JIN  2018, Vol. 17 Issue (3): 211-220    DOI: 10.31083/JIN-170055
 Research article Previous articles | Next articles
Saccadic dysfunction in patients with hypoxic-ischemic encephalopathy
Elena L. Teslenko1,Elena V. Damyanovich1,Ilija Damjanović2,*(),Zoran Gačić3,Boris K. Baziyan1
1 Research Center of Neurology, Volokolamskoye Highway, 80, Moscow, Russian Federation
2 Institute for Information Transmission Problems of the Russian Academy of Sciences, Moscow, Russian Federation
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Abstract

Electrophysiological monitoring of saccadic eye movements in patients with hypoxic-ischemic encephalopathy was carried out. Externally guided saccades (prosaccades) were recorded using a patented hardware-software complex for studying a subject's physical activity. Recordings were performed in two independent experimental procedures - for saccades separately and when they were coordinated with movement of the head and hand. In both cases statistically significant differences of latent period and duration of saccadic eye movement were detected for hypoxic-ischemic encephalopathy subjects in comparison with healthy controls of the same age (p < 0.05). Jerking and deviation of eyes after gaze fixation on a target were often present in hypoxic-ischemic encephalopathy subjects. In some cases saccades of these subjects were asymmetrical among themselves. Hypoxic-ischemic encephalopathy induced changes in the parameters of autosaccades were also found They were expressed through instability of gaze fixation periods, sometimes asymmetric eye movements, slow gaze shift from one target to another, and disturbance of gaze stabilization (jerking of eyeballs during the saccadic period).

Submitted:  14 August 2017      Accepted:  13 October 2017      Published:  15 August 2018
*Corresponding Author(s):  Ilija Damjanovi?     E-mail:  damjanov@iitp.ru

Elena L. Teslenko,Elena V. Damyanovich,Ilija Damjanović,Zoran Gačić,Boris K. Baziyan. Saccadic dysfunction in patients with hypoxic-ischemic encephalopathy. JIN, 2018, 17(3): 211-220.

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Fig. 1.  Hardware-software complex unit for studying physical activity of a subject. (A) A photo of the equipment: 1 - horizontal support; 2 - plastic helmet; 3 - hand lever used for movement of the cursor (5); 4 - hand movement indicator (detector); 6 - head movement indicator (detector); 7 - light emitting LEDs located at different positions along the horizontal support; each LED provided a single visual target. Detailed description of the equipment is given in the text. (B) A photo made during the coordinated test: The subject visually fixates on the far right and simultaneously moves the hand lever (${40^\circ}$ gaze shift to the right; rightward hand movement - 54 cm). Detailed explanation of the coordinated test (Test 2) is given in the text.

Fig. 2.  Differences in the mean value of saccade durations (A) and latent periods (B) between HIE subjects and healthy controls (norm) of the same age group in the Test 1 (Mann-Whitney U-test: small inner "$\Box$" - median; large outside "$\Box$" - 25%-75%; "I" - non outlier range (max and min value); p < 0.05). P-values for comparisons between the data of right and left saccades of two groups of subjects are given in the top right corners. A participant (HIE patient or healthy person) was initially positioned in front of the far left diode (control position). They were instructed to fixate on other LEDs as they illuminated sequentially in a quasi random sequence within the right half of the visual field i.e. right saccades were thus evoked (left eye right, right eye right). In the second part of the procedure a subject was placed in the front of the far right LED and left saccades were recorded (left eye left, right eye left). Distances between LEDs were arranged such that the peripheral visual targets were located 10, 20, 30 and 40 40${^\circ}$ apart from the control stimulus (far left or far right LED). Only 40 40${^\circ}$ saccades were recorded and afterwards processed and analysed. Detailed explanation of Test 1 is given in the text.

Fig. 3.  Saccadic movements to the right (Test 1; single responses from the series of 30 recorded prosaccades). (A) control; (B) HIE subject (with increased latent period and duration of saccadic eye movements); (C) multisaccades recorded in one HIE subject: 1, 2 - durations of the first and the second right eye saccades, respectively; 1', 2' - durations of the first and the second left eye saccades, respectively; note that second right eye saccade was interrupted by transient eye jerking (3)subsequently right eye stabilized on the lateral target (detailed explanation in the text). LP - saccadic latent periods, D - duration of saccades. Downward oriented vertical arrows indicate beginning of stimulation i.e. moment of target relocation from the control to peripheral position; upward oriented vertical arrows indicate moment of return of target from the peripheral to the control position. Saccades amplitudes - 40${^\circ}$. Time scale given at bottom.

Fig. 4.  Comparison of saccadic eye movement for HIE subjects and controls (norm) in same age group in coordinated test (Mann-Whitney U-test; $p <$ 0.05). $p$-values for comparisons between the averaged values of saccade durations (A) and the latencies (B) of the two subject groups are given in top right corners. Latency and duration of saccadic movement was independently recorded at 40 $\mathrm{{}^\circ}$ for gaze shifts of right and left saccades independently. Other conditions identical to Fig. 2. Detailed explanation of coordinated test (Test 2) given in the text.

Fig. 5.  Differences between Test 1 and Test 2 in averaged value of saccade durations (A) and latencies (B) for HIE subjects (Wilcoxon matched pairs test; $p <$ 0.05). P-values for comparisons between the saccade parameters in the two tests are given in the right bottom corner. Other conditions identical to Fig. 2.

Fig. 6.  Coordinated movements of eyes, head and hand for 40 $\mathrm{{}^\circ}$ gaze shift to the left. (A) control (a single response from 30 recorded prosaccades); note sequence of eye, head and hand movements typical for controls - initially eyes moved towards the target, subsequently a slightly delayed, head turn was initiated, followed by initiation of hand movement; (B) HIE subject (an inadequate single response from 25 recorded prosaccades). Other conditions identical to Fig. 3.

Fig. 7.  (A) control autosaccades; (B) HIE subject autosaccades. Time scales given at bottom.

Table 1  The range of saccade latencies recorded during a series of stimuli in 22 HIE subjects during Test 1 and Test 2 for right and left saccades. In both tests, a series of visual targets were presented to each subject as peripheral stimuli at 40${^\circ}$ 20-30 times. Latent periods were measured for all accurate saccades recorded in the series. Minimum, maximum and averaged ("mean") values were calculated for each patient in both, Test 1 and Test 2 are given in this Table (in "ms"). The averaged data were used for further statistical analysis (Fig. 2B, Fig. 4B and Fig. 5B). Ranges of saccade latencies -differences between min and max values. Detailed explanation in the text.
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