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) embe...

<ol>
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J., Kennard, C. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Using+saccades+as+a+research+tool+in+the+clinical+neurosciences.">Using saccades as a research tool in the clinical neurosciences.</a> Brain. 127, 460-477 (2004).</li><li>Ramat, S., Leigh, R. J., Zee, D. S., Optican, L. 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N. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Scleral+search+coils+influence+saccade+dynamics.">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/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Overestimation+of+saccadic+peak+velocity+recorded+by+electro-oculography+compared+to+video-oculography+and+scleral+search+coil.">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., B&#252;ttner-Ennever, J. A., 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=Pathophysiology+of+slow+vertical+saccades+in+progressive+supranuclear+palsy.">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/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Visualization+of+the+information+through+human+oculomotor+cortical+regions+by+transcranial+magnetic+stimulation.">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/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Effects+of+thirty-minute+mobile+phone+use+on+saccades.">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/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Initiation+and+inhibitory+control+of+saccades+with+the+progression+of+Parkinson's+disease+-+changes+in+three+major+drives+converging+on+the+superior+colliculus.">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.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Frontal+cortical+regions+controlling+small+and+large+amplitude+saccades:+a+TMS+study.">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/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Deterioration+of+horizontal+saccades+in+progressive+supranuclear+palsy.">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/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Saccade+abnormalities+associated+with+focal+cerebral+lesions+-How+cortical+and+basal+ganglia+commands+shape+saccades+in+humans.">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/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=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.">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/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Distinguishing+spinocerebellar+ataxia+with+pure+cerebellar+manifestation+from+multiple+system+atrophy+(MSA-C)+through+saccade+profiles.">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. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Saccade+related+responses+of+external+pallidal+neurons+in+monkey.">Saccade related responses of external pallidal neurons in monkey.</a> Neurosci Res. , 218 (1992).</li><li>Hikosaka, O., Fukuda, H., Kato, M., Uetake, K., Nomura, Y., Segawa, M., Segawa, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Deficits+in+saccadic+eye+movements+in+hereditary+progressive+dystonia+with+marked+diurnal+fluctuation.">Deficits in saccadic eye movements in hereditary progressive dystonia with marked diurnal fluctuation.</a> Hereditary Progressive Dystonia With Marked Diurnal Fluctuation. , 159-177 (1993).</li><li>Fukuda, H., 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+saccade+recording+system+in+humans:+simultaneous+measurment+of+electro-oculography+and+video-oculography.">Development of saccade recording system in humans: simultaneous measurment of electro-oculography and video-oculography.</a> 38th Annual Meeting of Japanese Society of Clinical Neurophysiology. , (2008).</li><li>Constable, P. A., Bach, M., Frishman, L. J., Jeffrey, B. G., Robson, A. G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=International+Society+for+Clinical+Electrophysiology+of+Vision.+ISCEV+Standard+for+clinical+electro-oculography+(2017+update).">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/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=An+automated+and+modified+technique+for+testing+the+retinal+function+(Arden+test)+by+use+of+the+electro-oculogram+(EOG)+for+clinical+and+research+use.">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/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Variations+in+the+corneo-retinal+standing+potential+of+the+vertebrate+eye+during+light+and+dark+adaptations.">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. 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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 border="0" cellpadding="0" cellspacing="0" style="width:927px;" width="926">
	<colgroup>
		<col />
		<col />
		<col />
		<col />
	</colgroup>
	<tbody>
		<tr height="21">
			<td height="21" style="height:21px;width:297px;">Electrode</td>
			<td style="width:276px;">Nihon-Kohden (Tokyo, Japan)</td>
			<td style="width:119px;">NS111-115</td>
			<td style="width:235px;">cup electrode</td>
		</tr>
		<tr height="21">
			<td height="21" style="height:21px;width:297px;">Electrode paste</td>
			<td style="width:276px;">Nihon-Kohden (Tokyo, Japan)</td>
			<td style="width:119px;">Gelaid Z-101BA</td>
			<td>gel electrode paste to fill in the cup electrode</td>
		</tr>
		<tr height="21">
			<td height="21" style="height:21px;width:297px;">Adhesive tape&#160;</td>
			<td style="width:276px;">Nihon-Kohden (Tokyo, Japan)</td>
			<td style="width:119px;">H261</td>
			<td>double-stick tape for fixating the electrode</td>
		</tr>
		<tr height="21">
			<td height="21" style="height:21px;width:297px;">DC-amplifier</td>
			<td style="width:276px;">Nihon-Kohden (Tokyo, Japan)</td>
			<td style="width:119px;">AN-601G</td>
			<td>amplifier for EOG</td>
		</tr>
		<tr height="42">
			<td height="42" style="height:42px;">video-based eye tracking system</td>
			<td style="width:276px;">SR research (Mississauga, Ontario, Canada)</td>
			<td style="width:119px;">Eyelink II</td>
			<td>eye tracking system for recording VOG</td>
		</tr>
		<tr height="21">
			<td height="21" style="height:21px;width:297px;">Filter</td>
			<td style="width:276px;">NF corporation</td>
			<td style="width:119px;">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 ...

The overall goal of the present oculogram is to observe the abnormality of saccade performance in patients especially in those with neurological disorders and to look at the pathophysiology underlying the disorder providing useful information about the diagnosis. This method can help answer key questions in the field such as diagnosis of patients with neurological disorders and to elucidate the pathophysiology underlying the disease. The main advantage of this technique is that it allows stable recording of eye movements noninvasively in a relatively short time and is widely applicable to neurological patients.Demonstrating the procedure will be Dr.Hideki Fukuda, an oculomotor researcher at Segawa Neurologic Clinic for Children and Dr.Yuseke Sugiyama, a graduate student from the Department of Neurology, the University of Tokyo. Begin by escorting the subject into a room with low ambient illumination. Have the subject sit in front of a black concave dome-shaped screen measuring 90 centimeters 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.Then provide the subject with a micro switch button connected to a microcomputer which allows them to initiate and terminate the test trial by pressing and releasing the button. Stabilize the subject's head position by chin and forehead rests as well as by a headband. Next, acquire a silver/sulfur chloride cup electrode for recording the Electrooculogram or EOG.Wipe the skin with an alcohol swab. Then fill the cup with electrode paste. Stably fixate the electrode on the skin by placing double stick adhesive tape beneath the plastic and attach the fringe to the skin.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. Finally, wait 10 to 20 minutes after placing the EOG electrode on the skin until sufficient light adaptation takes place.Begin by using a Direct Current, DC, amplifier for recording the EOG with the signal digitized at 500 hertz. Record Video Oculography, VOG, simultaneously using the video-based eye tracking system which records ocular fixation position data at a sampling rate of 500 to 1, 000 hertz. Then 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 hertz.Perform eye movement calibration before each test session by having the subject look at five pre-specified locations such that they 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. Then adjust the gain of EOG as the subject fixates 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. Next, instruct the subject about the oculomotor paradigms.Then have the subject press the button and begin the trials. 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 positions simultaneously displayed on the same screen. After the experiment is complete, 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 in order to compare the performances of the two methodologies.The records obtained by the two methods largely overlap with each other except that the EOG traces are slightly displaced towards the right compared to the VOG traces. These results show a comparison of EOG and VOG traces in the visually-guided saccade task. There is again substantial overlap between the traces for EOG and VOG, but the latency is slightly longer for EOG and the velocity curve of EOG shows a slightly lower peak velocity than that of VOG.Once mastered, this technique can be done in 30 minutes including preparation if it is performed properly. While attempting this procedure, it is important to remember to select proper electrodes and stably attach them as well as to take sufficient time for light adaptation to occur. Following this procedure, other methods like eye movement recording while the eyes are closed can be performed in order to answer additional questions like how the eyes move during sleep.After its development, this technique paved the way for researchers in the field of neurology and psychiatry to explore the pathophysiology of neurological disorders in the clinical setting. After watching this video, you should have a good understanding of how to implement stable recording of electrooculography which can be reliably used in the clinical setting.

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10.5K visualizações.  Kyorin University. The overall goal of the present oculogram is to observe the abnormality of saccade performance in patients especially in those with neurological disorders and to look at the pathophysiology underlying the disorder providing useful information about the diagnosis. This method can help answer key questions in the field such as diagnosis of patients with neurological disorders and to elucidate the pathophysiology underlying the disease. The main advantage of this technique is that it allows stab...