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After Effects of Cerebellar Continuous Theta Burst Stimulation on Reflexive Saccades and Smooth Pursuit in Humans

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Abstract

The use of cerebellar repetitive transcranial magnetic stimulation has been attempted for perturbing reflexive and voluntary eye movements, but discrepancies are seen between the results of distinct studies possibly due to the different stimulation sites, intensities, and paradigms. We describe the after effects of 20 and 40 s continuous Theta Burst Stimulation (cTBS) as compared to sham stimulation, applied over the lateral cerebellar vermis and paravermis on Reflexive Saccades (RS) and Smooth Pursuit (SP) eye movements, recorded in the 30 min following stimulation. The experiments were carried out in eight healthy volunteers, and eye movements were recorded monocularly with video-oculography. The 40 s cTBS significantly increased the amplitude of ipsilateral RS and the acceleration of the ipsilateral SP, and this effect was detectable all over the 30-min recording period; 40 s cTBS did not modify the other parameters, namely the peak velocity, the duration and the latency of RS, and the latency and the velocity of SP. The 20 s cTBS was ineffective on all RS and SP parameters. Finally, we detected a significant quite-linear reduction of RS peak velocity over time, but this was independent from cTBS and was probably caused by fatigue. The effects of 40 s cTBS in our experiments mimic the disorder of ocular motility in Wallenberg’s syndrome and could result from functional impairment of cerebellopontine pathways. This effect lasts 30 min at least, and can provide a useful framework for adaptive ocular motor studies.

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References

  1. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;45(2):201–6.

    Article  CAS  PubMed  Google Scholar 

  2. Huang YZ, Rothwell JC, Chen RS, Lu CS, Chuang WL. The theoretical model of theta burst form of repetitive transcranial magnetic stimulation. Clin Neurophysiol. 2011;122(5):1011–8.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Koch G. Repetitive transcranial magnetic stimulation: a tool for human cerebellar plasticity. Funct Neurol. 2010;25(3):159–63.

    PubMed  Google Scholar 

  4. Koch G, Mori F, Marconi B, Codeca C, Pecchioli C, Salerno S, et al. Changes in intracortical circuits of the human motor cortex following theta burst stimulation of the lateral cerebellum. Clin Neurophysiol. 2008;119(11):2559–69.

    Article  PubMed  Google Scholar 

  5. Popa T, Russo M, Meunier S. Long-lasting inhibition of cerebellar output. Brain Stimul. 2010;3(3):161–9.

    Article  CAS  PubMed  Google Scholar 

  6. Brusa L, Ponzo V, Mastropasqua C, Picazio S, Bonni S, Di Lorenzo F, et al. Theta burst stimulation modulates cerebellar-cortical connectivity in patients with progressive supranuclear palsy. Brain Stimul. 2014;7(1):29–35.

    Article  PubMed  Google Scholar 

  7. Colnaghi S, Honeine JL, Sozzi S, Schieppati M. Body Sway Increases After Functional Inactivation of the Cerebellar Vermis by cTBS. Cerebellum. 2016.

  8. Di Lorenzo F, Martorana A, Ponzo V, Bonni S, D'Angelo E, Caltagirone C, et al. Cerebellar theta burst stimulation modulates short latency afferent inhibition in Alzheimer’s disease patients. Front Aging Neurosci. 2013;5:2.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Monaco J, Casellato C, Koch G, D'Angelo E. Cerebellar theta burst stimulation dissociates memory components in eyeblink classical conditioning. Eur J Neurosci. 2014;40(9):3363–70.

    Article  CAS  PubMed  Google Scholar 

  10. Colnaghi S, Ramat S, D'Angelo E, Cortese A, Beltrami G, Moglia A, et al. Theta-burst stimulation of the cerebellum interferes with internal representations of sensory-motor information related to eye movements in humans. Cerebellum. 2011;10(4):711–9.

    Article  PubMed  Google Scholar 

  11. Jenkinson N, Miall RC. Disruption of saccadic adaptation with repetitive transcranial magnetic stimulation of the posterior cerebellum in humans. Cerebellum. 2010;9(4):548–55.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Panouilleres M, Neggers SF, Gutteling TP, Salemme R, van der Stigchel S, van der Geest JN, 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 

  13. Colnaghi S, Ramat S, D'Angelo E, Versino M. Transcranial magnetic stimulation over the cerebellum and eye movements: state of the art. Funct Neurol. 2010;25(3):165–71.

    PubMed  Google Scholar 

  14. Hashimoto M, Ohtsuka K. Transcranial magnetic stimulation over the posterior cerebellum during visually guided saccades in man. Brain. 1995;118(Pt 5):1185–93.

    Article  PubMed  Google Scholar 

  15. Ohtsuka K, Enoki T. Transcranial magnetic stimulation over the posterior cerebellum during smooth pursuit eye movements in man. Brain. 1998;121(Pt 3):429–35.

    Article  PubMed  Google Scholar 

  16. Nagel M, Behrmann H, Zangemeister WH. Disturbance of predictive response initiation of eye and head movements in cerebellar patients. Eur Neurol. 2008;60(4):179–85.

    Article  CAS  PubMed  Google Scholar 

  17. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol. 1994;91(2):79–92.

    Article  CAS  PubMed  Google Scholar 

  18. Rothwell JC. Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods. 1997;74(2):113–22.

    Article  CAS  PubMed  Google Scholar 

  19. Tofts PS. The distribution of induced currents in magnetic stimulation of the nervous system. Phys Med Biol. 1990;35(8):1119–28.

    Article  CAS  PubMed  Google Scholar 

  20. Leigh RJ, Zee DS. The neurology of eye movements. Fifth ed. New York: Oxford University Press; 2015.

    Google Scholar 

  21. Ohtsuka K, Noda H. Saccadic burst neurons in the oculomotor region of the fastigial nucleus of macaque monkeys. J Neurophysiol. 1991;65(6):1422–34.

    CAS  PubMed  Google Scholar 

  22. Robinson FR, Straube A, Fuchs AF. Role of the caudal fastigial nucleus in saccade generation. II. Effects of muscimol inactivation. J Neurophysiol. 1993;70(5):1741–58.

    CAS  PubMed  Google Scholar 

  23. Helmchen C, Straube A, Buttner U. Saccadic lateropulsion in Wallenberg’s syndrome may be caused by a functional lesion of the fastigial nucleus. J Neurol. 1994;241(7):421–6.

    Article  CAS  PubMed  Google Scholar 

  24. Kojima Y, Robinson FR, Soetedjo R. Cerebellar fastigial nucleus influence on ipsilateral abducens activity during saccades. J Neurophysiol. 2014;111(8):1553–63.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Eggert T, Robinson FR, Straube A. Modeling inter-trial variability of saccade trajectories: effects of lesions of the oculomotor part of the fastigial nucleus. PLoS Comput Biol. 2016;12(6):e1004866.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Fuchs AF, Robinson FR, Straube A. Participation of the caudal fastigial nucleus in smooth-pursuit eye movements. I Neuronal activity J Neurophysiol. 1994;72(6):2714–28.

    CAS  PubMed  Google Scholar 

  27. Vahedi K, Rivaud S, Amarenco P, Pierrot-Deseilligny C. Horizontal eye movement disorders after posterior vermis infarctions. J Neurol Neurosurg Psychiatry. 1995;58(1):91–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Waespe W, Wichmann W. Oculomotor disturbances during visual-vestibular interaction in Wallenberg's lateral medullary syndrome. Brain. 1990;113(Pt 3):821–46.

    Article  PubMed  Google Scholar 

  29. Gamboa OL, Antal A, Moliadze V, Paulus W. Simply longer is not better: reversal of theta burst aftereffect with prolonged stimulation. Exp Brain Res. 2010;204(2):181–7.

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to Silvia Colnaghi.

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Colnaghi, S., Colagiorgio, P., Ramat, S. et al. After Effects of Cerebellar Continuous Theta Burst Stimulation on Reflexive Saccades and Smooth Pursuit in Humans. Cerebellum 16, 764–771 (2017). https://doi.org/10.1007/s12311-017-0852-y

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