Transiently worse postural effects after vestibulo-ocular reflex gain-down adaptation in healthy adults.
Adaptation
Foam
Posture
VOR
Vestibular
Journal
Experimental brain research
ISSN: 1432-1106
Titre abrégé: Exp Brain Res
Pays: Germany
ID NLM: 0043312
Informations de publication
Date de publication:
05 Oct 2024
05 Oct 2024
Historique:
received:
17
04
2024
accepted:
05
09
2024
medline:
6
10
2024
pubmed:
6
10
2024
entrez:
5
10
2024
Statut:
aheadofprint
Résumé
Suffering an acute asymmetry in vestibular function (i.e., vestibular neuritis) causes increased sway. Non-causal studies report associations between lateral semicircular canal function and balance ability, but direct links remain controversial. We investigate the immediate effect on body sway after unilateral vestibulo-ocular reflex (VOR) gain down adaptation simulating acute peripheral vestibular hypofunction. Eighteen healthy adults, mean age 27.4 (± 12.4), stood wearing an inertial measurement device with their eyes closed on foam before and after incremental VOR gain down adaptation to simulate mild unilateral vestibular neuritis. Active head impulse VOR gain was measured before and after the adaptation to ensure VOR gain adaptation. Percentage change for VOR gain was determined. Sway area was compared before and after VOR adaptation. VOR gain decreased unilaterally exceeding meaningful change values. Sway area was significantly greater immediately after VOR gain down adaptation, but quickly returned to baseline. In a subset of subjects VOR gain was re-assessed and found to remain adapted despite sway normalization. These results indicate that oculomotor adaptation targeting the lateral semicircular canal VOR pathway has an immediate, albeit transient increase in body sway. Rapid return of body sway to baseline levels suggests dynamic sensory reweighting between vestibular and somatosensory inputs to resolve the undesirable increased body sway.
Identifiants
pubmed: 39368023
doi: 10.1007/s00221-024-06923-7
pii: 10.1007/s00221-024-06923-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIDCD NIH HHS
ID : K23 DC018303
Pays : United States
Organisme : Vestibular Disorders Association
ID : Travel Grant
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Agrawal Y, Van De Berg R, Wuyts F et al (2019) Presbyvestibulopathy: diagnostic criteria Consensus document of the classification committee of the Bárány Society. J Vestib Res 29:161–170. https://doi.org/10.3233/VES-190672
doi: 10.3233/VES-190672
pubmed: 31306146
Allison LK, Kiemel T, Jeka JJ (2018) Sensory-challenge balance exercises improve multisensory reweighting in fall-prone older adults. J Neurol Phys Ther 42:84–93. https://doi.org/10.1097/NPT.0000000000000214
doi: 10.1097/NPT.0000000000000214
pubmed: 29547483
Allum JHJ (2012) Recovery of vestibular ocular reflex function and balance control after a unilateral peripheral vestibular deficit. 3:1–7. https://doi.org/10.3389/fneur.2012.00083
Allum JHJ, Honegger F (2020) Correlations between multi-plane vHIT responses and Balance Control after Onset of an Acute Unilateral Peripheral vestibular deficit. Otology Neurotology 41:e952–e960. https://doi.org/10.1097/MAO.0000000000002482
doi: 10.1097/MAO.0000000000002482
pubmed: 32658113
Allum JHJ, Scheltinga A, Honegger F (2017) The effect of peripheral vestibular recovery on improvements in Vestibulo-ocular reflexes and Balance Control after Acute Unilateral Peripheral vestibular loss. Otology Neurotology 38:e531–e538. https://doi.org/10.1097/MAO.0000000000001477
doi: 10.1097/MAO.0000000000001477
pubmed: 29135873
Anson E, Bigelow RT, Swenor B et al (2017) Loss of peripheral sensory function explains much of the increase in postural sway in healthy older adults. Front Aging Neurosci 9. https://doi.org/10.3389/fnagi.2017.00202
Anson E, Bigelow RT, Studenski S et al (2019) Failure on the foam eyes closed test of standing Balance Associated with reduced semicircular canal function in healthy older adults. Ear Hear 40:340–344. https://doi.org/10.1097/AUD.0000000000000619
doi: 10.1097/AUD.0000000000000619
pubmed: 29894381
Anson ER (2024) BalanceSway_Repository_Dataset.xlsx. University of Rochester. Dataset. Figshare, ur.d.25601328.v1. https://rochester.figshare.com/articles/dataset/BalanceSway_Repository_Dataset_xlsx/25601328 .
Arntz AI, van der Putte DAM, Jonker ZD et al (2019) The vestibular drive for Balance Control is dependent on multiple sensory cues of gravity. Front Physiol 10:476. https://doi.org/10.3389/fphys.2019.00476
doi: 10.3389/fphys.2019.00476
pubmed: 31114504
Assländer L, Peterka RJ (2016) Sensory reweighting dynamics following removal and addition of visual and proprioceptive cues. J Neurophysiol 116:272–285. https://doi.org/10.1152/jn.01145.2015
doi: 10.1152/jn.01145.2015
pubmed: 27075544
Bartl K, Lehnen N, Kohlbecher S, Schneider E (2009) Head Impulse Testing using video-oculography. Ann N Y Acad Sci 1164:331–333
doi: 10.1111/j.1749-6632.2009.03850.x
pubmed: 19645921
Beylergil SB, Karmali F, Wang W et al (2019) Vestibular roll tilt thresholds partially mediate age-related effects on balance. Progress in Brain Research. Elsevier, pp 249–267
Brooks JX, Carriot J, Cullen KE (2015) Learning to expect the unexpected: Rapid updating in primate cerebellum during voluntary self-motion. Nat Neurosci 18. https://doi.org/10.1038/nn.4077
Carriot J, Brooks JX, Cullen KE (2013) Multimodal integration of self-motion cues in the vestibular system: active versus passive translations. J Neurosci 33:19555–19566. https://doi.org/10.1523/JNEUROSCI.3051-13.2013
doi: 10.1523/JNEUROSCI.3051-13.2013
pubmed: 24336720
Carriot J, Jamali M, Chacron MJ, Cullen KE (2014) Statistics of the vestibular input experienced during natural self-motion: implications for neural processing. J Neurosci 34:8347–8357. https://doi.org/10.1523/JNEUROSCI.0692-14.2014
doi: 10.1523/JNEUROSCI.0692-14.2014
pubmed: 24920638
Carriot J, Jamali M, Brooks JX, Cullen KE (2015) Integration of Canal and Otolith inputs by central vestibular neurons is Subadditive for both active and Passive Self-Motion: implication for perception. J Neurosci 35:3555–3565. https://doi.org/10.1523/JNEUROSCI.3540-14.2015
doi: 10.1523/JNEUROSCI.3540-14.2015
pubmed: 25716854
Cathers I, Day BL, Fitzpatrick RC (2005) Otolith and canal reflexes in human standing. J Physiol 563:229–234. https://doi.org/10.1113/jphysiol.2004.079525
doi: 10.1113/jphysiol.2004.079525
pubmed: 15618274
Cohen H, Blatchly CA, Gombash LL (1993) A study of the clinical test of sensory interaction and balance. Phys Ther 73:346–351
doi: 10.1093/ptj/73.6.346
pubmed: 8497509
Cohen HS, Mulavara AP, Stitz J et al (2019) Screening for vestibular disorders using the modified clinical test of sensory Interaction and Balance and Tandem walking with eyes closed. Otology Neurotology 40:658–665. https://doi.org/10.1097/MAO.0000000000002173
doi: 10.1097/MAO.0000000000002173
pubmed: 31083095
Cullen KE (2019) Vestibular processing during natural self-motion: implications for perception and action. Nat Rev Neurosci 20:346–363
doi: 10.1038/s41583-019-0153-1
pubmed: 30914780
Cullen KE (2023) Internal models of self-motion: neural computations by the vestibular cerebellum. Trends Neurosci 46:986–1002. https://doi.org/10.1016/J.TINS.2023.08.009
doi: 10.1016/J.TINS.2023.08.009
pubmed: 37739815
Cullen K, Roy J (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91:1919–1933. https://doi.org/10.1152/jn.00988.2003
doi: 10.1152/jn.00988.2003
pubmed: 15069088
Cullen KE, Zobeiri OA (2021) Proprioception and the predictive sensing of active self-motion. Curr Opin Physiol 20:29–38. https://doi.org/10.1016/j.cophys.2020.12.001
doi: 10.1016/j.cophys.2020.12.001
pubmed: 33954270
Dale A, Cullen KE (2019) The ventral posterior lateral thalamus preferentially encodes externally Applied Versus active Movement: implications for self-motion perception. https://doi.org/10.1093/cercor/bhx325 . Cerebral cortex 29:
Das VE, Dell’osso LF, Leigh RJ (1999) Enhancement of the vestibulo-ocular reflex by prior eye movements. J Neurophysiol 81:2884–2892. https://doi.org/10.1152/jn.1999.81.6.2884
doi: 10.1152/jn.1999.81.6.2884
pubmed: 10368405
Diaz-Artiles A, Karmali F (2021) Vestibular Precision at the level of Perception, Eye Movements, posture, and neurons. Neuroscience 468:282–320. https://doi.org/10.1016/J.NEUROSCIENCE.2021.05.028
doi: 10.1016/J.NEUROSCIENCE.2021.05.028
pubmed: 34087393
Faralli M, Ori M, Ricci G et al (2022) Disruption of self-motion perception without vestibular reflex alteration in ménière’s disease. J Vestib Res 32:193–203. https://doi.org/10.3233/VES-201520
doi: 10.3233/VES-201520
pubmed: 34151876
Fitzpatrick RC, Day BL (2004) Probing the human vestibular system with galvanic stimulation. J Appl Physiol 96:2301–2316. https://doi.org/10.1152/japplphysiol.00008.2004
doi: 10.1152/japplphysiol.00008.2004
pubmed: 15133017
Fox A, Koceja D (2017) Static otolithic drive alters presynaptic inhibition in soleus motor pool. J Electromyogr Kinesiol 32:37–43. https://doi.org/10.1016/j.jelekin.2016.12.002
doi: 10.1016/j.jelekin.2016.12.002
pubmed: 28039767
Fujimoto C, Kamogashira T, Kinoshita M et al (2014) Power Spectral Analysis of Postural Sway during Foam Posturography in patients with peripheral vestibular dysfunction. Otology Neurotology 35:e317–e323. https://doi.org/10.1097/MAO.0000000000000554
doi: 10.1097/MAO.0000000000000554
pubmed: 25111526
Gabriel GA, Harris LR, Gnanasegaram JJ et al (2022) Age-related changes to vestibular heave and pitch perception and associations with postural control. Scientific Reports 2022 12:1 12:1–16. https://doi.org/10.1038/s41598-022-09807-4
Gimmon Y, Migliaccio AA, Todd CJ et al (2018) Simultaneous and opposing horizontal VOR adaptation in humans suggests functionally independent neural circuits. J Neurophysiol 120:1496–1504. https://doi.org/10.1152/jn.00134.2018
doi: 10.1152/jn.00134.2018
pubmed: 29947586
Gimmon Y, Migliaccio AA, Kim KJ, Schubert MC (2019) VOR adaptation training and retention in a patient with profound bilateral vestibular hypofunction. Laryngoscope 129:2568–2573. https://doi.org/10.1002/LARY.27838
doi: 10.1002/LARY.27838
pubmed: 30779443
Giray M, Kirazli Y, Karapolat H et al (2009) Short-term effects of vestibular Rehabilitation in patients with chronic unilateral vestibular dysfunction: a randomized controlled study. Arch Phys Med Rehabil 90:1325–1331. https://doi.org/10.1016/j.apmr.2009.01.032
doi: 10.1016/j.apmr.2009.01.032
pubmed: 19651266
Grillner S, Hongo T (1972) Vestibulospinal effects on Motoneurones and Interneurones in the Lumbosacral Cord. Prog Brain Res 37:243–262. https://doi.org/10.1016/S0079-6123(08)63906-0
doi: 10.1016/S0079-6123(08)63906-0
pubmed: 4642044
Haggerty SE, Wu AR, Sienko KH, Kuo AD (2017) A shared neural integrator for human posture control. J Neurophysiol 118:894–903. https://doi.org/10.1152/jn.00428.2016
doi: 10.1152/jn.00428.2016
pubmed: 28446583
Hall CD, Herdman SJ, Whitney SL et al (2022) Vestibular Rehabilitation for Peripheral vestibular hypofunction: an updated clinical practice Guideline from the Academy of neurologic physical therapy of the American Physical Therapy Association. J Neurol Phys Ther 46:118–177. https://doi.org/10.1097/npt.0000000000000382
doi: 10.1097/npt.0000000000000382
pubmed: 34864777
Hwang S, Agada P, Kiemel T, Jeka JJ (2014) Dynamic reweighting of three modalities for sensor fusion. PLoS ONE 9:1–8
doi: 10.1371/journal.pone.0088132
Hwang S, Ma L, Kawata K et al (2016) Vestibular dysfunction following Sub-concussive Head Impact. J Neurotrauma. https://doi.org/10.1089/neu.2015.4238
doi: 10.1089/neu.2015.4238
pubmed: 26885560
Karmali F, Bermúdez Rey MC, Clark TK et al (2017) Multivariate analyses of Balance Test performance, vestibular thresholds, and Age. Front Neurol 8:578. https://doi.org/10.3389/fneur.2017.00578
doi: 10.3389/fneur.2017.00578
pubmed: 29167656
Lackner JR, DiZio P (2020) Velocity storage: its multiple roles. J Neurophysiol 123:1206–1215. https://doi.org/10.1152/jn.00139.2019
doi: 10.1152/jn.00139.2019
pubmed: 31913743
Lacour M, Tardivet L, Thiry A (2022) Posture deficits and recovery after unilateral vestibular loss: early Rehabilitation and Degree of Hypofunction Matter. Front Hum Neurosci 15. https://doi.org/10.3389/FNHUM.2021.776970
Laurens J, Angelaki DE (2017) A unified internal model theory to resolve the paradox of active versus passive self-motion sensation. Elife 6. https://doi.org/10.7554/eLife.28074
Mahfuz MM, Schubert MC, Figtree WVC et al (2018) Optimal Human Passive Vestibulo-Ocular Reflex Adaptation does not rely on Passive Training. JARO - J Association Res Otolaryngol 19. https://doi.org/10.1007/s10162-018-0657-9
Mahfuz MM, Schubert MC, Figtree WVC, Migliaccio AA (2020) Retinal image Slip must pass the threshold for Human Vestibulo-Ocular Reflex Adaptation. J Assoc Res Otolaryngol. https://doi.org/10.1007/s10162-020-00751-6
doi: 10.1007/s10162-020-00751-6
pubmed: 32232608
Mancini M, Salarian A, Carlson-Kuhta P et al (2012) ISway: a sensitive, valid and reliable measure of postural control. J Neuroeng Rehabil 9:1–8. https://doi.org/10.1186/1743-0003-9-59/TABLES/5
doi: 10.1186/1743-0003-9-59/TABLES/5
Markham CH (1987) Vestibular control of muscular tone and posture. Can J Neurol Sci 14:493–496. https://doi.org/10.1017/s0317167100037975
doi: 10.1017/s0317167100037975
pubmed: 3315150
Matsugi A, Ueta Y, Oku K et al (2017) Effect of gaze-stabilization exercises on vestibular function during postural control. NeuroReport 28:439–443. https://doi.org/10.1097/WNR.0000000000000776
doi: 10.1097/WNR.0000000000000776
pubmed: 28368883
Medendorp WP, Alberts BBGT, Verhagen WIM et al (2018) Psychophysical evaluation of sensory reweighting in bilateral Vestibulopathy. Front Neurol 9:377. https://doi.org/10.3389/fneur.2018.00377
doi: 10.3389/fneur.2018.00377
pubmed: 29910766
Migliaccio AA, Schubert MC (2013) Unilateral adaptation of the human angular vestibulo-ocular reflex. J Assoc Res Otolaryngol 14:29–36. https://doi.org/10.1007/S10162-012-0359-7
doi: 10.1007/S10162-012-0359-7
pubmed: 23180230
Nashner L (1971) A model describing vestibular detection of body sway motion. Acta Otoaryngologica 72:429–436
doi: 10.3109/00016487109122504
Newlands SD, Abbatematteo B, Wei M et al (2018) Convergence of linear acceleration and yaw rotation signals on non-eye movement neurons in the vestibular nucleus of macaques. J Neurophysiol 119:73–83. https://doi.org/10.1152/JN.00382.2017/ASSET/IMAGES/LARGE/Z9K0121744180009.JPEG .
doi: 10.1152/JN.00382.2017/ASSET
pubmed: 28978765
Panichi R, Faralli M, Bruni R et al (2017) Asymmetric vestibular stimulation reveals persistent disruption of motion perception in unilateral vestibular lesions. J Neurophysiol 118:2819–2832. https://doi.org/10.1152/jn.00674.2016
doi: 10.1152/jn.00674.2016
pubmed: 28814637
Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118
doi: 10.1152/jn.2002.88.3.1097
pubmed: 12205132
Pettorossi VE, Schieppati M (2014) Neck Proprioception shapes Body Orientation and Perception of Motion. Front Hum Neurosci 8:118211. https://doi.org/10.3389/FNHUM.2014.00895/BIBTEX
doi: 10.3389/FNHUM.2014.00895/BIBTEX
Pettorossi VE, Panichi R, Botti FM et al (2015) Long-lasting effects of neck muscle vibration and contraction on self-motion perception of vestibular origin. Clin Neurophysiol 126:1886–1900. https://doi.org/10.1016/J.CLINPH.2015.02.057
doi: 10.1016/J.CLINPH.2015.02.057
pubmed: 25812729
Rinaudo CN, Schubert MC, Cremer PD et al (2021) Comparison of incremental vestibulo-ocular reflex adaptation training versus x1 training in patients with chronic peripheral vestibular hypofunction: a two-year randomized controlled trial. J Neurol Phys Ther 45:246–258. https://doi.org/10.1097/NPT.0000000000000369
doi: 10.1097/NPT.0000000000000369
pubmed: 34369452
Schneider E, Villgrattner T, Vockeroth J et al (2009) Eyeseecam: an eye movement-driven head camera for the examination of natural visual exploration. Ann N Y Acad Sci 1164:461–467. https://doi.org/10.1111/j.1749-6632.2009.03858.x
doi: 10.1111/j.1749-6632.2009.03858.x
pubmed: 19645949
Schneider AD, Jamali M, Carriot J et al (2015) The increased sensitivity of irregular peripheral canal and otolith vestibular afferents optimizes their encoding of Natural Stimuli. J Neurosci 35:5522–5536. https://doi.org/10.1523/JNEUROSCI.3841-14.2015
doi: 10.1523/JNEUROSCI.3841-14.2015
pubmed: 25855169
Schor RH, Miller AD (1981) Vestibular reflexes in neck and forelimb muscles evoked by roll tilt. 46:167–178. https://doi.org/10.1152/JN.1981.46.1.167
Schubert MC, Migliaccio AA (2019) New advances regarding adaptation of the vestibulo-ocular reflex. J Neurophysiol 122:644–658. https://doi.org/10.1152/JN.00729.2018
doi: 10.1152/JN.00729.2018
pubmed: 31215309
Schubert MC, Migliaccio AA, Minor LB, Clendaniel RA (2008) Retention of VOR gain following short-term VOR adaptation. Exp Brain Res 187:117–127. https://doi.org/10.1007/S00221-008-1289-9
doi: 10.1007/S00221-008-1289-9
pubmed: 18231780
Serrador JM, Lipsitz LA, Gopalakrishnan GS et al (2009) Loss of otolith function with age is associated with increased postural sway measures. Neurosci Lett 465:10–15
doi: 10.1016/j.neulet.2009.08.057
pubmed: 19716400
Shinoda Y, Sugiuchi Y, Izawa Y, Hata Y (2006) Long descending motor tract axons and their control of neck and axial muscles. Prog Brain Res 151:527–563. https://doi.org/10.1016/S0079-6123(05)51017-3
doi: 10.1016/S0079-6123(05)51017-3
pubmed: 16221600
Sozzi S, Schieppati M (2022) Balance Adaptation while standing on a compliant base depends on the current sensory Condition in healthy young adults. Front Hum Neurosci 16. https://doi.org/10.3389/FNHUM.2022.839799/FULL
Sprenger A, Wojak JF, Jandl NM, Helmchen C (2017) Postural control in bilateral vestibular failure: its relation to visual, proprioceptive, vestibular, and cognitive input. Front Neurol 0:444. https://doi.org/10.3389/FNEUR.2017.00444
doi: 10.3389/FNEUR.2017.00444
Strupp M, Arbusow V, Maag KP et al (1998) Vestibular exercises improve central vestibulespinal compensation after vestibular neuritis. Neurology 51:838–844. https://doi.org/10.1212/WNL.51.3.838/ASSET/A7E0116B-3EA0-4674-8BBA-6073D0C94122/ASSETS/GRAPHIC/41FF5.JPEG
doi: 10.1212/WNL.51.3.838/ASSET/A7E0116B-3EA0-4674-8BBA-6073D0C94122/ASSETS/GRAPHIC/41FF5.JPEG
pubmed: 9748036
Suzuki JI, Cohen B (1964) Head, eye, body and limb movements from semicircular canal nerves. Exp Neurol 10:393–405. https://doi.org/10.1016/0014-4886(64)90031-7
doi: 10.1016/0014-4886(64)90031-7
pubmed: 14228399
Todd CJ, Schubert MC, Rinaudo CN, Migliaccio AA (2022) Unidirectional Vertical Vestibuloocular Reflex adaptation in humans using 1D and 2D scenes. Otology Neurotology 43:E1039–E1044. https://doi.org/10.1097/MAO.0000000000003684
doi: 10.1097/MAO.0000000000003684
pubmed: 36075099
Wagner AR, Kobel MJ, Merfeld DM (2021) Impact of Canal-Otolith integration on Postural Control. Front Integr Neurosci 15. https://doi.org/10.3389/FNINT.2021.773008/FULL