Abstract
The aim was to investigate the relative importance of cervical proprioception compared to vestibular input for head movements on trunk. Subjects with bilateral vestibulopathy (n = 11) were compared to healthy controls (n = 15). We studied their ability to move the head accurately to reproduce four specified target positions in the horizontal yaw plane (neutral head position, 10° target, 30° target, and 30° target with oscillating movements applied during target introduction). Repositioning ability was calculated as accuracy (constant error, the mean of signed differences between introduced and reproduced target) and precision (variable error, the standard deviation of differences between introduced and reproduced targets). Subjects with bilateral vestibulopathy did not differ significantly from controls in their ability to reproduce different target positions. When the 30° target position was introduced with oscillating movements, overshoot diminished and accuracy improved in both groups, although only statistically significantly when performed towards the right side. The results suggest that at least in some conditions, accurate head on trunk orientation can be achieved without vestibular information and that cervical somato-sensory input is either up-regulated as a compensatory mechanism after bilateral vestibular loss or is important for such tasks.
Similar content being viewed by others
References
Allum JH, Oude Nijhuis LB, Carpenter MG (2008) Differences in coding provided by proprioceptive and vestibular sensory signals may contribute to lateral instability in vestibular loss subjects. Exp Brain Res 184:391–410. doi:10.1007/s00221-007-1112-z
Angelaki DE, Cullen KE (2008) Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31:125–150. doi:10.1146/annurev.neuro.31.060407.125555
Brandt T (1996) Bilateral vestibulopathy revisited. Eur J Med Res 1:361–368
Brandt T, Bronstein AM (2001) Cervical vertigo. J Neurol Neurosurg Psychiatry 71:8–12. doi:10.1136/jnnp.71.1.8
Buchanan JJ, Horak FB (2001) Vestibular loss disrupts control of head and trunk on a sinusoidally moving platform. J Vestib Res 11:371–389
Colebatch JG, Halmagyi GM, Skuse NF (1994) Myogenic potentials generated by a click-evoked vestibulocollic reflex. J Neurol Neurosurg Psychiatry 57:190–197. doi:10.1136/jnnp.57.2.190
Curthoys IS (2000) Vestibular compensation and substitution. Curr Opin Neurol 13:27–30. doi:10.1097/00019052-200002000-00006
Curthoys IS, Halmagyi GM (1995) Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss. J Vestib Res 5:67–107. doi:10.1016/0957-4271(94)00026-X
Demaille-Wlodyka S, Chiquet C, Lavaste JF, Skalli W, Revel M, Poiraudeau S (2007) Cervical range of motion and cephalic kinesthesis: ultrasonographic analysis by age and sex. Spine 32:E254–E261. doi:10.1097/01.brs.0000259919.82461.57
Dvir Z, Prushansky T (2000) Reproducibility and instrument validity of a new ultrasonography-based system for measuring cervical spine kinematics. Clin Biomech (Bristol, Avon) 15:658–664. doi:10.1016/S0268-0033(00)00033-4
Earhart GM, Sibley KM, Horak FB (2004) Effects of bilateral vestibular loss on podokinetic after-rotation. Exp Brain Res 155:251–256. doi:10.1007/s00221-003-1816-7
Fransson PA, Karlberg M, Sterner T, Magnusson M (2000) Direction of galvanically-induced vestibulo-postural responses during active and passive neck torsion. Acta Otolaryngol 120:500–503. doi:10.1080/000164800750045992
Halmagyi GM, Curthoys IS (1988) A clinical sign of canal paresis. Arch Neurol 45:737–739
Heikkila HV, Wenngren BI (1998) Cervicocephalic kinesthetic sensibility, active range of cervical motion, and oculomotor function in patients with whiplash injury. Arch Phys Med Rehabil 79:1089–1094. doi:10.1016/S0003-9993(98)90176-9
Heikkila H, Johansson M, Wenngren BI (2000) Effects of acupuncture, cervical manipulation and NSAID therapy on dizziness and impaired head repositioning of suspected cervical origin: a pilot study. Man Ther 5:151–157. doi:10.1054/math.2000.0357
Hill R, Jensen P, Baardsen T, Kulvik K, Jull G, Treleaven J (2009) Head repositioning accuracy to neutral: a comparative study of error calculation. Man Ther 14:110–114. doi:10.1016/j.math.2008.02.008
Karlberg M, Magnusson M (1998) Head movement restriction and postural stability in patients with compensated unilateral vestibular loss. Arch Phys Med Rehabil 79:1448–1450. doi:10.1016/S0003-9993(98)90242-8
Karlberg M, Magnusson M, Malmstrom EM, Melander A, Moritz U (1996) Postural and symptomatic improvement after physiotherapy in patients with dizziness of suspected cervical origin. Arch Phys Med Rehabil 77:874–882. doi:10.1016/S0003-9993(96)90273-7
Kohl RL (1983) Sensory conflict theory of space motion sickness: an anatomical location for the neuroconflict. Aviat Space Environ Med 54:464–465
Kristjansson E, Dall’Alba P, Jull G (2003) A study of five cervicocephalic relocation tests in three different subject groups. Clin Rehabil 17:768–774. doi:10.1191/0269215503cr676oa
Lackner JR, DiZio P (2005) Vestibular, proprioceptive, and haptic contributions to spatial orientation. Annu Rev Psychol 56:115–147. doi:10.1146/annurev.psych.55.090902.142023
Lacour M, Barthelemy J, Borel L, Magnan J, Xerri C, Chays A, Ouaknine M (1997) Sensory strategies in human postural control before and after unilateral vestibular neurotomy. Exp Brain Res 115:300–310. doi:10.1007/PL00005698
Lee HY, Teng CC, Chai HM, Wang SF (2006) Test-retest reliability of cervicocephalic kinesthetic sensibility in three cardinal planes. Man Ther 11:61–68. doi:10.1016/j.math.2005.03.008
Lee HY, Wang JD, Yao G, Wang SF (2008) Association between cervicocephalic kinesthetic sensibility and frequency of subclinical neck pain. Man Ther 13:419–425. doi:10.1016/j.math.2007.04.001
Loudon JK, Ruhl M, Field E (1997) Ability to reproduce head position after whiplash injury. Spine 22:865–868. doi:10.1097/00007632-199704150-00008
Malmstrom EM, Karlberg M, Melander A, Magnusson M (2003) Zebris versus myrin: a comparative study between a three-dimensional ultrasound movement analysis and an inclinometer/compass method: intradevice reliability, concurrent validity, intertester comparison, intratester reliability, and intraindividual variability. Spine 28:E433–E440. doi:10.1097/01.BRS.0000090840.45802.D4
Malmstrom EM, Karlberg M, Fransson PA, Melander A, Magnusson M (2006) Primary and coupled cervical movements: the effect of age, gender, and body mass index. A 3-dimensional movement analysis of a population without symptoms of neck disorders. Spine 31:E44–E50. doi:10.1097/01.brs.0000194841.83419.0b
Malmstrom EM, Karlberg M, Melander A, Magnusson M, Moritz U (2007) Cervicogenic dizziness—musculoskeletal findings before and after treatment and long-term outcome. Disabil Rehabil 29:1193–1205. doi:10.1080/09638280600948383
Mergner T, Huber W, Becker W (1997) Vestibular-neck interaction and transformation of sensory coordinates. J Vestib Res 7:347–367. doi:10.1016/S0957-4271(96)00176-0
Mergner T, Nasios G, Maurer C, Becker W (2001) Visual object localisation in space. Interaction of retinal, eye position, vestibular and neck proprioceptive information. Exp Brain Res 141:33–51. doi:10.1007/s002210100826
Nakamura T, Bronstein AM (1995) The perception of head and neck angular displacement in normal and labyrinthine-defective subjects. A quantitative study using a ‘remembered saccade’ technique. Brain 118(Pt 5):1157–1168. doi:10.1093/brain/118.5.1157
Owens EF Jr, Henderson CN, Gudavalli MR, Pickar JG (2006) Head repositioning errors in normal student volunteers: a possible tool to assess the neck’s neuromuscular system. Chiropr Osteopat 14:5. doi:10.1186/1746-1340-14-5
Palmgren PJ, Sandstrom PJ, Lundqvist FJ, Heikkila H (2006) Improvement after chiropractic care in cervicocephalic kinesthetic sensibility and subjective pain intensity in patients with nontraumatic chronic neck pain. J Manipul Physiol Ther 29:100–106. doi:10.1016/j.jmpt.2005.12.002
Panjabi MM (1992) The stabilizing system of the spine. Part I. Function, dysfunction, adaptation, and enhancement. J Spinal Disord 5:383–389. doi:10.1097/00002517-199212000-00001 (discussion 397)
Peterka RJ, Loughlin PJ (2004) Dynamic regulation of sensorimotor integration in human postural control. J Neurophysiol 91:410–423. doi:10.1152/jn.00516.2003
Pinsault N, Fleury A, Virone G, Bouvier B, Vaillant J, Vuillerme N (2008a) Test-retest reliability of cervicocephalic relocation test to neutral head position. Physiother Theory Pract 24:380–391. doi:10.1080/09593980701884824
Pinsault N, Vuillerme N, Pavan P (2008b) Cervicocephalic relocation test to the neutral head position: assessment in bilateral labyrinthine-defective and chronic, nontraumatic neck pain patients. Arch Phys Med Rehabil 89:2375–2378. doi:10.1016/j.apmr.2008.06.009
Revel M, Andre-Deshays C, Minguet M (1991) Cervicocephalic kinesthetic sensibility in patients with cervical pain. Arch Phys Med Rehabil 72:288–291
Revel M, Minguet M, Gregoy P, Vaillant J, Manuel JL (1994) Changes in cervicocephalic kinesthesia after a proprioceptive rehabilitation program in patients with neck pain: a randomized controlled study. Arch Phys Med Rehabil 75:895–899. doi:10.1016/0003-9993(94)90115-5
Richmond FJ, Bakker DA (1982) Anatomical organization and sensory receptor content of soft tissues surrounding upper cervical vertebrae in the cat. J Neurophysiol 48:49–61
Richmond FJ, Singh K, Corneil BD (1999) Marked non-uniformity of fiber-type composition in the primate suboccipital muscle obliquus capitis inferior. Exp Brain Res 125:14–18. doi:10.1007/s002210050652
Schweigart G, Chien RD, Mergner T (2002) Neck proprioception compensates for age-related deterioration of vestibular self-motion perception. Exp Brain Res 147:89–97. doi:10.1007/s00221-002-1218-2
Swait G, Rushton AB, Miall RC, Newell D (2007) Evaluation of cervical proprioceptive function: optimizing protocols and comparison between tests in normal subjects. Spine 32:E692–E701. doi:10.1097/BRS.0b013e31815a5a1b
Teng CC, Chai H, Lai DM, Wang SF (2007) Cervicocephalic kinesthetic sensibility in young and middle-aged adults with or without a history of mild neck pain. Man Ther 12:22–28. doi:10.1016/j.math.2006.02.003
Treleaven J, LowChoy N, Darnell R, Panizza B, Brown-Rothwell D, Jull G (2008) Comparison of sensorimotor disturbance between subjects with persistent whiplash-associated disorder and subjects with vestibular pathology associated with acoustic neuroma. Arch Phys Med Rehabil 89:522–530. doi:10.1016/j.apmr.2007.11.002
Vuillerme N, Pinsault N, Bouvier B (2008) Cervical joint position sense is impaired in older adults. Aging Clin Exp Res 20:355–358
Weber KD, Fletcher WA, Melvill Jones G, Block EW (2002) Podokinetic after-rotation in patients with compensated unilateral vestibular ablation. Exp Brain Res 147:554–557. doi:10.1007/s00221-002-1279-2
Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science 269:1880–1882. doi:10.1126/science.7569931
Wyke B (1979) Neurology of the cervical spinal joints. Physiotherapy 65:72–76
Yagi T, Yajima H, Sakuma A, Aihara Y (2000) Influence of vibration to the neck, trunk and lower extremity muscles on equilibrium in normal subjects and patients with unilateral labyrinthine dysfunction. Acta Otolaryngol 120:182–186. doi:10.1080/000164800750000874
Zingler VC, Cnyrim C, Jahn K, Weintz E, Fernbacher J, Frenzel C, Brandt T, Strupp M (2007) Causative factors and epidemiology of bilateral vestibulopathy in 255 patients. Ann Neurol 61:524–532. doi:10.1002/ana.21105
Zingler VC, Weintz E, Jahn K, Mike A, Huppert D, Rettinger N, Brandt T, Strupp M (2008) Follow-up of vestibular function in bilateral vestibulopathy. J Neurol Neurosurg Psychiatry 79:284–288. doi:10.1136/jnnp.2007.122952
Acknowledgments
Financial support was received from the Skane County Council’s Research and Development Foundation, the Swedish Research Council, Stockholm, the Crafoord Foundation, Lund and the Faculty of Medicine, Lund University, Lund, Sweden.
Conflict of interest statement
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Malmström, EM., Karlberg, M., Fransson, PA. et al. Cervical proprioception is sufficient for head orientation after bilateral vestibular loss. Eur J Appl Physiol 107, 73–81 (2009). https://doi.org/10.1007/s00421-009-1097-3
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-009-1097-3