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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
3 Institute for Multidisciplinary Research, University of Belgrade, Belgrade, Serbia
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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).

Key words:  Saccades      brain ischemia      hypoxic-ischemic encephalopathy      hardware-software complex     
Submitted:  14 August 2017      Accepted:  13 October 2017      Published:  15 August 2018     
*Corresponding Author(s):  Ilija Damjanovi?     E-mail:  damjanov@iitp.ru

Cite this article: 

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.

URL: 

https://jin.imrpress.org/EN/10.31083/JIN-170055     OR     https://jin.imrpress.org/EN/Y2018/V17/I3/211

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.
Patient # Left eye right Right eye right Left eye left Right eye left
Test-1 Test-2 Test-1 Test-2 Test-1 Test-2 Test-1 Test-2
mean min max mean min max mean min max mean min max mean min max mean min max mean min max mean min max
1 204 198 226 232 204 247 204 198 216 229 201 247 222 212 232 226 200 251 221 212 230 225 200 250
2 266 251 273 251 234 281 266 250 271 251 232 280 295 286 304 276 251 301 295 286 304 276 250 301
3 259 245 275 251 226 280 258 244 272 250 225 278 268 257 278 249 226 278 267 257 277 251 226 282
4 237 224 250 249 223 273 238 226 250 247 223 271 243 231 256 244 220 269 245 231 259 245 221 269
5 215 205 226 225 202 246 215 205 226 224 202 244 239 229 248 235 210 265 237 227 248 230 207 263
6 263 246 274 250 233 283 263 246 272 255 236 287 276 265 290 273 245 300 279 269 290 273 245 300
7 227 216 230 244 219 257 228 215 231 242 219 255 241 227 253 238 214 262 239 225 253 238 214 262
8 213 208 230 236 211 259 219 208 230 234 211 257 234 222 243 235 212 262 231 219 243 235 212 262
9 253 240 268 253 231 288 254 241 267 252 230 286 266 255 277 252 226 284 266 255 277 252 226 284
10 221 211 236 238 213 261 222 211 234 238 213 264 243 228 255 238 211 264 240 226 254 236 211 262
11 245 231 259 246 221 268 244 231 257 244 220 268 259 246 273 241 222 268 259 246 273 247 222 272
12 261 248 276 253 236 287 263 250 276 253 236 286 273 261 284 263 242 290 276 265 287 263 242 290
13 234 221 247 240 218 268 234 223 245 243 220 267 247 231 257 258 235 286 245 231 255 260 235 286
14 273 250 278 255 232 290 270 248 278 254 231 290 279 270 294 265 240 294 284 274 294 263 240 292
15 226 214 232 241 218 256 226 214 232 241 218 257 231 220 244 240 216 264 233 220 246 240 216 264
16 248 235 263 245 223 275 247 235 262 248 225 275 253 240 266 246 228 276 254 242 266 246 228 276
17 231 216 244 246 221 271 229 216 242 246 221 271 243 229 256 251 225 277 243 229 256 250 225 275
18 258 243 268 257 236 286 259 245 267 257 236 288 267 256 278 250 223 275 268 258 278 253 221 277
19 251 239 263 248 220 276 250 237 263 248 220 275 259 248 272 250 223 277 260 248 274 251 225 277
20 248 235 262 246 222 270 247 235 260 245 222 268 260 246 272 246 222 272 258 244 272 248 224 272
21 262 248 274 251 228 284 261 247 275 252 228 282 273 261 279 253 226 278 269 261 279 251 223 279
22 240 232 254 238 223 275 239 230 256 238 221 273 255 245 266 245 226 278 255 245 266 248 226 280
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