Skip to main content

Advertisement

SpringerLink
Log in

Impaired Saccade Adaptation in Tremor-Dominant Cervical Dystonia—Evidence for Maladaptive Cerebellum

  • Original Paper
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

We examined the role of the cerebellum in patients with tremor-dominant cervical dystonia by measuring the adaptive capacity of rapid reflexive eye movements (saccades). We chose the saccade adaptation paradigm because, unlike other motor learning paradigms, the real-time modification of saccades cannot “wait” for the sensory (visual) feedback. Instead, saccades rely primarily on the internal reafference modulated by the cerebellum. The saccade adaptation happens over fast and slow timescales. The fast timescale has poor retention of learned response, while the slow timescale has strong retention. Cerebellar defects resulting in loss of function affect the fast timescale but the slow timescale of saccade adaptation is retained. In contrast, maladaptive cerebellar disorders feature the absence of both fast and slow timescales. We were able to measure both timescales using noninvasive oculography in 6 normal individuals. In contrast, both timescales were absent in 12 patients with tremor-dominant cervical dystonia. These findings are consistent with maladaptive cerebellar outflow as a putative pathophysiological basis for tremor-dominant cervical dystonia.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Tarsy D, Simon DK. Dystonia. N Engl J Med. 2006;355:818–29.

    Article  CAS  Google Scholar 

  2. Dauer WT, Burke RE, Greene P, Fahn S. Current concepts on the clinical features, aetiology and management of idiopathic cervical dystonia. Brain. 1998;121:547–60.

    Article  Google Scholar 

  3. Berardelli A, Rothwell JC, Hallett M, Thompson PD, Manfredi M, Marsden CD. The pathophysiology of primary dystonia. Brain. 1998;121(Pt 7):1195–212.

    Article  Google Scholar 

  4. Vitek JL. Pathophysiology of dystonia: a neuronal model. Mov Disord. 2002;17(Suppl 3):S49–62.

    Article  Google Scholar 

  5. Vitek JL, Chockkan V, Zhang JY, Kaneoke Y, Evatt M, DeLong MR, et al. Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus. Ann Neurol. 1999;46:22–35.

    Article  CAS  Google Scholar 

  6. Starr PA, Rau GM, Davis V, Marks WJ Jr, Ostrem JL, Simmons D, et al. Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson’s disease and normal macaque. J Neurophysiol. 2005;93:3165–76. https://doi.org/10.1152/jn.00971.2004.

    Article  PubMed  Google Scholar 

  7. Calderon DP, Fremont R, Kraenzlin F, Khodakhah K. The neural substrates of rapid-onset dystonia-parkinsonism. Nat Neurosci. 2011;14:357–65. https://doi.org/10.1038/nn.2753.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Vitek JL, Delong MR, Starr PA, Hariz MI, Metman LV. Intraoperative neurophysiology in DBS for dystonia. Mov Disord. 2011;26(Suppl 1):S31–6. https://doi.org/10.1002/mds.23619.

    Article  PubMed  Google Scholar 

  9. Lozano AM, Kumar R, Gross RE, Giladi N, Hutchison WD, Dostrovsky JO, et al. Globus pallidus internus pallidotomy for generalized dystonia. Mov Disord. 1997;12:865–70. https://doi.org/10.1002/mds.870120606.

    Article  CAS  PubMed  Google Scholar 

  10. Lenz FA, Suarez JI, Metman LV, Reich SG, Karp BI, Hallett M, et al. Pallidal activity during dystonia: somatosensory reorganisation and changes with severity. J Neurol Neurosurg Psychiatry. 1998;65:767–70.

    Article  CAS  Google Scholar 

  11. Neychev V, Fan X, Mitev VI, Hess EJ, Jinnah HA. The basal ganglia and cerebellum interact in the expression of dystonic movement. Brain. 2008;131:2499–509.

    Article  Google Scholar 

  12. Neychev VK, Gross R, Lehericy S, Hess EJ, Jinnah HA. The functional neuroanatomy of dystonia. Neurobiol Dis. 2011;42:185–201.

    Article  Google Scholar 

  13. Pizoli CE, Jinnah HA, Billingsley ML, Hess EJ. Abnormal cerebellar signaling induces dystonia in mice. J Neurosci. 2002;22:7825–33.

    Article  CAS  Google Scholar 

  14. Prudente CN, Hess EJ, Jinnah HA. Dystonia as a network disorder: what is the role of the cerebellum? Neuroscience. 2014;260:23–35. https://doi.org/10.1016/j.neuroscience.2013.11.062.

    Article  CAS  PubMed  Google Scholar 

  15. Prudente CN, Pardo CA, Xiao J, Hanfelt J, Hess EJ, Ledoux MS, et al. Neuropathology of cervical dystonia. Exp Neurol. 2013;241:95–104. https://doi.org/10.1016/j.expneurol.2012.11.019.

    Article  CAS  PubMed  Google Scholar 

  16. Roll JP, Vedel JP. Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography. Exp Brain Res. 1982;47:177–90.

    Article  CAS  Google Scholar 

  17. Lekhel H, Popov K, Anastasopoulos D, Bronstein A, Bhatia K, Marsden CD, et al. Postural responses to vibration of neck muscles in patients with idiopathic torticollis. Brain. 1997;120(Pt 4):583–91.

    Article  Google Scholar 

  18. Hubsch C, Vidailhet M, Rivaud-Pechoux S, Pouget P, Brochard V, Degos B, et al. Impaired saccadic adaptation in DYT11 dystonia. J Neurol Neurosurg Psychiatry. 2011;82:1103–6. https://doi.org/10.1136/jnnp.2010.232793.

    Article  PubMed  Google Scholar 

  19. Katschnig-Winter P, Schwingenschuh P, Davare M, Sadnicka A, Schmidt R, Rothwell JC, et al. Motor sequence learning and motor adaptation in primary cervical dystonia. J Clin Neurosci. 2014;21:934–8. https://doi.org/10.1016/j.jocn.2013.08.019.

    Article  PubMed  Google Scholar 

  20. Sadnicka A, Patani B, Saifee TA, Kassavetis P, Parees I, Korlipara P, et al. Normal motor adaptation in cervical dystonia: a fundamental cerebellar computation is intact. Cerebellum. 2014;13:558–67. https://doi.org/10.1007/s12311-014-0569-0.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Sadnicka A, Stevenson A, Bhatia KP, Rothwell JC, Edwards MJ, Galea JM. High motor variability in DYT1 dystonia is associated with impaired visuomotor adaptation. Sci Rep. 2018;8:3653. https://doi.org/10.1038/s41598-018-21545-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. LeDoux MS, Brady KA. Secondary cervical dystonia associated with structural lesions of the central nervous system. Mov Disord. 2003;18:60–9. https://doi.org/10.1002/mds.10301.

    Article  PubMed  Google Scholar 

  23. Kumandas S, Per H, Gumus H, Tucer B, Yikilmaz A, Kontas O, et al. Torticollis secondary to posterior fossa and cervical spinal cord tumors: report of five cases and literature review. Neurosurg Rev. 2006;29:333–8; discussion 8. https://doi.org/10.1007/s10143-006-0034-8.

    Article  PubMed  Google Scholar 

  24. Cancel G, Durr A, Didierjean O, Imbert G, Burk K, Lezin A, et al. Molecular and clinical correlations in spinocerebellar ataxia 2: a study of 32 families. Hum Mol Genet. 1997;6:709–15. https://doi.org/10.1093/hmg/6.5.709.

    Article  CAS  PubMed  Google Scholar 

  25. Hagenah JM, Zuhlke C, Hellenbroich Y, Heide W, Klein C. Focal dystonia as a presenting sign of spinocerebellar ataxia 17. Mov Disord. 2004;19:217–20. https://doi.org/10.1002/mds.10600.

    Article  PubMed  Google Scholar 

  26. Lang AE, Rogaeva EA, Tsuda T, Hutterer J, St George-Hyslop P. Homozygous inheritance of the Machado-Joseph disease gene. Ann Neurol. 1994;36:443–7. https://doi.org/10.1002/ana.410360318.

    Article  CAS  PubMed  Google Scholar 

  27. Le Ber I, Clot F, Vercueil L, Camuzat A, Viemont M, Benamar N, et al. Predominant dystonia with marked cerebellar atrophy: a rare phenotype in familial dystonia. Neurology. 2006;67:1769–73. https://doi.org/10.1212/01.wnl.0000244484.60489.50.

    Article  PubMed  Google Scholar 

  28. Batla A, Sanchez MC, Erro R, Ganos C, Stamelou M, Balint B, et al. The role of cerebellum in patients with late onset cervical/segmental dystonia?--evidence from the clinic. Parkinsonism Relat Disord. 2015;21:1317–22. https://doi.org/10.1016/j.parkreldis.2015.09.013.

    Article  CAS  PubMed  Google Scholar 

  29. DeSimone JC, Archer DB, Vaillancourt DE, Wagle SA. Network-level connectivity is a critical feature distinguishing dystonic tremor and essential tremor. Brain. 2019;142:1644–59. https://doi.org/10.1093/brain/awz085.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Merola A, Dwivedi AK, Shaikh AG, Tareen TK, Da Prat GA, Kauffman MA, et al. Head tremor at disease onset: an ataxic phenotype of cervical dystonia. J Neurol. 2019;266:1844–51. https://doi.org/10.1007/s00415-019-09341-w.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Ghasia FF, Gulati D, Westbrook EL, Shaikh AG. Viewing condition dependence of the gaze-evoked nystagmus in Arnold Chiari type 1 malformation. J Neurol Sci. 2014;339:134–9. https://doi.org/10.1016/j.jns.2014.01.045.

    Article  PubMed  Google Scholar 

  32. Ghasia FF, Shaikh AG. Uncorrected myopic refractive error increases microsaccade amplitude. Invest Ophthalmol Vis Sci. 2015;56:2531–5. https://doi.org/10.1167/iovs.14-15882.

    Article  PubMed  Google Scholar 

  33. Ghasia FF, Wilmot G, Ahmed A, Shaikh AG. Strabismus and micro-opsoclonus in Machado-Joseph disease. Cerebellum. 2016;15:491–7. https://doi.org/10.1007/s12311-015-0718-0.

    Article  PubMed  Google Scholar 

  34. Shaikh AG, Ghasia FF. Novel eye movement disorders in Whipple’s disease-staircase horizontal saccades, gaze-evoked nystagmus, and esotropia. Front Neurol. 2017;8:321. https://doi.org/10.3389/fneur.2017.00321.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Shaikh AG, Ghasia FF. Fixational saccades are more disconjugate in adults than in children. PLoS One. 2017;12:e0175295. https://doi.org/10.1371/journal.pone.0175295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Shaikh AG, Ghasia FF. Misdirected horizontal saccades in pan-cerebellar atrophy. J Neurol Sci. 2015;355:125–30. https://doi.org/10.1016/j.jns.2015.05.042.

    Article  PubMed  Google Scholar 

  37. Fujita M, Amagai A, Minakawa F, Aoki M. Selective and delay adaptation of human saccades. Brain Res Cogn Brain Res. 2002;13:41–52. https://doi.org/10.1016/s0926-6410(01)00088-x.

    Article  PubMed  Google Scholar 

  38. Ethier V, Zee DS, Shadmehr R. Spontaneous recovery of motor memory during saccade adaptation. J Neurophysiol. 2008;99:2577–83. https://doi.org/10.1152/jn.00015.2008.

    Article  PubMed  Google Scholar 

  39. Catz N, Dicke PW, Thier P. Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response. Proc Natl Acad Sci U S A. 2008;105:7309–14. https://doi.org/10.1073/pnas.0706032105.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Straube A, Deubel H. Rapid gain adaptation affects the dynamics of saccadic eye movements in humans. Vis Res. 1995;35:3451–8. https://doi.org/10.1016/0042-6989(95)00076-q.

    Article  CAS  PubMed  Google Scholar 

  41. Ethier V, Zee DS, Shadmehr R. Changes in control of saccades during gain adaptation. J Neurosci. 2008;28:13929–37. https://doi.org/10.1523/JNEUROSCI.3470-08.2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Schnier F, Lappe M. Differences in intersaccadic adaptation transfer between inward and outward adaptation. J Neurophysiol. 2011;106:1399–410. https://doi.org/10.1152/jn.00236.2011.

    Article  PubMed  Google Scholar 

  43. Kommerell G, Olivier D, Theopold H. Adaptive programming of phasic and tonic components in saccadic eye movements. Investigations of patients with abducens palsy. Investig Ophthalmol. 1976;15:657–60.

    CAS  Google Scholar 

  44. 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;22:2804–15.

    Article  Google Scholar 

  45. 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;99:449–54. https://doi.org/10.1073/pnas.012604899.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Kording KP, Tenenbaum JB, Shadmehr R. The dynamics of memory as a consequence of optimal adaptation to a changing body. Nat Neurosci. 2007;10:779–86. https://doi.org/10.1038/nn1901.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Carey MR. Synaptic mechanisms of sensorimotor learning in the cerebellum. Curr Opin Neurobiol. 2011;21:609–15. https://doi.org/10.1016/j.conb.2011.06.011.

    Article  CAS  PubMed  Google Scholar 

  48. Smith MA, Ghazizadeh A, Shadmehr R. Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol. 2006;4:e179. https://doi.org/10.1371/journal.pbio.0040179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Xu-Wilson M, Chen-Harris H, Zee DS, Shadmehr R. Cerebellar contributions to adaptive control of saccades in humans. J Neurosci. 2009;29:12930–9. https://doi.org/10.1523/JNEUROSCI.3115-09.2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Barash S, Melikyan A, Sivakov A, Zhang M, Glickstein M, Thier P. Saccadic dysmetria and adaptation after lesions of the cerebellar cortex. J Neurosci. 1999;19:10931–9.

    Article  CAS  Google Scholar 

  51. Golla H, Tziridis K, Haarmeier T, Catz N, Barash S, Thier P. Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease. Eur J Neurosci. 2008;27:132–44. https://doi.org/10.1111/j.1460-9568.2007.05996.x.

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  54. Panouilleres M, Alahyane N, Urquizar C, Salemme R, Nighoghossian N, Gaymard B, et al. Effects of structural and functional cerebellar lesions on sensorimotor adaptation of saccades. Exp Brain Res. 2013;231:1–11. https://doi.org/10.1007/s00221-013-3662-6.

    Article  CAS  PubMed  Google Scholar 

  55. 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;33:1512–25. https://doi.org/10.1002/hbm.21301.

    Article  PubMed  Google Scholar 

  56. Criscimagna-Hemminger SE, Bastian AJ, Shadmehr R. Size of error affects cerebellar contributions to motor learning. J Neurophysiol. 2010;103:2275–84. https://doi.org/10.1152/jn.00822.2009.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Shaikh AG, Hong S, Liao K, Tian J, Solomon D, Zee DS, et al. Oculopalatal tremor explained by a model of inferior olivary hypertrophy and cerebellar plasticity. Brain. 2010;133:923–40. https://doi.org/10.1093/brain/awp323.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Shaikh AG, Wong AL, Optican LM, Zee DS. Impaired motor learning in a disorder of the inferior olive: is the cerebellum confused? Cerebellum. 2017;16:158–67. https://doi.org/10.1007/s12311-016-0785-x.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Andreescu CE, Milojkovic BA, Haasdijk ED, Kramer P, De Jong FH, Krust A, et al. Estradiol improves cerebellar memory formation by activating estrogen receptor beta. J Neurosci. 2007;27:10832–9. https://doi.org/10.1523/JNEUROSCI.2588-07.2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Schonewille M, Belmeguenai A, Koekkoek SK, Houtman SH, Boele HJ, van Beugen BJ, et al. Purkinje cell-specific knockout of the protein phosphatase PP2B impairs potentiation and cerebellar motor learning. Neuron. 2010;67:618–28. https://doi.org/10.1016/j.neuron.2010.07.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Schonewille M, Gao Z, Boele HJ, Veloz MF, Amerika WE, Simek AA, et al. Reevaluating the role of LTD in cerebellar motor learning. Neuron. 2011;70:43–50. https://doi.org/10.1016/j.neuron.2011.02.044.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Zoons E, Booij J, Nederveen AJ, Dijk JM, Tijssen MA. Structural, functional and molecular imaging of the brain in primary focal dystonia—a review. Neuroimage. 2011;56:1011–20. https://doi.org/10.1016/j.neuroimage.2011.02.045.

    Article  CAS  PubMed  Google Scholar 

  63. LeDoux MS, Hurst DC, Lorden JF. Single-unit activity of cerebellar nuclear cells in the awake genetically dystonic rat. Neuroscience. 1998;86:533–45. https://doi.org/10.1016/s0306-4522(98)00007-4.

    Article  CAS  PubMed  Google Scholar 

  64. LeDoux MS, Lorden JF. Abnormal spontaneous and harmaline-stimulated Purkinje cell activity in the awake genetically dystonic rat. Exp Brain Res. 2002;145:457–67. https://doi.org/10.1007/s00221-002-1127-4.

    Article  PubMed  Google Scholar 

  65. LeDoux MS, Lorden JF. Abnormal cerebellar output in the genetically dystonic rat. Adv Neurol. 1998;78:63–78.

    CAS  PubMed  Google Scholar 

  66. LeDoux MS, Lorden JF, Ervin JM. Cerebellectomy eliminates the motor syndrome of the genetically dystonic rat. Exp Neurol. 1993;120:302–10. https://doi.org/10.1006/exnr.1993.1064.

    Article  CAS  PubMed  Google Scholar 

  67. LeDoux MS, Lorden JF, Meinzen-Derr J. Selective elimination of cerebellar output in the genetically dystonic rat. Brain Res. 1995;697:91–103. https://doi.org/10.1016/0006-8993(95)00792-o.

    Article  CAS  PubMed  Google Scholar 

  68. Alvarez-Fischer D, Grundmann M, Lu L, Samans B, Fritsch B, Moller JC, et al. Prolonged generalized dystonia after chronic cerebellar application of kainic acid. Brain Res. 2012;1464:82–8. https://doi.org/10.1016/j.brainres.2012.05.007.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by American Academy of Neurology Career Award (AS), George C. Cotzias Memorial Fellowship from American Parkinson’s Disease Association (AS), and Dystonia Medical Research Foundation Brain Circuits in Dystonia Research Grant (AS), NIH U54 NS116025-09 (HJ). AM was supported by the Dystonia Medical Research Foundation Clinical Fellowship. PG was supported by the philanthropic support to the University Hospitals Cleveland Medical Center—The Alan Woll Fund.

Funding

Dr. Shaikh is a section editor of The Cerebellum and Guest Editor of The Journal of Computational Neuroscience. Dr. Shaikh has received speaker honoraria from Acorda Therapeutics and editorial honoraria from Elsevier. Dr. Shaikh has received grant support from The American Academy of Neurology, American Parkinson’s Disease Association, and Dystonia Medical Research Foundation. Dr. Espay has received grant support from the NIH, Great Lakes Neurotechnologies and the Michael J Fox Foundation; personal compensation as a consultant/scientific advisory board member for Abbvie, TEVA, Impax, Acadia, Acorda, Cynapsus/Sunovion, Lundbeck, and USWorldMeds; publishing royalties from Lippincott Williams & Wilkins, Cambridge University Press, and Springer; and honoraria from Abbvie, UCB, USWorldMeds, Lundbeck, Acadia, the American Academy of Neurology, and the Movement Disorders Society. He serves as Associate Editor of the Journal of Clinical Movement Disorders and on the editorial boards of the Journal of Parkinson’s Disease and Parkinsonism and Related Disorders. H. A. Jinnah has active or recent grant support from the US government (National Institutes of Health), private philanthropic organizations (the Benign Essential Blepharospasm Research Foundation, Cure Dystonia Now), academically oriented institutions (the Dystonia Study Group), and industry (Cavion Therapeutics, Ipsen Pharmaceuticals, Retrophin Inc.). Dr. Jinnah has also served on advisory boards or as a consultant for Abide Therapeutics, Allergan Inc., CoA Therapeutics, Medtronic Inc., Psyadon Pharmaceuticals, Retrophin Inc., and Saol Therapeutics. He has received honoraria or stipends for lectures or administrative work from the American Academy of Neurology, the American Neurological Association, the Dystonia Medical Research Foundation, the International Neurotoxin Society, the International Parkinson’s Disease and Movement Disorders Society, The Parkinson’s Disease Foundation, Tyler’s Hope for a Cure. Dr. Jinnah serves on the Scientific Advisory Boards for several private foundations including the Benign Essential Blepharospasm Research Foundation, Cure Dystonia Now, the Dystonia Medical Research Foundation, The Tourette Association of American, and Tyler’s Hope for a Cure. He also is principle investigator for the Dystonia Coalition, which has received the majority of its support through NIH grants NS065701 and NS116025 from the National Institutes of Neurological Disorders and previously from TR001456 from the Office of Rare Diseases Research at the National Center for Advancing Translational Sciences. The Dystonia Coalition has received additional material or administrative support from industry sponsors (Allergan Inc. and Merz Pharmaceuticals) as well as private foundations (The American Dystonia Society, Beat Dystonia, The Benign Essential Blepharospasm Foundation, Cure Dystonia Now, Dystonia Europe, Dystonia Inc., Dystonia Ireland, The Dystonia Medical Research Foundation, The Foundation for Dystonia Research, The National Spasmodic Dysphonia Association, and The National Spasmodic Torticollis Association).

Author information

Author notes

  1. Abhimanyu Mahajan and Palak Gupta contributed equally to this work.

Authors and Affiliations

  1. University of Cincinnati Gardner Neuroscience Institute, Cincinnati, OH, USA

    Abhimanyu Mahajan, Luca Marsili, Andrea Sturchio & Alberto J. Espay

  2. Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH, USA

    Palak Gupta & Aasef G. Shaikh

  3. Louis Stokes Cleveland VA Medical Center, University Hospitals Cleveland Medical Center, 11100 Euclid Avenue, Cleveland, OH, 44110, USA

    Jonathan Jacobs & Aasef G. Shaikh

  4. Department of Neurology, Emory University, Atlanta, GA, USA

    H.A. Jinnah

  5. Department of Neurology, Case Western Reserve University, Cleveland, OH, USA

    Aasef G. Shaikh

  6. Neurological Institute, University Hospitals Cleveland Medical Center, Cleveland, OH, USA

    Aasef G. Shaikh

Authors
  1. Abhimanyu Mahajan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Palak Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jonathan Jacobs
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luca Marsili
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrea Sturchio
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. H.A. Jinnah
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alberto J. Espay
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Aasef G. Shaikh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aasef G. Shaikh.

Ethics declarations

The University of Cincinnati Institutional review board approved the study protocol and informed consent form that followed the Declaration of Helsinki.

Conflict of Interest

The authors declare that they have no conflict of interest.

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

Mahajan, A., Gupta, P., Jacobs, J. et al. Impaired Saccade Adaptation in Tremor-Dominant Cervical Dystonia—Evidence for Maladaptive Cerebellum. Cerebellum 20, 678–686 (2021). https://doi.org/10.1007/s12311-020-01104-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-020-01104-y

Keywords

Search

Navigation