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Published in: Journal of the Association for Research in Otolaryngology 1/2013

01-02-2013 | Research Article

Unilateral Adaptation of the Human Angular Vestibulo-Ocular Reflex

Authors: Americo A. Migliaccio, Michael C. Schubert

Published in: Journal of the Association for Research in Otolaryngology | Issue 1/2013

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Abstract

A recent study showed that the angular vestibulo-ocular reflex (VOR) can be better adaptively increased using an incremental retinal image velocity error signal compared with a conventional constant large velocity-gain demand (×2). This finding has important implications for vestibular rehabilitation that seeks to improve the VOR response after injury. However, a large portion of vestibular patients have unilateral vestibular hypofunction, and training that raises their VOR response during rotations to both the ipsilesional and contralesional side is not usually ideal. We sought to determine if the vestibular response to one side could selectively be increased without affecting the contralateral response. We tested nine subjects with normal vestibular function. Using the scleral search coil and head impulse techniques, we measured the active and passive VOR gain (eye velocity / head velocity) before and after unilateral incremental VOR adaptation training, consisting of self-generated (active) head impulses, which lasted ∼15 min. The head impulses consisted of rapid, horizontal head rotations with peak-amplitude 15 o, peak-velocity 150 o/s and peak-acceleration 3,000 o/s2. The VOR gain towards the adapting side increased after training from 0.92 ± 0.18 to 1.11 ± 0.22 (+22.7 ± 20.2 %) during active head impulses and from 0.91 ± 0.15 to 1.01 ± 0.17 (+11.3 ± 7.5 %) during passive head impulses. During active impulses, the VOR gain towards the non-adapting side also increased by ∼8 %, though this increase was ∼70 % less than to the adapting side. A similar increase did not occur during passive impulses. This study shows that unilateral vestibular adaptation is possible in humans with a normal VOR; unilateral incremental VOR adaptation may have a role in vestibular rehabilitation. The increase in passive VOR gain after active head impulse adaptation suggests that the training effect is robust.
Literature
go back to reference Aw ST, Haslwanter T, Halmagyi GM, Curthoys IS, Yavor RA, Todd MJ (1996) Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. I. Responses in normal subjects. J Neurophysiol 76:4009–4020PubMed Aw ST, Haslwanter T, Halmagyi GM, Curthoys IS, Yavor RA, Todd MJ (1996) Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. I. Responses in normal subjects. J Neurophysiol 76:4009–4020PubMed
go back to reference Babalian AL, Vidal PP (2000) Floccular modulation of vestibuloocular pathways and cerebellum-related plasticity: an in vitro whole brain study. J Neurophysiol 84:2514–2528PubMed Babalian AL, Vidal PP (2000) Floccular modulation of vestibuloocular pathways and cerebellum-related plasticity: an in vitro whole brain study. J Neurophysiol 84:2514–2528PubMed
go back to reference Belton T, McCrea RA (2004) Context contingent signal processing in the cerebellar flocculus and ventral paraflocculus during gaze saccades. J Neurophysiol 92:797–807PubMedCrossRef Belton T, McCrea RA (2004) Context contingent signal processing in the cerebellar flocculus and ventral paraflocculus during gaze saccades. J Neurophysiol 92:797–807PubMedCrossRef
go back to reference Blazquez PM, Hirata Y, Highstein SM (2006) Chronic changes in inputs to dorsal Y neurons accompany VOR motor learning. J Neurophysiol 95:1812–1825PubMedCrossRef Blazquez PM, Hirata Y, Highstein SM (2006) Chronic changes in inputs to dorsal Y neurons accompany VOR motor learning. J Neurophysiol 95:1812–1825PubMedCrossRef
go back to reference Cullen KE (2004) Sensory signals during active versus passive movement. Curr Opin Neurobiol 14:698–706PubMedCrossRef Cullen KE (2004) Sensory signals during active versus passive movement. Curr Opin Neurobiol 14:698–706PubMedCrossRef
go back to reference Diggle PJ, Liang KY, Zeger SL (1994) Analysis of longitudinal data. Oxford University Press, New York Diggle PJ, Liang KY, Zeger SL (1994) Analysis of longitudinal data. Oxford University Press, New York
go back to reference Galiana HL, Green AM (1998) Vestibular adaptation: how models can affect data interpretations. Otolaryngol Head Neck Surg 119:231–243PubMedCrossRef Galiana HL, Green AM (1998) Vestibular adaptation: how models can affect data interpretations. Otolaryngol Head Neck Surg 119:231–243PubMedCrossRef
go back to reference Gauthier GM, Robinson DA (1975) Adaptation of human’s vestibulo-ocular reflex to magnifying glasses. Brain Res 92:331–335PubMedCrossRef Gauthier GM, Robinson DA (1975) Adaptation of human’s vestibulo-ocular reflex to magnifying glasses. Brain Res 92:331–335PubMedCrossRef
go back to reference Gonshor A, Melvill Jones G (1976a) Short-term adaptive changes in the human vestibulo-ocular reflex arc. J Physiol 256:361–379 Gonshor A, Melvill Jones G (1976a) Short-term adaptive changes in the human vestibulo-ocular reflex arc. J Physiol 256:361–379
go back to reference Gonshor A, Melvill Jones G (1976b) Extreme vestibulo-ocular adaptation induced by prolonged optical reversal of vision. J Physiol 256:381–414 Gonshor A, Melvill Jones G (1976b) Extreme vestibulo-ocular adaptation induced by prolonged optical reversal of vision. J Physiol 256:381–414
go back to reference Halmagyi GM, Curthoys IS, Cremer PD, Henderson CJ, Todd MJ, Staples MJ, D'Cruz DM (1990) The human horizontal vestibulo-ocular reflex in response to high-acceleration stimulation before and after unilateral vestibular neurectomy. Exp Brain Res 81:479–490PubMedCrossRef Halmagyi GM, Curthoys IS, Cremer PD, Henderson CJ, Todd MJ, Staples MJ, D'Cruz DM (1990) The human horizontal vestibulo-ocular reflex in response to high-acceleration stimulation before and after unilateral vestibular neurectomy. Exp Brain Res 81:479–490PubMedCrossRef
go back to reference Haslwanter T (1995) Mathematics of three-dimensional eye rotations. Vis Res 35:1727–1739 Haslwanter T (1995) Mathematics of three-dimensional eye rotations. Vis Res 35:1727–1739
go back to reference Hullar TE, Minor LB (1999) High-frequency dynamics of regularly discharging canal afferents provide a linear signal for angular vestibuloocular reflexes. J Neurophysiol 82:2000–2005PubMed Hullar TE, Minor LB (1999) High-frequency dynamics of regularly discharging canal afferents provide a linear signal for angular vestibuloocular reflexes. J Neurophysiol 82:2000–2005PubMed
go back to reference Kagerer FA, Contreras-Vidal JL, Stelmach GE (1997) Adaptation to gradual as compared with sudden visuomotor distortions. Exp Brain Res 115:557–561PubMedCrossRef Kagerer FA, Contreras-Vidal JL, Stelmach GE (1997) Adaptation to gradual as compared with sudden visuomotor distortions. Exp Brain Res 115:557–561PubMedCrossRef
go back to reference Kilgard MP, Merzenich MM (2002) Order-sensitive plasticity in adult primary auditory cortex. Proc Natl Acad Sci USA 99:3205–3209PubMedCrossRef Kilgard MP, Merzenich MM (2002) Order-sensitive plasticity in adult primary auditory cortex. Proc Natl Acad Sci USA 99:3205–3209PubMedCrossRef
go back to reference Lisberger SG, Fuchs AF (1978) Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. J Neurophysiol 41:733–763PubMed Lisberger SG, Fuchs AF (1978) Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. J Neurophysiol 41:733–763PubMed
go back to reference Lisberger SG, Pavelko TA (1986) Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys. J Neurosci 6:346–354PubMed Lisberger SG, Pavelko TA (1986) Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys. J Neurosci 6:346–354PubMed
go back to reference 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 72:928–953PubMed 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 72:928–953PubMed
go back to reference 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 72:954–973PubMed 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 72:954–973PubMed
go back to reference Lisberger SG (1994) Neural basis for motor learning in the vestibulo-ocular reflex of primates. III Computational and behavioral analysis of the sites of learning. J Neurophysiol 72:974–999PubMed Lisberger SG (1994) Neural basis for motor learning in the vestibulo-ocular reflex of primates. III Computational and behavioral analysis of the sites of learning. J Neurophysiol 72:974–999PubMed
go back to reference McConville KM, Tomlinson RD, NA EQ (1996) Behavior of eye-movement-related cells in the vestibular nuclei during combined rotational and translational stimuli. J Neurophysiol 76:3136–3148PubMed McConville KM, Tomlinson RD, NA EQ (1996) Behavior of eye-movement-related cells in the vestibular nuclei during combined rotational and translational stimuli. J Neurophysiol 76:3136–3148PubMed
go back to reference 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 intra-axonal HRP injection in the alert cat. In: Fuchs A, Becker W (eds) Progress in oculomotor research. Elsevier/North Holland, Amsterdam, pp 379–386 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 intra-axonal HRP injection in the alert cat. In: Fuchs A, Becker W (eds) Progress in oculomotor research. Elsevier/North Holland, Amsterdam, pp 379–386
go back to reference McCrea RA, Luan H (2003) Signal processing of semicircular canal and otolith signals in the vestibular nuclei during passive and active head movements. Ann N Y Acad Sci 1004:169–182PubMedCrossRef McCrea RA, Luan H (2003) Signal processing of semicircular canal and otolith signals in the vestibular nuclei during passive and active head movements. Ann N Y Acad Sci 1004:169–182PubMedCrossRef
go back to reference Migliaccio AA, Todd MJ (1999) Real-time rotation vectors. Australas Phys Eng Sci Med 22:73–80PubMed Migliaccio AA, Todd MJ (1999) Real-time rotation vectors. Australas Phys Eng Sci Med 22:73–80PubMed
go back to reference Migliaccio AA, Minor LB, Carey JP (2004) Vergence-mediated modulation of the human horizontal vestibulo-ocular reflex is eliminated by a partial peripheral gentamicin lesion. Exp Brain Res 159:92–98PubMedCrossRef Migliaccio AA, Minor LB, Carey JP (2004) Vergence-mediated modulation of the human horizontal vestibulo-ocular reflex is eliminated by a partial peripheral gentamicin lesion. Exp Brain Res 159:92–98PubMedCrossRef
go back to reference Nagarajan S, Mahncke H, Salz T, Tallal P, Roberts T, Merzenich MM (1999) Cortical auditory signal processing in poor readers. Proc Natl Acad Sci USA 96:6483–6488PubMedCrossRef Nagarajan S, Mahncke H, Salz T, Tallal P, Roberts T, Merzenich MM (1999) Cortical auditory signal processing in poor readers. Proc Natl Acad Sci USA 96:6483–6488PubMedCrossRef
go back to reference 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 18:1559–1570PubMed 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 18:1559–1570PubMed
go back to reference Paige GD (1994) Senescence of human visual-vestibular interactions: smooth pursuit, optokinetic, and vestibular control of eye movements with aging. Exp Brain Res 98:355–372PubMedCrossRef Paige GD (1994) Senescence of human visual-vestibular interactions: smooth pursuit, optokinetic, and vestibular control of eye movements with aging. Exp Brain Res 98:355–372PubMedCrossRef
go back to reference Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29:467–492PubMed Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29:467–492PubMed
go back to reference Schubert MC, Della Santina CC, Shelhamer M (2008) Incremental angular vestibulo-ocular reflex adaptation to active head rotation. Exp Brain Res 191:435–446PubMedCrossRef Schubert MC, Della Santina CC, Shelhamer M (2008) Incremental angular vestibulo-ocular reflex adaptation to active head rotation. Exp Brain Res 191:435–446PubMedCrossRef
go back to reference Snyder LH, King WM (1996) Behavior and physiology of the macaque vestibulo-ocular reflex response to sudden off-axis rotation: computing eye translation. Brain Res Bull 40:293–301PubMedCrossRef Snyder LH, King WM (1996) Behavior and physiology of the macaque vestibulo-ocular reflex response to sudden off-axis rotation: computing eye translation. Brain Res Bull 40:293–301PubMedCrossRef
go back to reference Straumann D, Zee DS, Solomon D, Lasker AG, Roberts DC (1995) Transient torsion during and after saccades. Vision Res 35:3321–3334PubMedCrossRef Straumann D, Zee DS, Solomon D, Lasker AG, Roberts DC (1995) Transient torsion during and after saccades. Vision Res 35:3321–3334PubMedCrossRef
go back to reference Szturm T, Ireland DJ, Lessing-Turner M (1994) Comparison of different exercise programs in the rehabilitation of patients with chronic peripheral vestibular dysfunction. J Vestib Res 4:461–479PubMed Szturm T, Ireland DJ, Lessing-Turner M (1994) Comparison of different exercise programs in the rehabilitation of patients with chronic peripheral vestibular dysfunction. J Vestib Res 4:461–479PubMed
go back to reference Ushio M, Minor LB, Della Santina CC, Lasker DM (2011) Unidirectional rotations produce asymmetric changes in horizontal VOR gain before and after unilateral labyrinthectomy in macaques. Exp Brain Res 210:651–660PubMedCrossRef Ushio M, Minor LB, Della Santina CC, Lasker DM (2011) Unidirectional rotations produce asymmetric changes in horizontal VOR gain before and after unilateral labyrinthectomy in macaques. Exp Brain Res 210:651–660PubMedCrossRef
go back to reference Viirre E, Sitarz R (2002) Vestibular rehabilitation using visual displays: preliminary study. Laryngoscope 112:500–503PubMedCrossRef Viirre E, Sitarz R (2002) Vestibular rehabilitation using visual displays: preliminary study. Laryngoscope 112:500–503PubMedCrossRef
Metadata
Title
Unilateral Adaptation of the Human Angular Vestibulo-Ocular Reflex
Authors
Americo A. Migliaccio
Michael C. Schubert
Publication date
01-02-2013
Publisher
Springer-Verlag
Published in
Journal of the Association for Research in Otolaryngology / Issue 1/2013
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-012-0359-7

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