Experimental Brain Research

, Volume 230, Issue 3, pp 311–321 | Cite as

Proprioceptive sensitivity in Ehlers–Danlos syndrome patients

  • Holly A. Clayton
  • Erin K. Cressman
  • Denise Y. P. Henriques
Research Article

Abstract

Reaching movements are rapidly adapted following training with rotated visual feedback of the hand. Our laboratory has also found that this visuomotor adaptation results in changes in estimates of felt hand position (proprioceptive recalibration) in the direction of the visuomotor distortion (Cressman and Henriques in J Neurophysiol 102:3505–3518, 2009; Cressman et al. in Exp Brain Res 205:533–544, 2010). In the current study, we investigated proprioceptive acuity and proprioceptive recalibration in a group of individuals with Ehlers–Danlos syndrome (EDS), a degenerative condition associated with collagen malformation. Some studies have suggested that these patients may have proprioceptive impairments, but the exact nature of the impairment is unclear (Rombaut et al. in Clin Rheumatol 29:289–295, 2010a). In this study, we measured the ability of EDS patients to estimate their felt hand position and tested whether these estimates changed following visuomotor adaptation. We found EDS patients were less precise in estimating their felt hand position in the peripheral workspace compared to healthy controls. Despite this poorer sensitivity, they recalibrated hand proprioception to the same extent as healthy controls. This is consistent with other populations who experience proprioceptive deficits (e.g. the elderly, Parkinson’s disease patients), suggesting that sensory noise does not influence the extent of either motor or sensory plasticity.

Keywords

Proprioception Ehlers–Danlos syndrome Generalized joint hypermobility Reaches Multisensory integration 

Notes

Acknowledgments

Special thanks to each of the patients who participated in this study, as well as the Ehlers–Danlos Syndrome Ontario Support Group for promoting awareness of this project. This work has been funded by an NSERC Discovery Grant to DYPH.

References

  1. Anguera JA, Reuter-Lorenz PA, Willingham DT, Seidler RD (2011) Failure to engage spatial working memory contributes to age-related declines in visuomotor learning. J Cogn Neurosci 23:11–25PubMedCrossRefGoogle Scholar
  2. Beighton P, de Paepe A, Danks D, Finidori G, Gedde-Dahl T, Goodman R, Hall JG, Hollister DW, Horton W, McKusick VA (1988) International nosology of heritable disorders of connective tissue, Berlin, 1986. Am J Med Genet 29:581–594PubMedCrossRefGoogle Scholar
  3. Beighton P, De Paepe A, Hall JG, Hollister DW, Pope FM, Pyeritz RE, Steinmann B, Tsipouras P (1992) Molecular nosology of heritable disorders of connective tissue. Am J Med Genet 42:431–448PubMedCrossRefGoogle Scholar
  4. Beighton P, De Paepe A, Steinmann B, Tsipouras P, Wenstrup RJ (1997) Ehlers–Danlos syndromes: revised nosology, Villefranche, 1997. Ehlers–Danlos National Foundation (USA) and Ehlers–Danlos Support Group (UK). Am J Med Genet 77:31–37Google Scholar
  5. Bernier PM, Chua R, Bard C, Franks IM (2006) Updating of an internal model without proprioception: a deafferentation study. Neuroreport 17:1421–1425PubMedCrossRefGoogle Scholar
  6. Bock O (2005) Components of sensorimotor adaptation in young and elderly subjects. Exp Brain Res 160:259–263PubMedCrossRefGoogle Scholar
  7. Bock O, Girgenrath M (2006) Relationship between sensorimotor adaptation and cognitive functions in younger and older subjects. Exp Brain Res 169:400–406PubMedCrossRefGoogle Scholar
  8. Buch ER, Young S, Contreras-Vidal JL (2003) Visuomotor adaptation in normal aging. Learn Mem 10:55–63PubMedCrossRefGoogle Scholar
  9. Castori M (2012) Ehlers-danlos syndrome, hypermobility type: an underdiagnosed hereditary connective tissue disorder with mucocutaneous, articular, and systemic manifestations. ISRN Derm 2012:1–22CrossRefGoogle Scholar
  10. Celletti C, Castori M, Galli M, Rigoldi C, Grammatico P, Albertini G, Camerota F (2011) Evaluation of balance and improvement of proprioception by repetitive muscle vibration in a 15-year-old girl with joint hypermobility syndrome. Arthritis Care Res (Hoboken) 63:775–779CrossRefGoogle Scholar
  11. Cressman EK, Henriques DYP (2009) Sensory recalibration of hand position following visuomotor adaptation. J Neurophysiol 102:3505–3518PubMedCrossRefGoogle Scholar
  12. Cressman EK, Salomonczyk D, Henriques DYP (2010) Visuomotor adaptation and proprioceptive recalibration in older adults. Exp Brain Res 205:533–544PubMedCrossRefGoogle Scholar
  13. De Paepe A, Malfait F (2004) Bleeding and bruising in patients with Ehlers–Danlos syndrome and other collagen vascular disorders. Br J Haematol 127:491–500PubMedCrossRefGoogle Scholar
  14. Fatoye F, Palmer S, Macmillan F, Rowe P, van der Linden M (2009) Proprioception and muscle torque deficits in children with hypermobility syndrome. Rheumatology (Oxford) 48:152–157CrossRefGoogle Scholar
  15. Goble DJ, Coxon JP, Wenderoth N, Van Impe A, Swinnen SP (2009) Proprioceptive sensibility in the elderly: degeneration, functional consequences and plastic-adaptive processes. Neurosci Biobehav Rev 33:271–278PubMedCrossRefGoogle Scholar
  16. Hall MG, Ferrell WR, Sturrock RD, Hamblen DL, Baxendale RH (1995) The effect of the hypermobility syndrome on knee joint proprioception. Br J Rheumatol 34:121–125PubMedCrossRefGoogle Scholar
  17. Henriques DY, Soechting JF (2003) Bias and sensitivity in the haptic perception of geometry. Exp Brain Res 150:95–108PubMedGoogle Scholar
  18. Hollister DW (1978) Heritable disorders of connective tissue: Ehlers–Danlos syndrome. Pediatr Clin North Am 25:575–591PubMedGoogle Scholar
  19. Ingram HA, van Donkelaar P, Cole J, Vercher JL, Gauthier GM, Miall RC (2000) The role of proprioception and attention in a visuomotor adaptation task. Exp Brain Res 132:114–126PubMedCrossRefGoogle Scholar
  20. Izawa J, Criscimagna-Hemminger SE, Shadmehr R (2012) Cerebellar contributions to reach adaptation and learning sensory consequences of action. J Neurosci 32:4230–4239PubMedCrossRefGoogle Scholar
  21. Jeremiah HM, Alexander CM (2010) Do hypermobile subjects without pain have alteration to the feedback mechanisms controlling the shoulder girdle? Musculoskelet Care 8:157–163CrossRefGoogle Scholar
  22. Keer R, Grahame R (2003) Hypermobility syndrome: recognition and management for physiotherapists. Butterworth-Heinemann, New YorkGoogle Scholar
  23. Kesten H (1958) Accelerated stochastic approximation. Ann Math Stat 29:41–59CrossRefGoogle Scholar
  24. Lawrence EJ (2005) The clinical presentation of Ehlers–Danlos syndrome. Adv Neonatal Care 5:301–314PubMedCrossRefGoogle Scholar
  25. Malfait F, Wenstrup RJ, De Paepe A (2010) Clinical and genetic aspects of Ehlers–Danlos syndrome, classic type. Genet Med 12:597–605PubMedCrossRefGoogle Scholar
  26. Parapia LA, Jackson C (2008) Ehlers–Danlos syndrome—a historical review. Br J Haematol 141:32–35PubMedCrossRefGoogle Scholar
  27. Rombaut L, De Paepe A, Malfait F, Cools A, Calders P (2010a) Joint position sense and vibratory perception sense in patients with Ehlers–Danlos syndrome type III (hypermobility type). Clin Rheumatol 29:289–295PubMedCrossRefGoogle Scholar
  28. Rombaut L, Malfait F, Cools A, De Paepe A, Calders P (2010b) Musculoskeletal complaints, physical activity and health-related quality of life among patients with the Ehlers–Danlos syndrome hypermobility type. Disabil Rehabil 32:1339–1345PubMedCrossRefGoogle Scholar
  29. Sacheti A, Szemere J, Bernstein B, Tafas T, Schechter N, Tsipouras P (1997) Chronic pain is a manifestation of the Ehlers–Danlos syndrome. J Pain Symptom Manag 14:88–93CrossRefGoogle Scholar
  30. Sahin N, Baskent A, Cakmak A, Salli A, Ugurlu H, Berker E (2008) Evaluation of knee proprioception and effects of proprioception exercise in patients with benign joint hypermobility syndrome. Rheumatol Int 28:995–1000PubMedCrossRefGoogle Scholar
  31. Salomonczyk D, Cressman EK, Henriques DY (2011) Proprioceptive recalibration following prolonged training and increasing distortions in visuomotor adaptation. Neuropsychologia 49:3053–3062PubMedCrossRefGoogle Scholar
  32. Seidler RD (2006) Differential effects of age on sequence learning and sensorimotor adaptation. Brain Res Bull 70:337–346PubMedCrossRefGoogle Scholar
  33. Synofzik M, Lindner A, Thier P (2008) The cerebellum updates predictions about the visual consequences of one’s behavior. Curr Biol 18:814–818PubMedCrossRefGoogle Scholar
  34. Tinkle BT, Bird HA, Grahame R, Lavallee M, Levy HP, Sillence D (2009) The lack of clinical distinction between the hypermobility type of Ehlers–Danlos syndrome and the joint hypermobility syndrome (a.k.a. hypermobility syndrome). Am J Med Genet A 149A:2368–2370PubMedCrossRefGoogle Scholar
  35. Treutwein B (1995) Adaptive psychophysical procedures. Vision Res 35:2503–2522PubMedGoogle Scholar
  36. Voermans NC, Knoop H (2011) Both pain and fatigue are important possible determinants of disability in patients with the Ehlers–Danlos syndrome hypermobility type. Disabil Rehabil 33:706–707PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Holly A. Clayton
    • 1
    • 2
  • Erin K. Cressman
    • 3
  • Denise Y. P. Henriques
    • 1
    • 2
    • 4
  1. 1.Centre for Vision ResearchYork UniversityTorontoCanada
  2. 2.Department of PsychologyYork UniversityTorontoCanada
  3. 3.School of Human KineticsUniversity of OttawaOttawaCanada
  4. 4.School of Kinesiology and Health ScienceYork UniversityTorontoCanada

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