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Pendular Oscillation and Ocular Bobbing After Pontine Hemorrhage

Abstract

The pathophysiology of acute, vertical spontaneous eye movements following pontine hemorrhage is not well understood. Here, we present and discuss the video-oculography findings of a patient with acute pontine hemorrhage who developed vertical pendular oscillation and ocular bobbing while comatose. The amplitudes, peak velocities, frequency distribution, and phase planes (velocity versus position) of the eye movements were analyzed. The vertical pendular oscillation was rhythmic with a peak frequency of 1.7 Hz, but amplitudes (mean 1.9°, range 0.2–8.2°) and peak velocities (mean 20.6°/s; range 5.9–60.6°/sec) fluctuated. Overall, their peak velocities were asymmetric, faster with downward than upward. Higher peak velocities were seen with larger amplitudes (downward phase r = 0.95, p < 0.001; upward phase r = 0.91, p < 0.001) and with movements beginning at eye positions lower in the orbit (downward phase r = − 0.64, p < 0.001; upward phase r = − 0.86, p < 0.001). Interspersed were typical ocular bobbing waveforms with a fast (peak velocity 128.8°/s), large-amplitude (17.5°) downward movement, sometimes followed by a flat interphase interval (0.5 s) when the eye was nearly stationary, and then a slow return to mid-position with a decaying velocity waveform. To account for the presence and co-existence of pendular oscillations and bobbing, we present and discuss three hypothetical models, not necessarily mutually exclusive: (1) oscillations originating in the inferior olives due to disruption of the central tegmental tract(s); (2) unstable neural integrator function due to pontine cell group damage involving neurons involved in gaze-holding; (3) low-frequency saccadic intrusions following omnipause neuron damage.

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References

  1. 1.

    Fisher CM. Ocular bobbing. Arch Neurol. 1964;11:543–6.

    CAS  Article  Google Scholar 

  2. 2.

    Mehler MF. The clinical spectrum of ocular bobbing and ocular dipping. J Neurol Neurosurg Psychiatry. 1988;51:725–7.

    CAS  Article  Google Scholar 

  3. 3.

    Susac JO, Hoyt WF, Daroff RB, Lawrence W. Clinical spectrum of ocular bobbing. J Neurol Neurosurg Psychiatry. 1970;33:771–5.

    CAS  Article  Google Scholar 

  4. 4.

    Goldschmidt TJ, Wall M. Slow-upward ocular bobbing. J Clin Neuroophthalmol. 1987;7:241–3.

    CAS  PubMed  Google Scholar 

  5. 5.

    Lawrence WH, Lightfoote WE. Continuous vertical pendular eye movements after brain-stem hemorrhage. Neurology. 1975;25:896–8.

    CAS  Article  Google Scholar 

  6. 6.

    Keane JR. Acute vertical ocular myoclonus. Neurology. 1986;36:86–9.

    CAS  Article  Google Scholar 

  7. 7.

    Nelson JR, Johnston CH. Ocular Bobbing. Arch Neurol. 1970;22:348–56.

    CAS  Article  Google Scholar 

  8. 8.

    Nelson JR, Johnston CH. Ocular Bobbing. Arch Neurol. 1970;22:348–56.

    CAS  Article  Google Scholar 

  9. 9.

    CASSIDY L, TAYLOR D, WERNER K, VEYS P, HARRIS C. Reverse and converse ocular bobbing with synkinetic blinking and opsoclonus in a child with Epstein-Barr virus encephalitis after bone marrow transplant for MPS I. Br J Ophthalmol. 2000;84:1203.

    Article  Google Scholar 

  10. 10.

    Karakas HM, Yakinci C, Firat AK, Kahraman B. Unilateral reverse ocular bobbing caused by tuberous sclerosis. Dev Med Child Neurol. 2006;48:851–4.

    Article  Google Scholar 

  11. 11.

    Shimazaki H, Morita M, Nakano I, Dalmau J. Inverse ocular bobbing in a patient with encephalitis associated with antibodies to the N-methyl-D-aspartate receptor. Arch Neurol. 2008;65:1251–1.

  12. 12.

    Schneider J, Rossetti AO, Alvarez V. Ocular bobbing/dipping after cardiac arrest may be a post-anoxic myoclonus. Resuscitation. 2018;124:e7.

    Article  Google Scholar 

  13. 13.

    Munakomi S, Thapa L. Seesaw-Pattern Ocular Bobbing in a Patient With Pontine Bleed. JAMA Neurol. 2019;76:362–3.

    Article  Google Scholar 

  14. 14.

    Stacy CB. Continuous vertical ocular flutter, asynchronous palatal myoclonus, and alpha coma. Neuro-Ophthalmology. 1982;2:147–56.

    Article  Google Scholar 

  15. 15.

    Ruigrok TJ, de Zeeuw CI, Voogd J. Hypertrophy of inferior olivary neurons: a degenerative, regenerative or plasticity phenomenon. Eur J Morphol. 1990;28:224–39.

    CAS  PubMed  Google Scholar 

  16. 16.

    Hong S, Leigh RJ, Zee DS, Optican LM. Inferior olive hypertrophy and cerebellar learning are both needed to explain ocular oscillations in oculopalatal tremor. Progress in Brain Research [Internet]. Elsevier; 2008 [cited 2015 Nov 25]. p. 219–26. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0079612308006316

  17. 17.

    Tilikete C, Desestret V. Hypertrophic Olivary Degeneration and Palatal or Oculopalatal Tremor. Front Neurol [Internet]. 2017 [cited 2019 Apr 27];8. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5490180/.

  18. 18.

    Llinás R, Yarom Y. Oscillatory properties of guinea-pig inferior olivary neurones and their pharmacological modulation: an in vitro study. J Physiol. 1986;376:163–82.

    Article  Google Scholar 

  19. 19.

    Long MA, Deans MR, Paul DL, Connors BW. Rhythmicity without Synchrony in the Electrically Uncoupled Inferior Olive. J Neurosci. 2002;22:10898–905.

    CAS  Article  Google Scholar 

  20. 20.

    Leigh RJ, Zee DS. The Neurology of Eye Movements [Internet]. Oxford University Press; 2015 [cited 2018 Jul 27]. Available from: http://www.oxfordmedicine.com/view/10.1093/med/9780199969289.001.0001/med-9780199969289.

  21. 21.

    Das VE, Oruganti P, Kramer PD, Leigh RJ. Experimental tests of a neural-network model for ocular oscillations caused by disease of central myelin. Exp Brain Res. 2000;133:189–97.

    CAS  Article  Google Scholar 

  22. 22.

    Tilikete C, Jasse L, Pelisson D, Vukusic S, Durand-Dubief F, Urquizar C, et al. Acquired pendular nystagmus in multiple sclerosis and oculopalatal tremor. Neurology. 2011;76:1650–7.

    CAS  Article  Google Scholar 

  23. 23.

    Itoh Y, Sakata E. Acquired pendular oscillation after brain-stem hemorrhage. Acta Otolaryngol Suppl. 1989;468:205–8.

    CAS  Article  Google Scholar 

  24. 24.

    Averbuch-Heller L, Kori AA, Rottach KG, Dell’Osso LF, Remler BF, Leigh RJ. Dysfunction of pontine omnipause neurons causes impaired fixation: macrosaccadic oscillations with a unilateral pontine lesion. Neuroophthalmology. 1996;16:99–106.

    CAS  Article  Google Scholar 

  25. 25.

    Johnston JL, Sharpe JA, Ranalli PJ, Morrow MJ. Oblique misdirection and slowing of vertical saccades after unilateral lesions of the pontine tegmentum. Neurology. 1993;43:2238–44.

    CAS  Article  Google Scholar 

  26. 26.

    Kaneko CR. Effect of ibotenic acid lesions of the omnipause neurons on saccadic eye movements in rhesus macaques. J Neurophysiol. 1996;75:2229–42.

    CAS  Article  Google Scholar 

  27. 27.

    De Zeeuw CI, Simpson JI, Hoogenraad CC, Galjart N, Koekkoek SK, Ruigrok TJ. Microcircuitry and function of the inferior olive. Trends Neurosci. 1998;21:391–400.

    Article  Google Scholar 

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Acknowledgements

We thank Dr. Aasef Shaikh for sharing the raw data of oculopalatal tremor in his previous research to us for comparison.

Data Availability Statement

All available data can be obtained by contacting the corresponding author.

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Authors

Contributions

Tzu-Pu Chang collected the data, interpreted the data, drafted the manuscript and revised the manuscript.

Daniel R. Gold interpreted the data, drafted the manuscript and revised the manuscript.

Jorge Otero-Millan analyzed and interpreted the data.

Bor-Ren Huang collected the data.

David S. Zee interpreted the data, drafted the manuscript and revised the manuscript.

Corresponding author

Correspondence to David S. Zee.

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The study was performed in accordance with the ethical standards laid down in the Declaration of Helsinki (1964).

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The informed and written consent for publication of the data and videos was obtained by the patient’s family.

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The authors declare that they have no conflict of interest.

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Chang, TP., Gold, D.R., Otero-Millan, J. et al. Pendular Oscillation and Ocular Bobbing After Pontine Hemorrhage. Cerebellum (2019). https://doi.org/10.1007/s12311-019-01086-6

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Keywords

  • Pendular oscillation
  • Ocular bobbing
  • Nystagmus
  • Pontine hemorrhage
  • Inferior olive