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>

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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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-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. 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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 group12,13,14,15,16,17,18,19.
Admittedly, VOG has a higher spatial accuracy than EOG and has largely replaced EOG in the clinical setting, but the higher accuracy of VOG and SSC should not always be taken at face value. EOG has been recorded in combination with VOG or SSC, and has shown performance comparable to the latter two despite small differences7,8,9. Comparison of saccade peak velocities simultaneously measured by EOG, VOG, and SSC consistently showed that peak velocity measured by EOG is slightly but consistently faster than those measured by the other two methods7,8,9. This faster velocity measured by EOG is generally ascribed to the greater noise level for EOG recording, such as contamination from the alpha and beta bands of EEG9. On the other hand, peak velocity measured by VOG is also higher than that recorded by SSC simultaneously7. This difference is attributed to the load of the search coil, influencing the saccade dynamics; possible slippage of the coil over the cornea, especially during blinks, may reduce the accuracy of eye movement measurement, leading to a slightly larger peak velocity measured by SSC than by VOG. In the present study, the peak velocity was lower when measured by EOG as compared to VOG. Presumably, this is because the low-pass filtering used here tends to decrease the peak velocity. Therefore, the difference in &#34;accuracy&#34; of each methodology may be due not only to the confounding noise, but also to how signals are processed (e.g., low-pass filtering) as well as to inherent limitations of each recording method (e.g., slippage of the search coil).
Meanwhile, EOG has a clear advantage over the other eye movement recording methods in certain recording situations, i.e., subjects with narrow eye clefts and with cataract lenses. To adjust the method for the narrow eye cleft, experimenters can tape up the eyelids of subjects while recording, but this can irritate the eyes and result in excessive blinking and tears, which hampers reliable recording. In contrast, EOG can be used in patients with cataract lenses. For VOG, the signal is lost due to aberrant reflection associated with cataract lenses. Similarly, blinks may virtually &#34;truncate&#34; the VOG records, because the signal is lost during blinks. In contrast, horizontal EOG is less affected by blink artifacts, although small &#34;spikes&#34; corresponding to blinks in the records may be seen.
EOG requires only a short time for preparation, and may even be applicable to many patients with movement disorders that are less severe. Some neurological patients may have difficulty in stabilizing their trunk. Such movements may be detrimental for recording VOG as well. Considering these aspects, EOG shows a sufficient level of accuracy for clinical assessment; it is not that EOG is inherently &#34;inaccurate&#34; as a method for recording eye movements.
A practical guideline for recording the EOG in clinical applications has been published in 201723. The protocol here extends this proposal by including some additional procedures to further stabilize the EOG recording. The corneo-retinal potential can fluctuate with time, due to factors such as the alertness of subjects or environmental influences such as ambient light. The magnitude of the corneo-retinal potential difference is affected by various conditions and increases during light adaptation, while dark adaptation causes a decrease24,25. With sufficient dark adaptation, therefore, the corneo-retinal potential is expected to stabilize, leading to reduced drift. To reduce fluctuation further, the gain of EOG was continuously monitored throughout the experiment, and re-calibration was also performed for adjustment when necessary throughout the experiments. This re-calibration procedure took only 10 - 20 s to perform, so this did not intervene much with the recording procedures, and reduced the fluctuation of EOG signal. If the experimenter waits for 10 - 20 min after placing the electrodes, sufficient light adaptation will take place and the impedance between the electrode and the skin will also decrease and gradually asymptote to a low level (down to 20k&#937;). The waiting period enables the recorded potential to stabilize dramatically from the beginning of the recording and to become increasingly stable with time.
Instead of the specialized dome embedding LEDs as described in this article, any board with LEDs embedded in a similar arrangement may be used. An alternate current (AC) amplifier can be used instead of a DC amplifier, but in this case, the amplitude of recorded saccades will not be reliable enough for qualitative assessment because of the signal decay. Electrodes having a wide fringe, which also serves to maintain close and wide contact with the skin, may be substituted for the electrode described in this article.
Some drawbacks of EOG should also be acknowledged. EOG is generally only adequate for recording horizontal eye movements, as raised in the Introduction. Furthermore, it is difficult to reliably assess microsaccades by the EOG method, whereas VOG has the capability to do so. This issue is especially important because of the saccadic spike potential and its fingerprint in the high frequency range26. Although these aspects could be problematic in the clinical context, they cannot be solved even with the present protocol and remains to be addressed in future studies. On the other hand, the eye position signal recorded by EOG can be contaminated by artifacts and noise, such as electromyography from facial muscles and electroencephalography. Also, when a DC amplifier is used, the recorded EOG signal can drift with time. These issues can be largely resolved by using an electrode with a plastic fringe that allows close and stable fixation as well as reduction of impedance between the skin and the electrode, effectively reducing the surrounding noise. Secondly, increasing the contact area between the gel and the skin by using a cup-electrode as described above, helps to lower the impedance at skin contact. Another way to avoid the drift is to wait for a period of 10 - 15 min after electrode placement, until sufficient light adaptation takes place. This waiting period also helps to further lower the impedance between the electrode (gel) and the skin, and the recorded EOG signal usually stabilizes as the time elapses. Repeating calibration and setting the gain of the gaze signal appropriately during the performance of oculomotor tasks can further help to improve the recording quality. The drift of eye position signal can pose a problem when recording smooth pursuit for which recording is usually made for an extended period. However, for recording saccades, whose duration lasts only for several tens of milliseconds, this is usually not an issue.
In summary, for achieving &#34;accurate&#34; EOG recording, it is not the methodology itself that matters, but how the experimenter implements it. The critical step is how to cope with the instability of the recording. The necessary measures are to use an Ag-AgCl electrode with a wide plastic fringe capable of effectively reducing noise, and to wait for sufficient light adaptation. This waiting period also helps to lower the impedance between the electrodes and the skin, thereby ensuring a stable signal recorded. Furthermore, re-calibration is performed as needed during the task performance. Thus implemented, EOG can still be a method of high clinical practicability that can be widely applied to neurological patients, especially for recording saccades in the horizontal direction. Indeed, EOG can be a preferable method when only this is available for economic reasons or in practical clinical situations where a readily implemented method is required and where omission of data is not permissible.

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.

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	<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 obtained by the two methods largely overlap with each other. Also, the saccade parameters, such as latency and amplitude, are almost comparable for the two recording methods, although the velocity is slightly smaller for EOG (VGS: Figure 2B, AS: Figure 2C).
For EOG, electromyography and electroencephalography can confound eye movement records, which usually necessitates the use of low-pass filtering for proper eye recording. The use of low-pass filtering at 20 Hz has been reported to decrease the peak velocity, and to increase the onset of saccades slightly; the velocity of saccades is smaller by up to 10% for VGS and MGS, and the latency measured by EOG is longer than that measured by VOG by 2 - 3% (or on the order of 8 - 10 ms), whereas the amplitude of saccades is largely comparable22. On the other hand, previous studies by other groups have reported larger saccade velocity for EOG as compared to both VOG and SSC7,8,9,10, and the discrepancy between studies was considered due to the use of a smoothing procedure to calculate the saccade velocity profile and the low-pass filtering as mentioned.
<img alt="Figure 1" class="xfigimg" src="/files/ftp_upload/56934/56934fig1.jpg" /> 
Figure 1: The electrode and adhesive tape used for recording EOG. The electrode has a diameter of 1.8 cm and a thickness of 3.5 mm, where the bottom comprises the Ag-AgCl electrode and the lateral wall is surrounded by a plastic fringe of 5 mm thickness. This enables wide contact with the skin, allowing close and stable fixation, and serves to reduce the impedance between the skin and the electrode. Due to this, the recording becomes stable with time, thereby effectively reducing the artifacts from facial muscles and electroencephalography. <a href="https://cloudflare-jove-com.remotexs.ntu.edu.sg/files/ftp_upload/56934/56934fig1large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
<img alt="Figure 2" class="xfigimg" src="/files/ftp_upload/56934/56934fig2.jpg" /> 
Figure 2: Representative traces of saccades recorded by EOG and VOG. (A) Representative traces recorded by EOG and VOG. 8 VGS traces are superimposed, time-locked to the signal instructing the start of saccades. Saccades towards targets of four different eccentricities (5, 10, 20, and 30 degrees) to the left and right from the central fixation spot are recorded. The horizontal axis gives the time and the vertical axis gives the eye position (upper trace) or velocity (lower traces). The red curves are for VOG and the gray curves are for EOG. Ticks below are marked at a 100 ms interval. Gray curves are for EOG measured by the DC amplifier, and the red curves are for VOG measured by the video-based eye tracking system. When the eyes move to the right, the traces deflect upwards and when the eyes move to the left, they deflect downwards. Note the substantial overlap between the traces, except that the gray traces (EOG) are slightly displaced towards the right compared to the red traces (VOG), implying a slightly longer latency for EOG relative to VOG. (B) Comparison of EOG and VOG traces in the VGS task. Red curves are for EOG and black and blue curves are for VOG of the left and right eyes, respectively. The upper trace is for eye position, and the lower figure is for eye velocity. Again note the 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. (C) Comparison of EOG and VOG traces in the AS task. Similar EOG and VOG traces when subjects perform the AS task. Note again the substantial overlap and that the latency is slightly longer for EOG, and the velocity curve for EOG shows a slightly lower peak velocity than that for VOG. <a href="https://cloudflare-jove-com.remotexs.ntu.edu.sg/files/ftp_upload/56934/56934fig2large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>

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

Nanyang Technological University

Research

JoVE Journal

Behavior

10.6K Views.  Kyorin University. 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.

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

How to Detect Amygdala Activity with Magnetoencephalography using Source Imaging

In trace fear conditioning a conditional stimulus (CS) predicts the occurrence of the unconditional stimulus (UCS), which is presented after a brief stimulus free period (trace interval)1. Because the CS and UCS do not co-occur temporally, the subject must maintain a representation of that CS during the trace interval. In humans, this type of learning requires awareness of the stimulus contingencies in order to bridge the trace interval2-4. However when a face is used as a CS, subjects can implicitly learn to fear the face even in the absence of explicit awareness*. This suggests that there may be additional neural mechanisms capable of maintaining certain types of "biologically-relevant" stimuli during a brief trace interval. Given that the amygdala is involved in trace conditioning, and is sensitive to faces, it is possible that this structure can maintain a representation of a face CS during a brief trace interval.
It is challenging to understand how the brain can associate an unperceived face with an aversive outcome, even though the two stimuli are separated in time. Furthermore investigations of this phenomenon are made difficult by two specific challenges. First, it is difficult to manipulate the subject's awareness of the visual stimuli. One common way to manipulate visual awareness is to use backward masking. In backward masking, a target stimulus is briefly presented (&lt; 30 msec) and immediately followed by a presentation of an overlapping masking stimulus5. The presentation of the mask renders the target invisible6-8. Second, masking requires very rapid and precise timing making it difficult to investigate neural responses evoked by masked stimuli using many common approaches. Blood-oxygenation level dependent (BOLD) responses resolve at a timescale too slow for this type of methodology, and real time recording techniques like electroencephalography (EEG) and magnetoencephalography (MEG) have difficulties recovering signal from deep sources.
However, there have been recent advances in the methods used to localize the neural sources of the MEG signal9-11. By collecting high-resolution MRI images of the subject's brain, it is possible to create a source model based on individual neural anatomy. Using this model to "image" the sources of the MEG signal, it is possible to recover signal from deep subcortical structures, like the amygdala and the hippocampus*.

This article describes how to record amygdala activity with magnetoencephalography (MEG). In addition this article will describe how to conduct trace fear conditioning without awareness, a task that activates the amygdala. It will cover 3 topics: 1) Designing a trace conditioning paradigm using backward masking to manipulate awareness. 2) Recording brain activity during the task using magnetoencephalography. 3) Using source imaging to recover signal from subcortical structures.

In trace fear conditioning a conditional  stimulus (CS) predicts the occurrence of the unconditional stimulus (UCS),  which is presented after a brief ...

Automated Visual Cognitive Tasks for Recording Neural Activity Using a Floor Projection Maze

Neuropsychological tasks used in primates to investigate mechanisms of learning and memory are typically visually guided cognitive tasks. We have developed visual cognitive tasks for rats using the Floor Projection Maze1,2&#160;that are optimized for visual abilities of rats permitting stronger comparisons of experimental findings with other species.
In order to investigate neural correlates of learning and memory, we have integrated electrophysiological recordings into fully automated cognitive tasks on the Floor Projection Maze1,2. Behavioral software interfaced with an animal tracking system allows monitoring of the animal's behavior with precise control of image presentation and reward contingencies for better trained animals. Integration with an in vivo electrophysiological recording system enables examination of behavioral correlates of neural activity at selected epochs of a given cognitive task.
We describe protocols for a model system that combines automated visual presentation of information to rodents and intracranial reward with electrophysiological approaches. Our model system offers a sophisticated set of tools as a framework for other cognitive tasks to better isolate and identify specific mechanisms contributing to particular cognitive processes.

We describe protocols for training rats for chronic electrophysiological recordings in fully automated cognitive tasks on a Floor Projection Maze.

Neuropsychological tasks used in primates to investigate mechanisms of learning and memory are typically visually guided cognitive tasks. We have ...

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 ...

A Wireless, Bidirectional Interface for In Vivo Recording and Stimulation of Neural Activity in Freely Behaving Rats

In vivo electrophysiology is a powerful technique to investigate the relationship between brain activity and behavior at a millisecond and micrometer scale. However, current methods mostly rely on tethered cable recordings or only use unidirectional systems, allowing either recording or stimulation of neural activity, but not at the same time or same target. Here, a new wireless, bidirectional device for simultaneous multichannel recording and stimulation of neural activity in freely behaving rats is described. The system operates through a single portable head stage that both transmits recorded activity and can be targeted in real-time for brain stimulation using a telemetry-based multichannel software. The head stage is equipped with a preamplifier and a rechargeable battery, allowing stable long-term recordings or stimulation for up to 1 h. Importantly, the head stage is compact, weighs 12 g (including battery) and thus has minimal impact on the animal&#180;s behavioral repertoire, making the method applicable to a broad set of behavioral tasks. Moreover, the method has the major advantage that the effect of brain stimulation on neural activity and behavior can be measured simultaneously, providing a tool to assess the causal relationships between specific brain activation patterns and behavior. This feature makes the method particularly valuable for the field of deep brain stimulation, allowing precise assessment, monitoring, and adjustment of stimulation parameters during long-term behavioral experiments. The applicability of the system has been validated using the inferior colliculus as a model structure.

A Wireless, Bidirectional Interface for In Vivo Recording and Stimulation of Neural Activity in Freely Behaving Rats

A wireless, bidirectional system for multi-channel neural recordings and stimulation in freely behaving rats is introduced. The system is light and compact, thus having minimal impact on the animal&#180;s behavioral repertoire. Moreover, this bidirectional system provides a sophisticated tool to assess causal relationships between brain activation patterns and behavior.

In vivo electrophysiology is a powerful technique to investigate the relationship between brain activity and behavior at a millisecond and micrometer ...

Treating Low Back Pain in Failed Back Surgery Patients with Multicolumn-lead Spinal Cord Stimulation

Failed back surgery syndrome (FBSS) refers to persistent, chronic pain following spinal surgery. Spinal cord stimulation with dorsal epidural leads can be used to treat back and leg pain in FBSS patients. This paper presents a detailed protocol for using spinal cord stimulation with surgical leads in FBSS patients. In our department, with the patient under general anesthesia, we place the lead in the epidural space by means of a small laminectomy at the 10th thoracic level. Placement of the lead is followed by a 1 month trial period with an externalized lead. If pain relief is greater than 50% at the end of this 1 month stimulation trial (required by Belgian reimbursement criteria), an internal pulse generator is then placed under the skin and connected to the lead in a second surgical procedure. We have demonstrated that using this technique in rigorously selected FBSS patients can significantly improve back pain, leg pain, patient activity, and quality of life for a sustained period of time.

This paper presents a method that uses spinal cord stimulation with a multicolumn lead to treat neuropathic low back pain in failed back surgery patients.

Failed back surgery syndrome (FBSS) refers to persistent, chronic pain following spinal surgery. Spinal cord stimulation with dorsal epidural leads can be ...

Using Electroencephalography Measurements and High-quality Video Recording for Analyzing Visual Perception of Media Content

This article explores a method to detect differences in visual perception in humans. The method used is based on the psychological (or "cognitive") function of eyeblinks. Participants' eyeblinks are detected and acquired while watching videos specifically created for the investigation. The detection and acquisition of eyeblinks are carried out with the help of a 20-channel electroencephalographic (EEG) wireless device. The international 10-20 system for electrode placement is followed. A high-definition (HD) video camera is used to record participants' facial expressions, for contrast purposes. Instead of using pre-existing media content, purpose-made video content has been created following specific criteria of interest for this investigation, with stimuli enabling researchers to manage the precise parameters of interest. Otherwise, results could be contaminated with uncontrolled variables. The synchronization of the presentation of video stimuli with EEG recordings needs to be done in milliseconds. Analysis of collected data is performed with robust software for working with big matrices. Statistically significant differences in eyeblink rate related to media professionalization and editing style are found with the reported experimental procedures.

We present detection, acquisition, and analysis of eyeblink rates while watching media content.

This article explores a method to detect differences in visual perception in humans. The method used is based on the psychological (or "cognitive") ...

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 ...

Home-Based Prescribed Pulmonary Exercise in Patients with Stable Chronic Obstructive Pulmonary Disease

As a systemic disease, chronic obstructive pulmonary disease (COPD) affects the respiratory system, inducing restless and exercise dyspnea. It also impacts exercise capacity and forms a vicious circle in which it further aggravates the condition of patients and accelerates disease progression. As a functional holistic exercise, traditional Chinese exercises (TCE) play an important role in the rehabilitation of COPD on the basis of adjusting the breath and performing coordinated movements. This study investigates the effects of prescribed pulmonary exercises (which are modified from TCE) on exercise capacity of upper and lower limbs, endurance exercise capacity, and quality of life in stable COPD patients. The goal is to determine the accessibility of these prescribed exercises in COPD rehabilitation. Participants are randomly divided into a non-exercise control group (CG) or prescribed pulmonary exercise group (PG) at a ratio of 1: 1. The PG receives intervention for 60 min twice per day, 7 days a week, for a total of 3 months. The intensity is measured using the Borg category-ratio 10 scale and with a heart-rate monitor. Then, an exercise capacity test and quality of life questionnaire are scheduled at 1 week before and after the formal intervention. After 3 months of intervention, the 30 s arm curl test, 30 s sit-to-stand test, 6 min walking test, and quality of life show significant improvement in COPD patients (p &#60; 0.05). These findings indicate that prescribed pulmonary exercises can be applied as alternative, convenient, and effective home- and community-based exercises for stable COPD patients.

Presented here is a protocol to investigate the effects of home-based prescribed pulmonary exercise in stable chronic obstructive pulmonary disease (COPD) patients, which is modified based on traditional Chinese exercises according to dyspnea and limited exercise capacity observed in COPD patients.

As a systemic disease, chronic obstructive pulmonary disease (COPD) affects the respiratory system, inducing restless and exercise dyspnea. It also ...

Assessing the Coherence of Parents' Short Narratives Regarding their Child Using the Five-Minute Speech Sample Procedure

Valid and efficient measures for assessing the quality of parent-child relationships are needed to facilitate research and evidence-based practice with parents. This paper focuses on such a method, namely Five-Minute Speech Sample-Coherence (FMSS-Coherence). In this method, a parent is asked to speak for five uninterrupted minutes about her/his child and their relationship. The resulted narrative is coded for coherence, namely the extent to which the parent provides&#160;in the narrative&#160;a clear, consistent, multidimensional and well-supported portrayal of the child. FMSS-Coherence is based on attachment research that shows that the coherence of parents&#8217; narratives is indicative of the quality of the parent-child relationship and child adjustment. It overcomes the limitations of attachment narrative measures which are typically labor intensive. FMSS-Coherence is less nuanced than extant attachment narrative measures. Yet, studies of families from different cultural backgrounds, across different child ages and in the context of typically developing children as well as children with special needs suggest that coherence can be reliably evaluated using the FMSS procedure. Furthermore, parents&#8217; FMSS-Coherence is associated with parenting quality and children&#8217;s socio-emotional adjustment. Thus, it holds promise for researchers and practitioners who seek a relatively time- and cost-effective method for assessing the coherence of parents&#8217; narratives regarding their child.

This paper introduces a method for assessing the coherence of parents' short narratives regarding their child and their relationship using the five-minute speech sample procedure.

Valid and efficient measures for assessing the quality of parent-child relationships are needed to facilitate research and evidence-based practice with ...

Using Unidirectional Rotations to Improve Vestibular System Asymmetry in Patients with Vestibular Dysfunction

The vestibular system provides information about head movement and mediates reflexes that contribute to balance control and gaze stabilization during daily activities. Vestibular sensors are located in the inner ear on both sides of the head and project to the vestibular nuclei in the brainstem. Vestibular dysfunction is often due to an asymmetry between input from the two sides. This results in asymmetrical neural inputs from the two ears, which can produce an illusion of rotation, manifested as vertigo. The vestibular system has an impressive capacity for compensation, which serves to rebalance how asymmetrical information from the sensory end organs on both sides is processed at the central level. To promote compensation, various rehabilitation programs are used in the clinic; however, they primarily use exercises that improve multisensory integration. Recently, visual-vestibular training has also been used to improve the vestibulo-ocular reflex (VOR) in animals with compensated unilateral lesions. Here, a new method is introduced for rebalancing the vestibular activity on both sides in human subjects. This method consists of five unidirectional rotations in the dark (peak velocity of 320&#176;/s) toward the weaker side. The efficacy of this method was shown in a sequential, double-blinded clinical trial in 16 patients with VOR asymmetry (measured by the directional preponderance in response to sinusoidal rotations). In most cases, VOR asymmetry decreased after a single session, reached normal values within the first two sessions in one week, and the effects lasted up to 6 weeks. The rebalancing effect is due to both an increase in VOR response from the weaker side and a decrease in response from the stronger side. The findings suggest that unidirectional rotation can be used as a supervised rehabilitation method to reduce VOR asymmetry in patients with longstanding vestibular dysfunction.

A new rehabilitation method is presented for rebalancing the vestibular system in patients with asymmetric responses, which consists of unidirectional rotations toward the weaker side. By directly modifying the vestibular pathway rather than enhancing the multisensory aspects of compensation, asymmetry can be normalized within 1-2 sessions and show lasting effects.

The vestibular system provides information about head movement and mediates reflexes that contribute to balance control and gaze stabilization during ...

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

Summary

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Chapters in this video

How to Detect Amygdala Activity with Magnetoencephalography using Source Imaging

Automated Visual Cognitive Tasks for Recording Neural Activity Using a Floor Projection Maze

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

A Wireless, Bidirectional Interface for In Vivo Recording and Stimulation of Neural Activity in Freely Behaving Rats

Treating Low Back Pain in Failed Back Surgery Patients with Multicolumn-lead Spinal Cord Stimulation

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

Home-Based Prescribed Pulmonary Exercise in Patients with Stable Chronic Obstructive Pulmonary Disease

Assessing the Coherence of Parents' Short Narratives Regarding their Child Using the Five-Minute Speech Sample Procedure

Using Unidirectional Rotations to Improve Vestibular System Asymmetry in Patients with Vestibular Dysfunction