, C., Sprenger, A. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Overestimation+of+saccadic+peak+velocity+recorded+by+electro-oculography+compared+to+video-oculography+and+scleral+search+coil%5BTitle%5D)+AND+%22Clin+Neurophysiol%22%5BJournal%5D)">Overestimation of saccadic peak velocity recorded by electro-oculography compared to video-oculography and scleral search coil.</a> Clin Neurophysiol. 121 (10), 1786-1787 (2010).</li>
<li>Bhidayasiri, R., Riley, D. E., Somers, J. T., Lerner, A. J., Büttner-Ennever, J. A., Leigh, R. J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Pathophysiology+of+slow+vertical+saccades+in+progressive+supranuclear+palsy%5BTitle%5D)+AND+%22Neurology%22%5BJournal%5D)">Pathophysiology of slow vertical saccades in progressive supranuclear palsy.</a> Neurology. 57 (11), 2070-2077 (2001).</li>
<li>Terao, Y., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Visualization+of+the+information+through+human+oculomotor+cortical+regions+by+transcranial+magnetic+stimulation%5BTitle%5D)+AND+%22J+Neurophysiol%22%5BJournal%5D)">Visualization of the information through human oculomotor cortical regions by transcranial magnetic stimulation.</a> J Neurophysiol. 80 (2), 936-946 (1998).</li>
<li>Terao, Y., Okano, T., Furubayashi, T., Yugeta, A., Inomata-Terada, S., Ugawa, Y. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Effects+of+thirty-minute+mobile+phone+use+on+saccades%5BTitle%5D)+AND+%22Clin+Neurophysiol%22%5BJournal%5D)">Effects of thirty-minute mobile phone use on saccades.</a> Clin Neurophysiol. 118 (7), 1545-1556 (2007).</li>
<li>Terao, Y., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Initiation+and+inhibitory+control+of+saccades+with+the+progression+of+Parkinson%27s+disease+-+changes+in+three+major+drives+converging+on+the+superior+colliculus%5BTitle%5D)+AND+%22Neuropsychologia%22%5BJournal%5D)">Initiation and inhibitory control of saccades with the progression of Parkinson's disease - changes in three major drives converging on the superior colliculus.</a> Neuropsychologia. 49 (7), 1794-1806 (2011).</li>
<li>Terao, Y., et al. <a target="_blank" href="http://www.sciencedirect.com/science/article/pii/S2210533611001870">Frontal cortical regions controlling small and large amplitude saccades: a TMS study.</a> Basal Ganglia. 1 (4), 221-229 (2011).</li>
<li>Terao, Y., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Deterioration+of+horizontal+saccades+in+progressive+supranuclear+palsy%5BTitle%5D)+AND+%22Clin+Neurophysiol%22%5BJournal%5D)">Deterioration of horizontal saccades in progressive supranuclear palsy.</a> Clin Neurophysiol. 124 (2), 354-363 (2013).</li>
<li>Terao, Y., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Saccade+abnormalities+associated+with+focal+cerebral+lesions+-How+cortical+and+basal+ganglia+commands+shape+saccades+in+humans%5BTitle%5D)+AND+%22Clin+Neurophsyiol%22%5BJournal%5D)">Saccade abnormalities associated with focal cerebral lesions -How cortical and basal ganglia commands shape saccades in humans.</a> Clin Neurophsyiol. 127 (8), 2953-2967 (2016).</li>
<li>Terao, Y., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Is+multiple+system+atrophy+with+cerebellar+ataxia+%28MSA-C%29+like+spinocerebellar+ataxia+and+multiple+system+atrophy+with+parkinsonism+%28MSA-P%29+like+Parkinson%27s+disease%3F+-A+saccade+study+on+pathophysiology%5BTitle%5D)+AND+%22Clin+Neurophysiol%22%5BJournal%5D)">Is multiple system atrophy with cerebellar ataxia (MSA-C) like spinocerebellar ataxia and multiple system atrophy with parkinsonism (MSA-P) like Parkinson's disease? -A saccade study on pathophysiology.</a> Clin Neurophysiol. 127 (2), 1491-1502 (2016).</li>
<li>Terao, Y., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Distinguishing+spinocerebellar+ataxia+with+pure+cerebellar+manifestation+from+multiple+system+atrophy+%28MSA-C%29+through+saccade+profiles%5BTitle%5D)+AND+%22Clin+Neurophysiol%22%5BJournal%5D)">Distinguishing spinocerebellar ataxia with pure cerebellar manifestation from multiple system atrophy (MSA-C) through saccade profiles.</a> Clin Neurophysiol. 128 (1), 31-43 (2016).</li>
<li>Kato, M., Hikosaka, O. Saccade related responses of external pallidal neurons in monkey. Neurosci Res. , Suppl. 17 [Abstract] 218(1992).</li>
<li>Hikosaka, O., Fukuda, H., Kato, M., Uetake, K., Nomura, Y., Segawa, M. Deficits in saccadic eye movements in hereditary progressive dystonia with marked diurnal fluctuation. <a target="_blank" href="NULL">Hereditary Progressive Dystonia With Marked Diurnal Fluctuation</a>. Segawa, M. , The Parthenon Publishing Group. New York. 159-177 (1993).</li>
<li>Fukuda, H., et al. Development of saccade recording system in humans: simultaneous measurment of electro-oculography and video-oculography. 38th Annual Meeting of Japanese Society of Clinical Neurophysiology. , [Japanese abstract] (2008).</li>
<li>Constable, P. A., Bach, M., Frishman, L. J., Jeffrey, B. G., Robson, A. G. <a target="_blank" href="https://link.springer.com/article/10.1007/s10633-017-9573-2">International Society for Clinical Electrophysiology of Vision. ISCEV Standard for clinical electro-oculography (2017 update).</a> Doc Ophthalmol. 134 (1), 134(2017).</li>
<li>Behrens, F., Weiss, L. R. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((An+automated+and+modified+technique+for+testing+the+retinal+function+%28Arden+test%29+by+use+of+the+electro-oculogram+%28EOG%29+for+clinical+and+research+use%5BTitle%5D)+AND+%22Doc+Ophthalmol%22%5BJournal%5D)">An automated and modified technique for testing the retinal function (Arden test) by use of the electro-oculogram (EOG) for clinical and research use.</a> Doc Ophthalmol. 96 (4), 283-292 (1999).</li>
<li>Kikawada, N. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Variations+in+the+corneo-retinal+standing+potential+of+the+vertebrate+eye+during+light+and+dark+adaptations%5BTitle%5D)+AND+%22Jpn+J+Physiol%22%5BJournal%5D)">Variations in the corneo-retinal standing potential of the vertebrate eye during light and dark adaptations.</a> Jpn J Physiol. 18 (6), 687-702 (1968).</li>
<li>Yuval-Greenberg, S., Tomer, O., Keren, A. S., Nelken, I., Deouell, L. Y. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/pubmed?term=((Transient+induced+gamma-band+response+in+EEG+as+a+manifestation+of+miniature+saccades%5BTitle%5D)+AND+%22Neuron%22%5BJournal%5D)">Transient induced gamma-band response in EEG as a manifestation of miniature saccades.</a> Neuron. 58 (3), 429-441 (2008).</li>
</ol>

The authors have nothing to disclose with regard to this study.

Although nowadays, the prevailing method for recording saccades has become the VOG, the present study showed that EOG can achieve an accuracy almost comparable to that of VOG if properly implemented (Figure 2). The present EOG method has been shown to achieve a good correlation with VOG when recording horizontal saccades and has been successfully used in many previous studies by the same group12,13,14</su...

There are three major ways to record eye movements, the conventional EOG, the VOG recorded by the video-based eye tracking system, and the scleral search coil (SSC) method. Among them, EOG has been frequently used for recording eye movements in patients since the 1970s because of its simplicity. Widely applicable to the clinical population, this method has been extensively utilized for the diagnosis of neurological patients and has provided useful information about the pathophysiology underlying the disorders1,2,3,4,5. In addition, it is still the only technique that can be feasibly used for recording eye movements during sleep (rapid eye movement during REM sleep and other forms of eye movements).
Since the eyeball is positively charged in its anterior aspect including the cornea relative to its posterior aspect, there is a voltage difference between the anterior and posterior aspects of the eyes termed the corneo-retinal potential. Due to the presence of this potential, the right electrode will become more positive than the left when the subjects turns their gaze toward the right, and become negative when they turn their gaze to the left. Since the voltage difference between the left and right electrodes correlates significantly with the rotation angle of the eyeballs for horizontal saccades, it can be used to measure horizontal eye movements. However, this correlation does not hold for the vertical direction, although vertical EOG still can be used to measure eye movements6. On the other hand, some studies mainly use vertical EOG for monitoring blinks.
Recently, however, VOG has largely taken the place of EOG due to its higher spatial accuracy reaching up to 0.25 - 0.5 degrees, and has now become the standard method for saccade recording in the clinical setting. Meanwhile, EOG has come to be considered rather outdated, since its spatial accuracy, at most 0.5 degrees, is inferior to that of VOG.
However, VOG also has its own drawbacks if used in the clinical setting. There are cases in which VOG is not feasible; for example, eye tracking becomes inaccurate in subjects with a narrow eye cleft such as when the greater area of the cornea is occluded by the eyelids. In patients with cataract lenses, aberrant reflection of the infrared light hampers reliable recording of the gaze direction. Furthermore, EOG can offer advantages for some people for whom their movement disorder makes VOG recording difficult. In addition, the VOG system is more expensive compared to the setup of EOG, which often makes the former unavailable in ordinary medical facilities.
On the other hand, the SSC method is regarded as the gold standard for measuring eye movements. Compared with VOG and EOG, this method provides the highest spatial accuracy, down to 0.1 degrees, and is especially useful when the recording involves high-frequency head motion6. However, this method is potentially invasive, i.e., painful and very irritating to the eyes, and allows recording for only a brief period, approximately under 30 min or shorter7,8,9,10. This short duration makes it a method unsuitable for extensive clinical application, although it has been used successfully in some specialized facilities11.
Based on previous studies recording more than 250 neurological patients and 480 normal subjects by the same group12,13,14,15,16,17,18,19, the present study shows that EOG can be accurate enough to serve as a standard technique of eye movement recording, and widely applicable to the clinical population, while circumventing various drawbacks of VOG and SSC. The present article describes a stable EOG recording method, using an electrode with a wide fringe to allow wide and stable contact with the skin, similar to that of an EEG electrode attached securely on the scalp by collodion for recording a long time period. The impedance of the electrode goes down and the recording becomes stable with time, thereby effectively reducing the artifacts from facial muscles and electroencephalography. This method is compared with simultaneously recorded VOG. When properly prepared and implemented, EOG is as good as VOG in terms of accuracy for recording saccades in neurological patients, and EOG may even be more amenable to saccade recording in normal subjects.

<table><tbody><tr><td>Electrode</td><td>Nihon-Kohden (Tokyo, Japan)</td><td>NS111-115</td><td>cup electrode</td></tr><tr><td>Electrode paste</td><td>Nihon-Kohden (Tokyo, Japan)</td><td>Gelaid Z-101BA</td><td>gel electrode paste to fill in the cup electrode</td></tr><tr><td>Adhesive tape&amp;nbsp;</td><td>Nihon-Kohden (Tokyo, Japan)</td><td>H261</td><td>double-stick tape for fixating the electrode</td></tr><tr><td>DC-amplifier</td><td>Nihon-Kohden (Tokyo, Japan)</td><td>AN-601G</td><td>amplifier for EOG</td></tr><tr><td>video-based eye tracking system</td><td>SR research (Mississauga, Ontario, Canada)</td><td>Eyelink II</td><td>eye tracking system for recording VOG</td></tr><tr><td>Filter</td><td>NF corporation</td><td>MS-521</td><td>filter for the EOG signal</td></tr></tbody></table>

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.

Figure 2&#160;shows representative simultaneous records of EOG and VOG in a normal subject. 8 trials of VGS are superimposed for EOG (gray curves) and VOG (red curves; Figure 2A). Calibrated by the present method, EOG and VOG data are known to be linear over a range of 5-30 degrees, and the spatial accuracy of the data is 0.5 degrees.
The records obtain...

Watch this Scientific Journal Video about Recording Horizontal Saccade Performances Accurately in Neurological Patients Using Electro-oculogram at JoVE.com

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

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 ...

recording-horizontal-saccade-performances-accurately-neurological

Research

JoVE Journal

Behavior

10.6K Views.  Kyorin University. Het artikel beschrijft een praktische methode voor het opnemen van horizontale oogbewegingen met hoge nauwkeurigheid door electro-oculogram bij neurologische patiënten, met behulp van een beker Ag-AgCl-elektrode met een brede kunststof rand. Stabiele meting vereist goede selectie en fixatie van elektroden, met voldoende tijd voor licht aanpassing aan het optreden, en re-kalibratie zoals nodig.

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

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

Event-related Potentials During Target-response Tasks to Study Cognitive Processes of Upper Limb Use in Children with Unilateral Cerebral Palsy

Unilateral Cerebral Palsy (CP) is a neurodevelopmental disorder that is a very common cause of disability in childhood. It is characterized by unilateral motor impairments that are frequently dominated in the upper limb. In addition to a reduced movement capacity of the affected upper limb, several children with unilateral CP show a reduced awareness of the remaining movement capacity of that limb. This phenomenon of disregarding the preserved capacity of the affected upper limb is regularly referred to as Developmental Disregard (DD). Different theories have been postulated to explain DD, each suggesting slightly different guidelines for therapy. Still, cognitive processes that might additionally contribute to DD in children with unilateral CP have never been directly studied. The current protocol was developed to study cognitive aspects involved in upper limb control in children with unilateral CP with and without DD. This was done by recording event-related potentials (ERPs) extracted from the ongoing EEG during target-response tasks asking for a hand-movement response. ERPs consist of several components, each of them associated with a well-defined cognitive process (e.g., the N1 with early attention processes, the N2 with cognitive control and the P3 with cognitive load and mental effort). Due to its excellent temporal resolution, the ERP technique enables to study several covert cognitive processes preceding overt motor responses and thus allows insight into the cognitive processes that might contribute to the phenomenon of DD. Using this protocol adds a new level of explanation to existing behavioral studies and opens new avenues to the broader implementation of research on cognitive aspects of developmental movement restrictions in children.

Several children with unilateral Cerebral Palsy seem to disregard the preserved capacity of their affected upper limb. This Developmental Disregard is extensively described in the literature but the involved cognitive processes have not been studied. To study underlying cognitive factors of upper limb control, an event-related potential protocol was developed.

Unilateral Cerebral Palsy (CP) is a neurodevelopmental disorder that is a very common cause of disability in childhood. It is characterized by unilateral ...

Combined Invasive Subcortical and Non-invasive Surface Neurophysiological Recordings for the Assessment of Cognitive and Emotional Functions in Humans

In spite of the success in applying non-invasive electroencephalography (EEG), magneto-encephalography (MEG) and functional magnetic resonance imaging (fMRI) for extracting crucial information about the mechanism of the human brain, such methods remain insufficient to provide information about physiological processes reflecting cognitive and emotional functions at the subcortical level. In this respect, modern invasive clinical approaches in humans, such as deep brain stimulation (DBS), offer a tremendous possibility to record subcortical brain activity, namely local field potentials (LFPs) representing coherent activity of neural assemblies from localized basal ganglia or thalamic regions. Notwithstanding the fact that invasive approaches in humans are applied only after medical indication and thus recorded data correspond to altered brain circuits, valuable insight can be gained regarding the presence of intact brain functions in relation to brain oscillatory activity and the pathophysiology of disorders in response to experimental cognitive paradigms. In this direction, a growing number of DBS studies in patients with Parkinson&#39;s disease (PD) target not only motor functions but also higher level processes such as emotions, decision-making, attention, memory and sensory perception. Recent clinical trials also emphasize the role of DBS as an alternative treatment in neuropsychiatric disorders ranging from obsessive compulsive disorder (OCD) to chronic disorders of consciousness (DOC). Consequently, we focus on the use of combined invasive (LFP) and non-invasive (EEG) human brain recordings in assessing the role of cortical-subcortical structures in cognitive and emotional processing trough experimental paradigms (e.g. speech stimuli with emotional connotation or paradigms of cognitive control such as the Flanker task), for patients undergoing DBS treatment.

The present protocol aims at assessing cognitive-emotional functions in the basal ganglia by simultaneous neurophysiological recording of local field potentials and non-invasive brain cortical activity (EEG). The procedure is exemplified by the use of paradigms involving speech stimuli with emotional connotation or the Flanker task involving cognitive control.

In spite of the success in applying non-invasive electroencephalography (EEG), magneto-encephalography (MEG) and functional magnetic resonance imaging ...

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.

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 ...

Video-oculography in Mice

Eye movements are very important in order to track an object or to stabilize an image on the retina during movement. Animals without a fovea, such as the mouse, have a limited capacity to lock their eyes onto a target. In contrast to these target directed eye movements, compensatory ocular eye movements are easily elicited in afoveate animals1,2,3,4. Compensatory ocular movements are generated by processing vestibular and optokinetic information into a command signal that will drive the eye muscles. The processing of the vestibular and optokinetic information can be investigated separately and together, allowing the specification of a deficit in the oculomotor system. The oculomotor system can be tested by evoking an optokinetic reflex (OKR), vestibulo-ocular reflex (VOR) or a visually-enhanced vestibulo-ocular reflex (VVOR). The OKR is a reflex movement that compensates for "full-field" image movements on the retina, whereas the VOR is a reflex eye movement that compensates head movements. The VVOR is a reflex eye movement that uses both vestibular as well as optokinetic information to make the appropriate compensation. The cerebellum monitors and is able to adjust these compensatory eye movements. Therefore, oculography is a very powerful tool to investigate brain-behavior relationship under normal as well as under pathological conditions (f.e. of vestibular, ocular and/or cerebellar origin).
Testing the oculomotor system, as a behavioral paradigm, is interesting for several reasons. First, the oculomotor system is a well understood neural system5. Second, the oculomotor system is relative simple6; the amount of possible eye movement is limited by its ball-in-socket architecture ("single joint") and the three pairs of extra-ocular muscles7. Third, the behavioral output and sensory input can easily be measured, which makes this a highly accessible system for quantitative analysis8. Many behavioral tests lack this high level of quantitative power. And finally, both performance as well as plasticity of the oculomotor system can be tested, allowing research on learning and memory processes9.
Genetically modified mice are nowadays widely available and they form an important source for the exploration of brain functions at various levels10. In addition, they can be used as models to mimic human diseases. Applying oculography on normal, pharmacologically-treated or genetically modified mice is a powerful research tool to explore the underlying physiology of motor behaviors under normal and pathological conditions. Here, we describe how to measure video-oculography in mice8.

Video-oculography is a very quantitative method to investigate ocular motor performance as well as motor learning. Here, we describe how to measure video-oculography in mice. Applying this technique on normal, pharmacologically-treated or genetically modified mice is a powerful research tool to explore the underlying physiology of motor behaviors.

Eye movements are very important in order to track an object or to stabilize an image on the retina during movement. Animals without a fovea, such as the ...

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 ...

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 ...

Medicine

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 ...

Simultaneous Eye Tracking and Single-Neuron Recording to Identify Target-Selective Neurons

Source: Wang, S., et al. <a href="https://app.jove.com/v/59117">Simultaneous Eye Tracking and Single-Neuron Recordings in Human Epilepsy Patients.</a> J. Vis. Exp. (2019).
The video demonstrates an assay to identify target-selective neurons via simultaneous eye-tracking and single-neuron recordings. A human participant is tasked with identifying a target object among an array of objects in a display, and the eye movement is tracked. Simultaneously, single neurons&#39; firing rate is recorded via electrodes implanted in the brain. The data from both recordings are correlated to assess the presence of target-selective neurons.

All procedures involving human participants have been performed in compliance with the institutional, national, and international guidelines for human ...

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

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