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Journal of Neurology, Neurosurgery, and Psychiatry logoLink to Journal of Neurology, Neurosurgery, and Psychiatry
. 2005 May;76(5):670–678. doi: 10.1136/jnnp.2004.046565

The vestibular control of balance after stroke

J Marsden 1, D Playford 1, B Day 1
PMCID: PMC1739624  PMID: 15834025

Abstract

Objectives: To examine vestibular control of balance in those who recovered the ability to stand after middle cerebral artery (MCA) stroke.

Methods: Sixteen patients with MCA stroke were compared with 10 age matched controls. Two additional patients were studied with isolated corticospinal tract lesions, one each at the level of the pons and medulla. Vestibular evoked postural responses were obtained using galvanic vestibular stimulation (GVS) while patients stood with their eyes closed and head facing forwards, equally loading both legs. The GVS response was characterised by measuring the amplitude of the stimulus evoked lateral forces acting through each leg and the lateral displacement of the axial skeleton.

Results: Lateral displacement and net lateral force following GVS were significantly larger after stroke. Unlike controls, the lateral forces in the stroke group were asymmetrical, being enhanced on the side of the non-paretic limb and small on the side of the paretic limb. The degree of GVS evoked asymmetry correlated with corticospinal damage assessed using transcranial magnetic stimulation. A similar asymmetrical response was seen in the patient with the pontine lesion but not the patient with the medullary lesion.

Conclusions: MCA stroke may disrupt corticobulbar projections to brainstem output pathways involved in vestibular control of balance. These projections are either collaterals of the corticospinal tract or lie close to that tract and terminate in the pons/upper medulla. This hypothesis accounts for the association between corticospinal tract damage and GVS response asymmetry, and the lack of GVS evoked asymmetry with corticospinal lesions below the rostral medulla.

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Selected References

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  1. Akbarian S., Grüsser O. J., Guldin W. O. Corticofugal connections between the cerebral cortex and brainstem vestibular nuclei in the macaque monkey. J Comp Neurol. 1994 Jan 15;339(3):421–437. doi: 10.1002/cne.903390309. [DOI] [PubMed] [Google Scholar]
  2. Akbarian S., Grüsser O. J., Guldin W. O. Corticofugal projections to the vestibular nuclei in squirrel monkeys: further evidence of multiple cortical vestibular fields. J Comp Neurol. 1993 Jun 1;332(1):89–104. doi: 10.1002/cne.903320107. [DOI] [PubMed] [Google Scholar]
  3. Berardelli A., Inghilleri M., Cruccu G., Mercuri B., Manfredi M. Electrical and magnetic transcranial stimulation in patients with corticospinal damage due to stroke or motor neurone disease. Electroencephalogr Clin Neurophysiol. 1991 Oct;81(5):389–396. doi: 10.1016/0168-5597(91)90028-v. [DOI] [PubMed] [Google Scholar]
  4. Bohannon R. W., Larkin P. A. Lower extremity weight bearing under various standing conditions in independently ambulatory patients with hemiparesis. Phys Ther. 1985 Sep;65(9):1323–1325. doi: 10.1093/ptj/65.9.1323. [DOI] [PubMed] [Google Scholar]
  5. Brandt T., Dieterich M. The vestibular cortex. Its locations, functions, and disorders. Ann N Y Acad Sci. 1999 May 28;871:293–312. doi: 10.1111/j.1749-6632.1999.tb09193.x. [DOI] [PubMed] [Google Scholar]
  6. Branston N. M., Bentivoglio P., Momma F., Symon L. Changes in pyramidal tract conduction with experimental brain-stem ischaemia in the monkey. Electroencephalogr Clin Neurophysiol. 1988 May;69(5):469–475. doi: 10.1016/0013-4694(88)90069-7. [DOI] [PubMed] [Google Scholar]
  7. Britton T. C., Day B. L., Brown P., Rothwell J. C., Thompson P. D., Marsden C. D. Postural electromyographic responses in the arm and leg following galvanic vestibular stimulation in man. Exp Brain Res. 1993;94(1):143–151. doi: 10.1007/BF00230477. [DOI] [PubMed] [Google Scholar]
  8. Bucher S. F., Dieterich M., Wiesmann M., Weiss A., Zink R., Yousry T. A., Brandt T. Cerebral functional magnetic resonance imaging of vestibular, auditory, and nociceptive areas during galvanic stimulation. Ann Neurol. 1998 Jul;44(1):120–125. doi: 10.1002/ana.410440118. [DOI] [PubMed] [Google Scholar]
  9. Cauquil A. S., Day B. L. Galvanic vestibular stimulation modulates voluntary movement of the human upper body. J Physiol. 1998 Dec 1;513(Pt 2):611–619. doi: 10.1111/j.1469-7793.1998.611bb.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Courjon J. H., Precht W., Sirkin D. W. Vestibular nerve and nuclei unit responses and eye movement responses to repetitive galvanic stimulation of the labyrinth in the rat. Exp Brain Res. 1987;66(1):41–48. doi: 10.1007/BF00236200. [DOI] [PubMed] [Google Scholar]
  11. Curthoys I. S., Halmagyi G. M. Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss. J Vestib Res. 1995 Mar-Apr;5(2):67–107. [PubMed] [Google Scholar]
  12. Day B. L., Séverac Cauquil A., Bartolomei L., Pastor M. A., Lyon I. N. Human body-segment tilts induced by galvanic stimulation: a vestibularly driven balance protection mechanism. J Physiol. 1997 May 1;500(Pt 3):661–672. doi: 10.1113/jphysiol.1997.sp022051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Di Fabio R. P., Badke M. B., Duncan P. W. Adapting human postural reflexes following localized cerebrovascular lesion: analysis of bilateral long latency responses. Brain Res. 1986 Jan 22;363(2):257–264. doi: 10.1016/0006-8993(86)91010-3. [DOI] [PubMed] [Google Scholar]
  14. Di Fabio R. P., Badke M. B. Influence of cerebrovascular accident on elongated and passively shortened muscle responses after forward sway. Phys Ther. 1988 Aug;68(8):1215–1220. [PubMed] [Google Scholar]
  15. Di Fabio R. P. Lower extremity antagonist muscle response following standing perturbation in subjects with cerebrovascular disease. Brain Res. 1987 Mar 17;406(1-2):43–51. doi: 10.1016/0006-8993(87)90767-0. [DOI] [PubMed] [Google Scholar]
  16. Fukushima K. Corticovestibular interactions: anatomy, electrophysiology, and functional considerations. Exp Brain Res. 1997 Oct;117(1):1–16. doi: 10.1007/pl00005786. [DOI] [PubMed] [Google Scholar]
  17. Garland S. J., Stevenson T. J., Ivanova T. Postural responses to unilateral arm perturbation in young, elderly, and hemiplegic subjects. Arch Phys Med Rehabil. 1997 Oct;78(10):1072–1077. doi: 10.1016/s0003-9993(97)90130-1. [DOI] [PubMed] [Google Scholar]
  18. Goldberg J. M., Fernández C., Smith C. E. Responses of vestibular-nerve afferents in the squirrel monkey to externally applied galvanic currents. Brain Res. 1982 Dec 2;252(1):156–160. doi: 10.1016/0006-8993(82)90990-8. [DOI] [PubMed] [Google Scholar]
  19. Guldin W. O., Grüsser O. J. Is there a vestibular cortex? Trends Neurosci. 1998 Jun;21(6):254–259. doi: 10.1016/s0166-2236(97)01211-3. [DOI] [PubMed] [Google Scholar]
  20. Horak F. B., Esselman P., Anderson M. E., Lynch M. K. The effects of movement velocity, mass displaced, and task certainty on associated postural adjustments made by normal and hemiplegic individuals. J Neurol Neurosurg Psychiatry. 1984 Sep;47(9):1020–1028. doi: 10.1136/jnnp.47.9.1020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kably B., Drew T. Corticoreticular pathways in the cat. I. Projection patterns and collaterization. J Neurophysiol. 1998 Jul;80(1):389–405. doi: 10.1152/jn.1998.80.1.389. [DOI] [PubMed] [Google Scholar]
  22. Karnath H. O., Ferber S., Dichgans J. The neural representation of postural control in humans. Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13931–13936. doi: 10.1073/pnas.240279997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Keizer K., Kuypers H. G. Distribution of corticospinal neurons with collaterals to lower brain stem reticular formation in cat. Exp Brain Res. 1984;54(1):107–120. doi: 10.1007/BF00235823. [DOI] [PubMed] [Google Scholar]
  24. Keizer K., Kuypers H. G. Distribution of corticospinal neurons with collaterals to the lower brain stem reticular formation in monkey (Macaca fascicularis). Exp Brain Res. 1989;74(2):311–318. doi: 10.1007/BF00248864. [DOI] [PubMed] [Google Scholar]
  25. Kirker S. G., Jenner J. R., Simpson D. S., Wing A. M. Changing patterns of postural hip muscle activity during recovery from stroke. Clin Rehabil. 2000 Dec;14(6):618–626. doi: 10.1191/0269215500cr370oa. [DOI] [PubMed] [Google Scholar]
  26. LOWENSTEIN O. The effect of galvanic polarization on the impulse discharge from sense endings in the isolated labyrinth of the thornback ray (Raja clavata). J Physiol. 1955 Jan 28;127(1):104–117. doi: 10.1113/jphysiol.1955.sp005241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lamas J. A., Martinez L., Canedo A. Pericruciate fibres to the red nucleus and to the medial bulbar reticular formation. Neuroscience. 1994 Sep;62(1):115–124. doi: 10.1016/0306-4522(94)90319-0. [DOI] [PubMed] [Google Scholar]
  28. Mizrahi J., Solzi P., Ring H., Nisell R. Postural stability in stroke patients: vectorial expression of asymmetry, sway activity and relative sequence of reactive forces. Med Biol Eng Comput. 1989 Mar;27(2):181–190. doi: 10.1007/BF02446228. [DOI] [PubMed] [Google Scholar]
  29. Muto N., Shinomiya K., Komori H., Mochida K., Furuya K. Spinal cord monitoring of the ventral funiculus function. Analysis of spinal field potentials after galvanic vestibular stimulation. Spine (Phila Pa 1976) 1995 Nov 15;20(22):2429–2435. doi: 10.1097/00007632-199511001-00010. [DOI] [PubMed] [Google Scholar]
  30. Palmer E., Downes L., Ashby P. Associated postural adjustments are impaired by a lesion of the cortex. Neurology. 1996 Feb;46(2):471–475. doi: 10.1212/wnl.46.2.471. [DOI] [PubMed] [Google Scholar]
  31. Pastor M. A., Day B. L., Marsden C. D. Vestibular induced postural responses in Parkinson's disease. Brain. 1993 Oct;116(Pt 5):1177–1190. doi: 10.1093/brain/116.5.1177. [DOI] [PubMed] [Google Scholar]
  32. Pérennou D. A., Leblond C., Amblard B., Micallef J. P., Rouget E., Pélissier J. The polymodal sensory cortex is crucial for controlling lateral postural stability: evidence from stroke patients. Brain Res Bull. 2000 Oct;53(3):359–365. doi: 10.1016/s0361-9230(00)00360-9. [DOI] [PubMed] [Google Scholar]
  33. Pérennou Dominic Alain, Amblard Bernard, Laassel El Mostafa, Benaim Charles, Hérisson Christian, Pélissier Jacques. Understanding the pusher behavior of some stroke patients with spatial deficits: a pilot study. Arch Phys Med Rehabil. 2002 Apr;83(4):570–575. doi: 10.1053/apmr.2002.31198. [DOI] [PubMed] [Google Scholar]
  34. Rogers M. W., Hedman L. D., Pai Y. C. Kinetic analysis of dynamic transitions in stance support accompanying voluntary leg flexion movements in hemiparetic adults. Arch Phys Med Rehabil. 1993 Jan;74(1):19–25. [PubMed] [Google Scholar]
  35. Terao S., Miura N., Takeda A., Takahashi A., Mitsuma T., Sobue G. Course and distribution of facial corticobulbar tract fibres in the lower brain stem. J Neurol Neurosurg Psychiatry. 2000 Aug;69(2):262–265. doi: 10.1136/jnnp.69.2.262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Thompson P. D., Day B. L., Rothwell J. C., Dick J. P., Cowan J. M., Asselman P., Griffin G. B., Sheehy M. P., Marsden C. D. The interpretation of electromyographic responses to electrical stimulation of the motor cortex in diseases of the upper motor neurone. J Neurol Sci. 1987 Aug;80(1):91–110. doi: 10.1016/0022-510x(87)90224-3. [DOI] [PubMed] [Google Scholar]
  37. Watson S. R., Colebatch J. G. EMG responses in the soleus muscles evoked by unipolar galvanic vestibular stimulation. Electroencephalogr Clin Neurophysiol. 1997 Dec;105(6):476–483. doi: 10.1016/s0924-980x(97)00044-1. [DOI] [PubMed] [Google Scholar]
  38. Welgampola M. S., Colebatch J. G. Vestibulospinal reflexes: quantitative effects of sensory feedback and postural task. Exp Brain Res. 2001 Aug;139(3):345–353. doi: 10.1007/s002210100754. [DOI] [PubMed] [Google Scholar]
  39. Yelnik Alain P., Lebreton Frederique O., Bonan Isabelle V., Colle Florence M. C., Meurin Francesca A., Guichard Jean Pierre, Vicaut Eric. Perception of verticality after recent cerebral hemispheric stroke. Stroke. 2002 Sep;33(9):2247–2253. doi: 10.1161/01.str.0000027212.26686.48. [DOI] [PubMed] [Google Scholar]

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