Skip to main content
Top
Published in: Journal of the Association for Research in Otolaryngology 3/2010

Open Access 01-09-2010

Peaks and Troughs of Three-Dimensional Vestibulo-ocular Reflex in Humans

Authors: Janine Goumans, Mark M. J. Houben, Joyce Dits, Johannes van der Steen

Published in: Journal of the Association for Research in Otolaryngology | Issue 3/2010

Login to get access

Abstract

The three-dimensional vestibulo-ocular reflex (3D VOR) ideally generates compensatory ocular rotations not only with a magnitude equal and opposite to the head rotation but also about an axis that is collinear with the head rotation axis. Vestibulo-ocular responses only partially fulfill this ideal behavior. Because animal studies have shown that vestibular stimulation about particular axes may lead to suboptimal compensatory responses, we investigated in healthy subjects the peaks and troughs in 3D VOR stabilization in terms of gain and alignment of the 3D vestibulo-ocular response. Six healthy upright sitting subjects underwent whole body small amplitude sinusoidal and constant acceleration transients delivered by a six-degree-of-freedom motion platform. Subjects were oscillated about the vertical axis and about axes in the horizontal plane varying between roll and pitch at increments of 22.5° in azimuth. Transients were delivered in yaw, roll, and pitch and in the vertical canal planes. Eye movements were recorded in with 3D search coils. Eye coil signals were converted to rotation vectors, from which we calculated gain and misalignment. During horizontal axis stimulation, systematic deviations were found. In the light, misalignment of the 3D VOR had a maximum misalignment at about 45°. These deviations in misalignment can be explained by vector summation of the eye rotation components with a low gain for torsion and high gain for vertical. In the dark and in response to transients, gain of all components had lower values. Misalignment in darkness and for transients had different peaks and troughs than in the light: its minimum was during pitch axis stimulation and its maximum during roll axis stimulation. We show that the relatively large misalignment for roll in darkness is due to a horizontal eye movement component that is only present in darkness. In combination with the relatively low torsion gain, this horizontal component has a relative large effect on the alignment of the eye rotation axis with respect to the head rotation axis.
Appendix
Available only for authorised users
Literature
go back to reference Angelaki DE, Dickman JD (2003) Gravity or translation: central processing of vestibular signals to detect motion or tilt. J Vestib Res 13:245–253PubMed Angelaki DE, Dickman JD (2003) Gravity or translation: central processing of vestibular signals to detect motion or tilt. J Vestib Res 13:245–253PubMed
go back to reference Angelaki DE, Cullen KE (2008) Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31:125–150CrossRefPubMed Angelaki DE, Cullen KE (2008) Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31:125–150CrossRefPubMed
go back to reference Aw ST, Halmagyi GM, Haslwanter T, Curthoys IS, Yavor RA, Todd MJ (1996a) Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. II. Responses in subjects with unilateral vestibular loss and selective semicircular canal occlusion. J Neurophysiol 76:4021–4030PubMed Aw ST, Halmagyi GM, Haslwanter T, Curthoys IS, Yavor RA, Todd MJ (1996a) Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. II. Responses in subjects with unilateral vestibular loss and selective semicircular canal occlusion. J Neurophysiol 76:4021–4030PubMed
go back to reference Aw ST, Haslwanter T, Halmagyi GM, Curthoys IS, Yavor RA, Todd MJ (1996b) 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 (1996b) 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 Bockisch CJ, Straumann D, Haslwanter T (2005) Human 3-D aVOR with and without otolith stimulation. Exp Brain Res 161:358–367CrossRefPubMed Bockisch CJ, Straumann D, Haslwanter T (2005) Human 3-D aVOR with and without otolith stimulation. Exp Brain Res 161:358–367CrossRefPubMed
go back to reference Bruno P, Van den Berg AV (1997) Torsion during saccades between tertiary positions. Exp Brain Res 117:251–265CrossRefPubMed Bruno P, Van den Berg AV (1997) Torsion during saccades between tertiary positions. Exp Brain Res 117:251–265CrossRefPubMed
go back to reference Crane BT, Demer JL (1997) Human gaze stabilization during natural activities: translation, rotation, magnification, and target distance effects. J Neurophysiol 78:2129–2144PubMed Crane BT, Demer JL (1997) Human gaze stabilization during natural activities: translation, rotation, magnification, and target distance effects. J Neurophysiol 78:2129–2144PubMed
go back to reference Crane BT, Tian JR, Demer JL (2005) Human angular vestibulo-ocular reflex initiation: relationship to Listing’s law. Ann N Y Acad Sci 1039:26–35CrossRefPubMed Crane BT, Tian JR, Demer JL (2005) Human angular vestibulo-ocular reflex initiation: relationship to Listing’s law. Ann N Y Acad Sci 1039:26–35CrossRefPubMed
go back to reference Crane BT, Tian J, Demer JL (2006) Temporal dynamics of ocular position dependence of the initial human vestibulo-ocular reflex. Invest Ophthalmol Vis Sci 47:1426–1438CrossRefPubMed Crane BT, Tian J, Demer JL (2006) Temporal dynamics of ocular position dependence of the initial human vestibulo-ocular reflex. Invest Ophthalmol Vis Sci 47:1426–1438CrossRefPubMed
go back to reference Crawford JD, Vilis T (1991) Axes of eye rotation and Listing’s law during rotations of the head. J Neurophysiol 65:407–423PubMed Crawford JD, Vilis T (1991) Axes of eye rotation and Listing’s law during rotations of the head. J Neurophysiol 65:407–423PubMed
go back to reference Cremer PD, Halmagyi GM, Aw ST, Curthoys IS, McGarvie LA, Todd MJ, Black RA, Hannigan IP (1998) Semicircular canal plane head impulses detect absent function of individual semicircular canals. Brain 121(Pt 4):699–716CrossRefPubMed Cremer PD, Halmagyi GM, Aw ST, Curthoys IS, McGarvie LA, Todd MJ, Black RA, Hannigan IP (1998) Semicircular canal plane head impulses detect absent function of individual semicircular canals. Brain 121(Pt 4):699–716CrossRefPubMed
go back to reference Della Santina CC, Potyagaylo V, Migliaccio AA, Minor LB, Carey JP (2005) Orientation of human semicircular canals measured by three-dimensional multiplanar CT reconstruction. J Assoc Res Otolaryngol 6:191–206CrossRefPubMed Della Santina CC, Potyagaylo V, Migliaccio AA, Minor LB, Carey JP (2005) Orientation of human semicircular canals measured by three-dimensional multiplanar CT reconstruction. J Assoc Res Otolaryngol 6:191–206CrossRefPubMed
go back to reference Demer JL, Crane BT, Tian JR (2005) Human angular vestibulo-ocular reflex axis disconjugacy: relationship to magnetic resonance imaging evidence of globe translation. Ann N Y Acad Sci 1039:15–25CrossRefPubMed Demer JL, Crane BT, Tian JR (2005) Human angular vestibulo-ocular reflex axis disconjugacy: relationship to magnetic resonance imaging evidence of globe translation. Ann N Y Acad Sci 1039:15–25CrossRefPubMed
go back to reference Ferman L, Collewijn H, Jansen TC, Van den Berg AV (1987) Human gaze stability in the horizontal, vertical and torsional direction during voluntary head movements, evaluated with a three-dimensional scleral induction coil technique. Vision Res 27:811–828CrossRefPubMed Ferman L, Collewijn H, Jansen TC, Van den Berg AV (1987) Human gaze stability in the horizontal, vertical and torsional direction during voluntary head movements, evaluated with a three-dimensional scleral induction coil technique. Vision Res 27:811–828CrossRefPubMed
go back to reference Groen E, Bos JE, de Graaf B (1999) Contribution of the otoliths to the human torsional vestibulo-ocular reflex. J Vestib Res 9:27–36PubMed Groen E, Bos JE, de Graaf B (1999) Contribution of the otoliths to the human torsional vestibulo-ocular reflex. J Vestib Res 9:27–36PubMed
go back to reference Grossman GE, Leigh RJ, Abel LA, Lanska DJ, Thurston SE (1988) Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 70:470–476CrossRefPubMed Grossman GE, Leigh RJ, Abel LA, Lanska DJ, Thurston SE (1988) Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 70:470–476CrossRefPubMed
go back to reference Grossman GE, Leigh RJ, Bruce EN, Huebner WP, Lanska DJ (1989) Performance of the human vestibuloocular reflex during locomotion. J Neurophysiol 62:264–272PubMed Grossman GE, Leigh RJ, Bruce EN, Huebner WP, Lanska DJ (1989) Performance of the human vestibuloocular reflex during locomotion. J Neurophysiol 62:264–272PubMed
go back to reference Halmagyi GM, Aw ST, Cremer PD, Curthoys IS, Todd MJ (2001) Impulsive testing of individual semicircular canal function. Ann N Y Acad Sci 942:192–200CrossRefPubMed Halmagyi GM, Aw ST, Cremer PD, Curthoys IS, Todd MJ (2001) Impulsive testing of individual semicircular canal function. Ann N Y Acad Sci 942:192–200CrossRefPubMed
go back to reference Halmagyi GM, Black RA, Thurtell MJ, Curthoys IS (2003) The human horizontal vestibulo-ocular reflex in response to active and passive head impulses after unilateral vestibular deafferentation. Ann N Y Acad Sci 1004:325–336CrossRefPubMed Halmagyi GM, Black RA, Thurtell MJ, Curthoys IS (2003) The human horizontal vestibulo-ocular reflex in response to active and passive head impulses after unilateral vestibular deafferentation. Ann N Y Acad Sci 1004:325–336CrossRefPubMed
go back to reference Haslwanter T, Moore ST (1995) A theoretical analysis of three-dimensional eye position measurement using polar cross-correlation. IEEE Trans Biomed Eng 42:1053–1061CrossRefPubMed Haslwanter T, Moore ST (1995) A theoretical analysis of three-dimensional eye position measurement using polar cross-correlation. IEEE Trans Biomed Eng 42:1053–1061CrossRefPubMed
go back to reference Haustein W (1989) Considerations on Listing’s law and the primary position by means of a matrix description of eye position control. Biol Cybern 60:411–420CrossRefPubMed Haustein W (1989) Considerations on Listing’s law and the primary position by means of a matrix description of eye position control. Biol Cybern 60:411–420CrossRefPubMed
go back to reference Houben MMJ, Goumans J, Dejongste AH, Van der Steen J (2005) Angular and linear vestibulo-ocular responses in humans. Ann N Y Acad Sci 1039:68–80CrossRefPubMed Houben MMJ, Goumans J, Dejongste AH, Van der Steen J (2005) Angular and linear vestibulo-ocular responses in humans. Ann N Y Acad Sci 1039:68–80CrossRefPubMed
go back to reference Houben MMJ, Goumans J, Van der Steen J (2006) Recording three-dimensional eye movements: scleral search coils versus video oculography. Invest Ophthalmol Vis Sci 47:179–187CrossRefPubMed Houben MMJ, Goumans J, Van der Steen J (2006) Recording three-dimensional eye movements: scleral search coils versus video oculography. Invest Ophthalmol Vis Sci 47:179–187CrossRefPubMed
go back to reference Ito M, Nisimaru N, Yamamoto M (1976) Pathways for the vestibulo-ocular reflex excitation arising from semicircular canals of rabbits. Exp Brain Res 24:257–271PubMed Ito M, Nisimaru N, Yamamoto M (1976) Pathways for the vestibulo-ocular reflex excitation arising from semicircular canals of rabbits. Exp Brain Res 24:257–271PubMed
go back to reference Merfeld DM (1995) Modeling human vestibular responses during eccentric rotation and off vertical axis rotation. Acta Otolaryngol Suppl 520(Pt 2):354–359CrossRefPubMed Merfeld DM (1995) Modeling human vestibular responses during eccentric rotation and off vertical axis rotation. Acta Otolaryngol Suppl 520(Pt 2):354–359CrossRefPubMed
go back to reference Merfeld DM, Park S, Gianna-Poulin C, Black FO, Wood S (2005) Vestibular perception and action employ qualitatively different mechanisms. II. VOR and perceptual responses during combined Tilt&Translation. J Neurophysiol 94:199–205CrossRefPubMed Merfeld DM, Park S, Gianna-Poulin C, Black FO, Wood S (2005) Vestibular perception and action employ qualitatively different mechanisms. II. VOR and perceptual responses during combined Tilt&Translation. J Neurophysiol 94:199–205CrossRefPubMed
go back to reference Migliaccio AA, Schubert MC, Jiradejvong P, Lasker DM, Clendaniel RA, Minor LB (2004) The three-dimensional vestibulo-ocular reflex evoked by high-acceleration rotations in the squirrel monkey. Exp Brain Res 159:433–446CrossRefPubMed Migliaccio AA, Schubert MC, Jiradejvong P, Lasker DM, Clendaniel RA, Minor LB (2004) The three-dimensional vestibulo-ocular reflex evoked by high-acceleration rotations in the squirrel monkey. Exp Brain Res 159:433–446CrossRefPubMed
go back to reference Misslisch H, Hess BJ (2000) Three-dimensional vestibuloocular reflex of the monkey: optimal retinal image stabilization versus Listing’s law. J Neurophysiol 83:3264–3276PubMed Misslisch H, Hess BJ (2000) Three-dimensional vestibuloocular reflex of the monkey: optimal retinal image stabilization versus Listing’s law. J Neurophysiol 83:3264–3276PubMed
go back to reference Misslisch H, Tweed D (2000) Torsional dynamics and cross-coupling in the human vestibulo-ocular reflex during active head rotation. J Vestib Res 10:119–125PubMed Misslisch H, Tweed D (2000) Torsional dynamics and cross-coupling in the human vestibulo-ocular reflex during active head rotation. J Vestib Res 10:119–125PubMed
go back to reference Misslisch H, Tweed D, Fetter M, Sievering D, Koenig E (1994) Rotational kinematics of the human vestibuloocular reflex. III. Listing’s law. J Neurophysiol 72:2490–2502PubMed Misslisch H, Tweed D, Fetter M, Sievering D, Koenig E (1994) Rotational kinematics of the human vestibuloocular reflex. III. Listing’s law. J Neurophysiol 72:2490–2502PubMed
go back to reference Paige GD (1991) Linear vestibulo-ocular reflex (LVOR) and modulation by vergence. Acta Otolaryngol Suppl 481:282–286CrossRefPubMed Paige GD (1991) Linear vestibulo-ocular reflex (LVOR) and modulation by vergence. Acta Otolaryngol Suppl 481:282–286CrossRefPubMed
go back to reference Paige GD, Seidman SH (1999) Characteristics of the VOR in response to linear acceleration. Ann N Y Acad Sci 871:123–135CrossRefPubMed Paige GD, Seidman SH (1999) Characteristics of the VOR in response to linear acceleration. Ann N Y Acad Sci 871:123–135CrossRefPubMed
go back to reference Roy FD, Tomlinson RD (2004) Characterization of the vestibulo-ocular reflex evoked by high-velocity movements. Laryngoscope 114:1190–1193CrossRefPubMed Roy FD, Tomlinson RD (2004) Characterization of the vestibulo-ocular reflex evoked by high-velocity movements. Laryngoscope 114:1190–1193CrossRefPubMed
go back to reference Schmid-Priscoveanu A, Straumann D, Kori AA (2000) Torsional vestibulo-ocular reflex during whole-body oscillation in the upright and the supine position. I. Responses in healthy human subjects. Exp Brain Res 134:212–219CrossRefPubMed Schmid-Priscoveanu A, Straumann D, Kori AA (2000) Torsional vestibulo-ocular reflex during whole-body oscillation in the upright and the supine position. I. Responses in healthy human subjects. Exp Brain Res 134:212–219CrossRefPubMed
go back to reference Seidman SH, Leigh RJ (1989) The human torsional vestibulo-ocular reflex during rotation about an earth-vertical axis. Brain Res 504:264–268CrossRefPubMed Seidman SH, Leigh RJ (1989) The human torsional vestibulo-ocular reflex during rotation about an earth-vertical axis. Brain Res 504:264–268CrossRefPubMed
go back to reference Seidman SH, Leigh RJ, Tomsak RL, Grant MP, Dell'Osso LF (1995) Dynamic properties of the human vestibulo-ocular reflex during head rotations in roll. Vision Res 35:679–689CrossRefPubMed Seidman SH, Leigh RJ, Tomsak RL, Grant MP, Dell'Osso LF (1995) Dynamic properties of the human vestibulo-ocular reflex during head rotations in roll. Vision Res 35:679–689CrossRefPubMed
go back to reference Simpson JI, Graf W (1985) The selection of reference frames by nature and its investigators. Rev Oculomot Res 1:3–16PubMed Simpson JI, Graf W (1985) The selection of reference frames by nature and its investigators. Rev Oculomot Res 1:3–16PubMed
go back to reference Tabak S, Collewijn H (1994) Human vestibulo-ocular responses to rapid, helmet-driven head movements. Exp Brain Res 102:367–378CrossRefPubMed Tabak S, Collewijn H (1994) Human vestibulo-ocular responses to rapid, helmet-driven head movements. Exp Brain Res 102:367–378CrossRefPubMed
go back to reference Tabak S, Collewijn H (1995) Evaluation of the human vestibulo-ocular reflex at high frequencies with a helmet, driven by reactive torque. Acta Otolaryngol Suppl 520(Pt 1):4–8CrossRefPubMed Tabak S, Collewijn H (1995) Evaluation of the human vestibulo-ocular reflex at high frequencies with a helmet, driven by reactive torque. Acta Otolaryngol Suppl 520(Pt 1):4–8CrossRefPubMed
go back to reference Tabak S, Collewijn H, Boumans LJ, van der Steen J (1997a) Gain and delay of human vestibulo-ocular reflexes to oscillation and steps of the head by a reactive torque helmet. I. Normal subjects. Acta Otolaryngol 117:785–795CrossRefPubMed Tabak S, Collewijn H, Boumans LJ, van der Steen J (1997a) Gain and delay of human vestibulo-ocular reflexes to oscillation and steps of the head by a reactive torque helmet. I. Normal subjects. Acta Otolaryngol 117:785–795CrossRefPubMed
go back to reference Tabak S, Collewijn H, Boumans LJ, van der Steen J (1997b) Gain and delay of human vestibulo-ocular reflexes to oscillation and steps of the head by a reactive torque helmet. II. Vestibular-deficient subjects. Acta Otolaryngol 117:796–809CrossRefPubMed Tabak S, Collewijn H, Boumans LJ, van der Steen J (1997b) Gain and delay of human vestibulo-ocular reflexes to oscillation and steps of the head by a reactive torque helmet. II. Vestibular-deficient subjects. Acta Otolaryngol 117:796–809CrossRefPubMed
go back to reference Tweed D, Sievering D, Misslisch H, Fetter M, Zee D, Koenig E (1994) Rotational kinematics of the human vestibuloocular reflex. I. Gain matrices. J Neurophysiol 72:2467–2479PubMed Tweed D, Sievering D, Misslisch H, Fetter M, Zee D, Koenig E (1994) Rotational kinematics of the human vestibuloocular reflex. I. Gain matrices. J Neurophysiol 72:2467–2479PubMed
go back to reference Van der Steen J, Collewijn H (1984) Ocular stability in the horizontal, frontal and sagittal planes in the rabbit. Exp Brain Res 56:263–274CrossRefPubMed Van der Steen J, Collewijn H (1984) Ocular stability in the horizontal, frontal and sagittal planes in the rabbit. Exp Brain Res 56:263–274CrossRefPubMed
go back to reference Van der Steen J, Simpson JI, Tan J (1994) Functional and anatomic organization of three-dimensional eye movements in rabbit cerebellar flocculus. J Neurophysiol 72:31–46PubMed Van der Steen J, Simpson JI, Tan J (1994) Functional and anatomic organization of three-dimensional eye movements in rabbit cerebellar flocculus. J Neurophysiol 72:31–46PubMed
go back to reference Yakushin SB, Xiang Y, Cohen B, Raphan T (2009) Dependence of the roll angular vestibuloocular reflex (aVOR) on gravity. J Neurophysiol 102:2616–2626CrossRefPubMed Yakushin SB, Xiang Y, Cohen B, Raphan T (2009) Dependence of the roll angular vestibuloocular reflex (aVOR) on gravity. J Neurophysiol 102:2616–2626CrossRefPubMed
go back to reference Zupan LH, Merfeld DM (2005) An internal model of head kinematics predicts the influence of head orientation on reflexive eye movements. J Neural Eng 2:S180–S197CrossRefPubMed Zupan LH, Merfeld DM (2005) An internal model of head kinematics predicts the influence of head orientation on reflexive eye movements. J Neural Eng 2:S180–S197CrossRefPubMed
Metadata
Title
Peaks and Troughs of Three-Dimensional Vestibulo-ocular Reflex in Humans
Authors
Janine Goumans
Mark M. J. Houben
Joyce Dits
Johannes van der Steen
Publication date
01-09-2010
Publisher
Springer-Verlag
Published in
Journal of the Association for Research in Otolaryngology / Issue 3/2010
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-010-0210-y

Other articles of this Issue 3/2010

Journal of the Association for Research in Otolaryngology 3/2010 Go to the issue