Skip to main content
SpringerLink
Log in

Human Vestibulo-Ocular Reflex Adaptation Training: Time Beats Quantity

  • Research Article
  • Published:
Journal of the Association for Research in Otolaryngology Aims and scope Submit manuscript

Abstract

The vestibulo-ocular reflex (VOR) is the main gaze stabilising system during rapid head movements. The VOR is highly plastic and its gain (eye/head velocity) can be increased via training that induces an incrementally increasing retinal image slip error signal to drive VOR adaptation. Using the unilateral incremental VOR adaptation technique and horizontal active head impulses as the vestibular stimulus, we sought to determine the factors important for VOR adaptation including: the total training time, ratio and number of head impulses to each side (adapting and non-adapting sides; the adapting side was pseudo-randomised left or right) and exposure time to the visual target during each head impulse. We tested 11 normal subjects, each over 5 separate sessions and training protocols. The basic training protocol (protocol one) consisted of unilateral incremental VOR adaptation training lasting 15 min with the ratio of head impulses to each side 1:1. Each protocol varied from the basic. For protocol two, the ratio of impulses were in favour of the adapting side by 2:1. For protocol three, all head impulses were towards the adapting side and the training only lasted 7.5 min. For protocol four, all impulses were towards the adapting side and lasted 15 min. For protocol five, all head impulses were to the adapting side and the exposure time to the visual target during each impulse was doubled. We measured the active and passive VOR gains before and after the training. Albeit with small sample size, our data suggest that the total training time and the visual target exposure time for each head impulse affected adaptation, whereas the total number and repetition rate of head impulses did not. These data have implications for vestibular rehabilitation, suggesting that quality and duration of VOR adaptation exercises are more important than rapid repetition of exercises.

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

  • Bahill AT, McDonald JD (1983a) Model emulates human smooth pursuit system producing zero-latency target tracking. Biol Cybern 48:213–222

    Article  CAS  PubMed  Google Scholar 

  • Bahill AT, McDonald JD (1983b) Smooth pursuit eye movements in response to predictable target motions. Vis Res 23:1573–1583

    Article  CAS  PubMed  Google Scholar 

  • Barnes GR, Goodbody S, Collins S (1995) Volitional control of anticipatory ocular pursuit responses under stabilised image conditions in humans. Exp Brain Res 106:301–317

    Article  CAS  PubMed  Google Scholar 

  • Bartl K, Lehnen N, Kohlbecher S, Schneider E (2009) Head impulse testing using video-oculography. Ann N Y Acad Sci 1164:331–333

    Article  PubMed  Google Scholar 

  • Carcaud J, França de Barros F, Idoux E, Eugène D, Reveret L, Moore LE, Vidal PP, Beraneck M (2017) Long-lasting visuo-vestibular mismatch in freely-behaving mice reduces the vestibulo-ocular reflex and leads to neural changes in the direct vestibular pathway. eNeuro 4:1

    Article  Google Scholar 

  • Carey JP, Minor LB, Peng GC, Della Santina CC, Cremer PD, Haslwanter T. Changes in the three-dimensional angular vestibulo-ocular reflex following intratympanic gentamicin for Ménière's disease. J Assoc Res Otolaryngol 3:430-443, 2002

  • Carriot J, Jamali M, Brooks JX, Cullen KE. 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, 2015

  • Clendaniel RA, Lasker DM, Minor LB (2001) Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. IV. Responses after spectacle-induced adaptation. J Neurophysiol 86:1594–1611

    Article  CAS  PubMed  Google Scholar 

  • Fadaee SB, Migliaccio AA (2016) The effect of retinal image error update rate on human vestibulo-ocular reflex gain adaptation. Exp Brain Res 234:1085–1094

    Article  PubMed  Google Scholar 

  • Gauthier GM, Robinson DA (1975) Adaptation of human’s vestibulo-ocular reflex to magnifying glasses. Brain Res 92:331–335

    Article  CAS  PubMed  Google Scholar 

  • Gonshor A, Melvill Jones G (1976a) Short-term adaptive changes in the human vestibulo-ocular reflex arc. J Physiol 256:361–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonshor A, Melvill Jones G (1976b) Extreme vestibulo-ocular adaptation induced by prolonged optical reversal of vision. J Physiol 256:381–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grossman GE, Leigh RJ, Abel LA, Lanska DJ, Thurston SE (1988) Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 70:470–476

    Article  CAS  PubMed  Google Scholar 

  • Halmagyi GM, Curthoys IS (1988) A clinical sign of canal paresis. Arch Neurol 45:737–739

    Article  CAS  PubMed  Google Scholar 

  • Hübner PP, Khan SI, Migliaccio AA (2014) Velocity-selective adaptation of the horizontal and cross-axis vestibulo-ocular reflex in the mouse. Exp Brain Res 232:3035–3046

    Article  PubMed  Google Scholar 

  • Hübner PP, Khan SI, Migliaccio AA (2015) The mammalian efferent vestibular system plays a crucial role in the high-frequency response and short-term adaptation of the vestibuloocular reflex. J Neurophysiol 114:3154–3165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kagerer FA, Contreras-Vidal JL, Stelmach GE (1997) Adaptation to gradual as compared with sudden visuo-motor distortions. Exp Brain Res 115(3):557–561

    Article  CAS  PubMed  Google Scholar 

  • Kettner RE, Leung HC, Peterson BW (1996) Predictive smooth pursuit of complex two-dimensional trajectories in monkey: component interactions. Exp Brain Res 108:221–235

    Article  CAS  PubMed  Google Scholar 

  • Khan SI, Hübner PP, Brichta AM, Smith DW, Migliaccio AA (2017) Aging reduces the high-frequency and short-term adaptation of the vestibulo-ocular reflex in mice. Neurobiol Aging 51:122–131

    Article  PubMed  Google Scholar 

  • Kilgard MP, Merzenich MM (2002) Order-sensitive plasticity in adult primary auditory cortex. Proc Natl Acad Sci U S A 99:3205–3209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Körding KP, Tenenbaum JB, Shadmehr R (2007) The dynamics of memory as a consequence of optimal adaptation to a changing body. Nat Neurosci 10:779–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krauzlis RJ, Lisberger SG (1994) Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys. J Neurophysiol 72:150–162

    Article  CAS  PubMed  Google Scholar 

  • Lisberger SG, Pavelko TA, Broussard DM (1994a) Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons. J Neurophysiol 72:928–953

    Article  CAS  Google Scholar 

  • Lisberger SG, Pavelko TA, Bronte-Stewart HM, Stone LS (1994b) Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocculus and ventral paraflocculus. J Neurophysiol 72:954–973

    Article  CAS  Google Scholar 

  • Mahfuz MM, Schubert MC, Todd CJ, Figtree WVC, Khan SI, Migliaccio AA (2018) The effect of visual contrast on human vestibulo-ocular reflex training. J Assoc Res Otolaryngol 19:113–122

    Article  Google Scholar 

  • McCrea RA, Yoshida K, Evinger C, Berthoz A (1981) The location, axonal arborization and termination sites of eye-movement related secondary vestibular neurons demonstrated by intraaxonal HRP injection in the alert cat. In: Fuchs A, Becker W (eds) Progress in oculomotor research. Elsevier, North Holland, Amsterdam, pp 379–386

    Google Scholar 

  • McHugh DE, Bahill AT (1985) Learning to track predictable target waveforms without a time delay. Invest Opthalmol Vis Sci 26:932–937

    CAS  Google Scholar 

  • Migliaccio AA, Schubert MC (2013) Unilateral adaptation of the human angular vestibulo-ocular reflex. J Assoc Res Otolaryngol 14:29–36

    Article  PubMed  Google Scholar 

  • Migliaccio AA, Schubert MC (2014) Pilot study of a new rehabilitation tool: improved unilateral short-term adaptation of the human angular vestibulo-ocular reflex. Otol Neurotol 35:310–316

    Article  Google Scholar 

  • Minor LB, Lasker DM, Backous DD, Hullar TE (1999) Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. I. Normal responses. J Neurophysiol 82:1254–1270

    Article  CAS  PubMed  Google Scholar 

  • Mitchell DE, Della Santina CC, Cullen KE (2017) Plasticity within excitatory and inhibitory pathways of the vestibulo-spinal circuitry guides changes in motor performance. Sci Rep 7(853):853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagarajan SS, Blake DT, Wright BA, Byl N, Merzenich MM (1998) Practice-related improvements in somatosensory interval discrimination are temporally specific but generalize across skin location, hemisphere, and modality. J Neurosci 18:1559–1570

    Article  CAS  PubMed  Google Scholar 

  • Paige GD, Sargent EW (1991) Visually-induced adaptive plasticity in the human vestibulo-ocular reflex. Exp Brain Res 84:25–34

    Article  CAS  PubMed  Google Scholar 

  • Sadeghi SG, Minor LB, Cullen KE (2011) Multimodal integration after unilateral labyrinthine lesion: single vestibular nuclei neuron responses and implications for postural compensation. J Neurophysiol 105:661–673

    Article  PubMed  Google Scholar 

  • Schubert MC, Della Santina CC, Shelhamer M (2008) Incremental angular vestibulo-ocular reflex adaptation to active head rotation. Exp Brain Res 191:435–446

    Article  PubMed  PubMed Central  Google Scholar 

  • Shelhamer M, Robinson DA, Tan HS (1992) Context-specific adaptation of the gain of the vestibulo-ocular reflex in humans. J Vestib Res 2:89–96

    CAS  PubMed  Google Scholar 

  • Shelhamer M, Tiliket C, Roberts D, Kramer PD, Zee DS (1994) Short-term vestibulo-ocular reflex adaptation in humans. II. Error signals. Exp Brain Res 100:328–336

    Article  CAS  PubMed  Google Scholar 

  • Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29:467–492

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

A.A. Migliaccio was supported by The Garnett Passe and Rodney Williams Memorial Foundation, Senior/Principal Research Fellowship in Otorhinolaryngology and Project Grant (2013-15) and NHMRC Development Grant APP105550.

Author information

Authors and Affiliations

  1. Balance and Vision Laboratory, Neuroscience Research Australia, Cnr Barker Street & Easy Street, Randwick, NSW, 2031, Australia

    M. Muntaseer Mahfuz, William V. C. Figtree, Christopher J. Todd & Americo A. Migliaccio

  2. University of New South Wales, Sydney, NSW, 2033, Australia

    M. Muntaseer Mahfuz, William V. C. Figtree, Christopher J. Todd & Americo A. Migliaccio

  3. Laboratory of Vestibular NeuroAdaptation, Department of Otolaryngology—Head and Neck Surgery, Johns Hopkins University, Baltimore, MD, 21205, USA

    Michael C. Schubert

  4. Department of Physical Medicine and Rehabilitation, Johns Hopkins University, Baltimore, MD, 21205, USA

    Michael C. Schubert

  5. Department of Otolaryngology—Head and Neck Surgery, Johns Hopkins University, Baltimore, MD, 21205, USA

    Americo A. Migliaccio

Authors
  1. M. Muntaseer Mahfuz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael C. Schubert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William V. C. Figtree
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher J. Todd
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Americo A. Migliaccio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Americo A. Migliaccio.

Ethics declarations

Ethical Approval

Participation in this study was voluntary and subjects gave written informed consent before participating as approved by the University of New South Wales, Human Ethics Committee.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Muntaseer Mahfuz, M., Schubert, M.C., Figtree, W.V.C. et al. Human Vestibulo-Ocular Reflex Adaptation Training: Time Beats Quantity. JARO 19, 729–739 (2018). https://doi.org/10.1007/s10162-018-00689-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10162-018-00689-w

Keywords

Search

Navigation