Published date: Dec 31 2024

Journal Title: Journal of Ophthalmic and Vision Research

Issue title: Oct–Dec 2024, Volume 19, Issue 4

Pages: 449 - 458

DOI: 10.18502/jovr.v19i4.14429

Elissavet Kemanetzogloulisakemanetzoglou@gmail.comFirst Department of Neurology, National and Kapodistrian University of Athens, Eginition Hospital, School of Medicine, Athens, Greece

Klio Chatzistefanoukliochat@med.uoa.grFirst Department of Ophthalmology, National and Kapodistrian University of Athens Gennimatas General Hospital, School of Medicine, Athens, Greece

Nikolaos Smyrnissmyrnis@med.uoa.grSecond Department of Psychiatry, National and Kapodistrian University of Athens, Attikon General Hospital, School of Medicine, Athens, Greece

Evangelia Kararizouekarariz@med.uoa.grFirst Department of Neurology, National and Kapodistrian University of Athens, Eginition Hospital, School of Medicine, Athens, Greece

Evangelos Anagnostoueanagnost@eginitio.uoa.grFirst Department of Neurology, National and Kapodistrian University of Athens, Eginition Hospital, School of Medicine, Athens, Greece

Purpose: To examine the natural adaptive course of ocular motor system in unilateral abducens nerve palsy while addressing the scarce literature on saccade dynamics and natural adaptation.
Methods: Binocular horizontal eye movements were recorded from 18 healthy adults and 21 adults with unilateral abducens nerve palsy during the acute and chronic phases. Dynamics of the paretic and non-paretic eyes were compared, and the non-paretic eye dynamics were correlated with the respective prism diopters. Non-parametric tests were used for statistical comparisons.
Results: The paretic eye, compared to the non-paretic eye, presented a slightly lower saccadic gain and velocity/amplitude ratio and a higher duration/amplitude ratio. The nonparetic eye, compared to healthy controls, showed consistent amplitude gain (>1) and a tendency for a higher duration/amplitude ratio. In the acute phase, when the non-paretic eye was covered, the paretic eye’s amplitude ratio was lower and the duration/amplitude ratio decreased significantly. In the acute phase, a greater degree of esotropia in the paretic eye was associated with a lower amplitude gain and duration/amplitude ratio in the nonparetic eye.
Conclusion: During adaptation in abducens nerve palsy, the saccade duration of the paretic eye increased, and a similar tendency was observed in the non-paretic eye. This finding likely reflects a change in the “pulse-step” pattern and may be related to plastic changes in central structures, such as the cerebellum, that support learning processes.

Keywords: Saccade, Abducens nerve palsy, Eye Movements

1. Abel LA, Schmidt D, Dell’Osso LF, Daroff RB. Saccadic system plasticity in humans. Ann Neurol 1978;4:313–318.

2. Sparks DL. The brainstem control of saccadic eye movements. Nat Rev Neurosci 2002;3:952–964.

3. Danchaivijitr C, Kennard C. Diplopia and eye movement disorders. Neurol Pract 2004;75:iv24–iv31.

4. Richards BW, Jones FR, Younge BR. Causes and prognosis in 4,278 cases of paralysis of the oculomotor, trochlear, and abducens cranial nerves. Am J Ophthalmol 1992;113:489–496.

5. Peters GB, Bakri SJ, Krohel GB. Cause and prognosis of nontraumatic sixth nerve palsies in young adults. Ophthalmology 2002;109:1925–1928.

6. Leigh RJ, Zee DS. The neurology of eye movements. 4th ed. Oxford University Press; 2015.

7. Ramat S, Leigh RJ, Zee DS, Optican LM. What clinical disorders tell us about the neural control of saccadic eye movements. Brain 2007;130:10–35.

8. Bronstein AM, Rudge P, Gresty MA, Du Boulay G, Morris J. Abnormalities of horizontal gaze. Clinical, oculographic and magnetic resonance imaging findings. II. Gaze palsy and internuclear ophthalmoplegia. J Neurol Neurosurg Psychiatry 1990;53:200–207.

9. Optican LM, Zee DS, Chu FC. Adaptive response to ocular muscle weakness in human pursuit and saccadic eye movements. J Neurophysiol 1985;54:110–122.

10. Anagnostou E, Spengos K, Margeti S, Vassilopoulou S, Paraskevas GP, Zis V. Vertical and horizontal integrator failure in a ponto-medullary infarction: A possible role for paramedian tract neurons. J Neurol Sci 2009;280:118–119.

11. Snow R, Hore J, Vilis T. Adaptation of saccadic and vestibulo-ocular systems after extraocular muscle tenectomy. Invest Ophthalmol Vis Sci 1985;26:924–931.

12. Wong AMF, McReelis K, Sharpe JA. Saccade dynamics in peripheral vs central sixth nerve palsies. Neurology 2006;66:1390–1398.

13. Munoz DP, Everling S. Look away: The anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 2004;5:218–228.

14. Chen AL, Ramat S, Serra A, King SA, Leigh RJ. The role of the medial longitudinal fasciculus in horizontal gaze: Tests of current hypotheses for saccade-vergence interactions. Exp Brain Res 2011;208:335–343.

15. Schmidt RA, Zelaznik H, Hawkins B, Frank JS, Quinn Jr. JT. Motor-output variability: A theory for the accuracy of rapid motor acts. Psychol Rev 1979;86:415–451.

16. Wong AM, Sharpe JA. Adaptations and deficits in the vestibulo-ocular reflex after third nerve palsy. Arch Ophthalmol 2002;120:360–368.

17. Sharpe JA, Wong AMF, Fouladvand M. Ocular motor nerve palsies: Implications for diagnosis and mechanisms of repair. Prog Brain Res 2008;171:59–66.

18. Anagnostou E, Kouzi I, Kararizou E. Painful ophthalmoplegia: The role of imaging and steroid response in the acute and subacute setting. J Neurol Sci 2013;331:145–149.

19. Goffart L, Bourrelly C, Quinton JC. Neurophysiology of visually guided eye movements: Critical review and alternative viewpoint. J Neurophysiol 2018;120:3234– 3245.

20. Huber A. Electromyography of eye muscles. Trans Ophthal Soc UK 1962;62:455–472.

21. Metz HS, Scott AB, O’meara D, Stewart HL. Ocular saccades in lateral rectus palsy. Arch Ophthalmol 1970;84:453–460.

22. Weber RB, Daroff RB. The metrics of horizontal saccadic eye movements in normal humans. Vision Res 1971;11:921– 928.

23. Zingale CM KE. Planning sequences of saccades. Vision Res 1987;27:1327–1341.

24. Collewijn H, Erkelens CJ, Steinman RM. Binocular coordination of human horizontal saccadic eye movements. J Physiol 1998;404:157–182.

25. Bahill AT, Clark MR, Stark L. The main sequence, a tool for studying human eye movements. Math Biosci 1975;24:191–204.

26. Gibaldi A, Sabatini SP. The saccade main sequence revised: A fast and repeatable tool for oculomotor analysis. Behav Res Methods 2021;53:167–187.

27. Pickwell LD. Hering’s law of equal innervation and the position of the binoculus. Vision Res 1972;12:1499–1507.

28. Bucci MP, Kapoula Z, Eggert T, Garraud L. Deficiency of adaptive control of the binocular coordination of saccades in strabismus. Vision Res 1997;37:2767–2777.

29. Bucci MP, Kapoula Z, Yang Q, Roussat B, Brémond-Gignac D. Binocular coordination of saccades in children with strabismus before and after surgery. Invest Ophthalmol Vis Sci 2002;43:1040–1047.

30. Kapoula Z, Bucci MP, Eggert T GL. Impairment of the binocular coordination of saccades in strabismus. Vision Res 1997;37:2757–2766.

31. De Brouwer S, Yuksel D, Blohm G, Missal M, Lefèvre P. What triggers catch-up saccades during visual tracking? J Neurophysiol 2002;87:1646–1650.

32. Theopold H, Kommerell G. Phasische und tonische Funktion den Augenmuskeln – Untersuchungen an Patienten mit Oculomotorius- oder Abducens-Paralyse. Albr Von Graefes Arch Klin Exp Ophthalmol 1974;192:247– 254.

33. Kommerell G, Olivier D, Theopold H. Adaptive programming of phasic and tonic components in saccadic eye movements. Investigations of patients with abducens palsy. Invest Ophthalmol Vis Sci 1976;15:657–660.

34. Zee DS, Yee RD. Abnormal saccades in paralytic strabismus. Am J Ophthalmol 1977;83:112–114.

35. Kömpf D. Dynamik der Augenbewegungen beim Lähmungsschielen. Fortschr Neurol Psychiatr 1986;54:259–266.

36. Straube A, Deubel H. Rapid gain adaptation affects the dynamics of saccadic eye movements in humans. Vision Res 1995;35:3451–3458.