Skip to main content

Advertisement

Log in

Classics to Contemporary of Saccadic Dysmetria and Oscillations

  • Cerebellar Classic
  • Published:
The Cerebellum Aims and scope Submit manuscript

A CEREBELLAR CLASSIC to this article was published on 26 July 2022

Abstract

Clear vision requires accurate gaze shift from one object to the other and steadily maintaining it when eyes are at the target. The rapid gaze shifts are assured by the high-frequency burst in the brainstem neuronal firing, the mechanism relying on the tight cerebellar supervision. The cerebellar oversight is equally essential for maintaining gaze on the object of interest. The cerebellar significance on the motor control of gaze and the consequences of cerebellar illness are known for almost three quarters of the century – since David Cogan published the classic paper titled “Ocular Dysmetria, Flutter Like Oscillations of the Eyes, and Opsoclonus.” In this classic series of cases, three disorders of gaze shifting and gaze holding were described in a number of etiologies, ultimately manifesting in a final common pathway involving the cerebellum. Since the 1950s, there had been substantial progress in contemporary neurology, experimental neuroscience literature has expanded, and computational models of ocular motor control have flourished in the field. In this short commentary, I will highlight Cogan’s cerebellar classic in the context of contemporary research on motor control of saccades.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  1. Cogan DG. Ocular dysmetria; flutterlike oscillations of the eyes, and opsoclonus. AMA Arch Ophthalmol. 1954;51(3):318–35.

    Article  CAS  Google Scholar 

  2. Robinson DA. Editorial: How the oculomotor system repairs itself. Invest Ophthalmol. 1975;14(6):413–5.

    CAS  PubMed  Google Scholar 

  3. Kommerell G, Olivier V, Theopold H. Adaptive programming of phasic and tonic components in saccadic eye movements. Investigations of patients with abducens palsy. Invest Ophthalmol. 1976;15(8):657–60.

    CAS  PubMed  Google Scholar 

  4. Leznik E, Makarenko V, Llinas R. Electrotonically mediated oscillatory patterns in neuronal ensembles: an in vitro voltage-dependent dye-imaging study in the inferior olive. J Neurosci. 2002;22(7):2804–15.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Llinas RR, Leznik E, Urbano FJ. Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: a voltage-dependent dye-imaging study in mouse brain slices. Proc Natl Acad Sci U S A. 2002;99(1):449–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Barash S, et al. Saccadic dysmetria and adaptation after lesions of the cerebellar cortex. J Neurosci. 1999;19(24):10931–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Coesmans M, et al. Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron. 2004;44(4):691–700.

    Article  CAS  PubMed  Google Scholar 

  8. Andreescu CE, et al. Estradiol improves cerebellar memory formation by activating estrogen receptor beta. J Neurosci. 2007;27(40):10832–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Schonewille M, et al. Purkinje cell-specific knockout of the protein phosphatase PP2B impairs potentiation and cerebellar motor learning. Neuron. 2010;67(4):618–28.

    Article  CAS  PubMed Central  Google Scholar 

  10. Schonewille M, et al. Reevaluating the role of LTD in cerebellar motor learning. Neuron. 2011;70(1):43–50.

    Article  CAS  PubMed Central  Google Scholar 

  11. Marr D. A theory of cerebellar cortex. J Physiol. 1969;202(2):437–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ito M. Cerebellar control of the vestibulo-ocular reflex—around the flocculus hypothesis. Annu Rev Neurosci. 1982;5:275–96.

    Article  CAS  PubMed  Google Scholar 

  13. Zheng N, Raman IM. Synaptic inhibition, excitation, and plasticity in neurons of the cerebellar nuclei. Cerebellum. 2010;9(1):56–66.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Person AL, Raman IM. Deactivation of L-type Ca current by inhibition controls LTP at excitatory synapses in the cerebellar nuclei. Neuron. 2010;66(4):550–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Medina JF. A recipe for bidirectional motor learning: using inhibition to cook plasticity in the vestibular nuclei. Neuron. 2010;68(4):607–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. McElvain LE, et al. Bidirectional plasticity gated by hyperpolarization controls the gain of postsynaptic firing responses at central vestibular nerve synapses. Neuron. 2010;68(4):763–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Menzies JR, et al. Synaptic plasticity in medial vestibular nucleus neurons: comparison with computational requirements of VOR adaptation. PLoS One. 2010;5(10):e13182.

  18. Albus JS. A theory of cerebellar function. Math Biosci. 1971;10:25–61.

    Article  Google Scholar 

  19. Kojima Y, Soetedjo R, Fuchs AF. Changes in simple spike activity of some Purkinje cells in the oculomotor vermis during saccade adaptation are appropriate to participate in motor learning. J Neurosci. 2010;30(10):3715–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kojima Y, Soetedjo R, Fuchs AF. Effect of inactivation and disinhibition of the oculomotor vermis on saccade adaptation. Brain Res. 2011;1401:30–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Soetedjo R, Fuchs AF. Complex spike activity of purkinje cells in the oculomotor vermis during behavioral adaptation of monkey saccades. J Neurosci. 2006;26(29):7741–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ito M. Error detection and representation in the olivo-cerebellar system. Front Neural Circuits. 2013;7:1.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Kording KP, Tenenbaum JB, Shadmehr R. The dynamics of memory as a consequence of optimal adaptation to a changing body. Nat Neurosci. 2007;10(6):779–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Carey MR. Synaptic mechanisms of sensorimotor learning in the cerebellum. Curr Opin Neurobiol. 2011;21(4):609–15.

    Article  CAS  PubMed  Google Scholar 

  25. Smith MA, Ghazizadeh A, Shadmehr R. Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol. 2006;4(6): e179.

    Article  PubMed  Google Scholar 

  26. Xu-Wilson M, et al. Cerebellar contributions to adaptive control of saccades in humans. J Neurosci. 2009;29(41):12930–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Golla H, et al. Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease. Eur J Neurosci. 2008;27(1):132–44.

    Article  PubMed  Google Scholar 

  28. Takagi M, Zee DS, Tamargo RJ. Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: smooth pursuit. J Neurophysiol. 2000;83(4):2047–62.

    Article  CAS  PubMed  Google Scholar 

  29. Takagi M, Zee DS, Tamargo RJ. Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J Neurophysiol. 1998;80(4):1911–31.

    Article  CAS  PubMed  Google Scholar 

  30. Panouilleres M, et al. Transcranial magnetic stimulation and motor plasticity in human lateral cerebellum: dual effect on saccadic adaptation. Hum Brain Mapp. 2012;33(7):1512–25.

    Article  PubMed  Google Scholar 

  31. Panouilleres M, et al. Effects of structural and functional cerebellar lesions on sensorimotor adaptation of saccades. Exp Brain Res. 2013;231:1–11.

    Article  CAS  PubMed  Google Scholar 

  32. Criscimagna-Hemminger SE, Bastian AJ, Shadmehr R. Size of error affects cerebellar contributions to motor learning. J Neurophysiol. 2010;103(4):2275–84.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Shaikh AG, et al. Impaired motor learning in a disorder of the inferior olive: is the cerebellum confused? Cerebellum. 2017;16(1):158–67.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Mahajan A, et al. Impaired saccade adaptation in tremor-dominant cervical dystonia-evidence for maladaptive cerebellum. Cerebellum. 2021;20(5):678–86.

    Article  PubMed  Google Scholar 

  35. Shaikh AG, et al. Saccadic burst cell membrane dysfunction is responsible for saccadic oscillations. J Neuroophthalmol. 2008;28(4):329–36.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ghasia FF, et al. Strabismus and micro-opsoclonus in Machado-Joseph disease. Cerebellum. 2016;15(4):491–7.

    Article  PubMed  Google Scholar 

  37. Shaikh AG, et al. Gaze fixation deficits and their implication in ataxia-telangiectasia. J Neurol Neurosurg Psychiatry. 2009;80(8):858–64.

    Article  CAS  PubMed  Google Scholar 

  38. Shaikh AG, Wilmot G. Opsoclonus in a patient with increased titers of anti-GAD antibody provides proof for the conductance-based model of saccadic oscillations. J Neurol Sci. 2016;362:169–73.

    Article  PubMed  Google Scholar 

  39. Theeranaew W, et al. Gaze-holding and anti-GAD antibody: prototypic heterogeneous motor dysfunction in immune disease. Cerebellum. 2022;21(1):55–63.

    Article  CAS  PubMed  Google Scholar 

  40. Shaikh AG, et al. A new familial disease of saccadic oscillations and limb tremor provides clues to mechanisms of common tremor disorders. Brain. 2007;130(Pt 11):3020–31.

    Article  PubMed  Google Scholar 

  41. Shaikh AG, et al. Sustained eye closure slows saccades. Vision Res. 2010;50(17):1665–75.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Shaikh AG, et al. The effects of ion channel blockers validate the conductance-based model of saccadic oscillations. Ann N Y Acad Sci. 2011;1233:58–63.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aasef G. Shaikh.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shaikh, A.G. Classics to Contemporary of Saccadic Dysmetria and Oscillations. Cerebellum 22, 527–530 (2023). https://doi.org/10.1007/s12311-022-01443-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-022-01443-y

Navigation