Abstract
The vestibular system is vital for motor control and spatial self-motion perception. Afferents from the otolith organs and the semicircular canals converge with optokinetic, somatosensory and motor-related signals in the vestibular nuclei, which are reciprocally interconnected with the vestibulocerebellar cortex and deep cerebellar nuclei. Here, we review the properties of the many cell types in the vestibular nuclei, as well as some fundamental computations implemented within this brainstem–cerebellar circuitry. These include the sensorimotor transformations for reflex generation, the neural computations for inertial motion estimation, the distinction between active and passive head movements, as well as the integration of vestibular and proprioceptive information for body motion estimation. A common theme in the solution to such computational problems is the concept of internal models and their neural implementation. Recent studies have shed new insights into important organizational principles that closely resemble those proposed for other sensorimotor systems, where their neural basis has often been more difficult to identify. As such, the vestibular system provides an excellent model to explore common neural processing strategies relevant both for reflexive and for goal-directed, voluntary movement as well as perception.
Similar content being viewed by others
Abbreviations
- VOR:
-
Vestibulo-ocular reflex
- RVOR:
-
Rotational vestibulo-ocular reflex
- TVOR:
-
Translational vestibulo-ocular reflex
- VN:
-
Vestibular nuclei
- PH:
-
Prepositus hypoglossi
- rFN:
-
Rostral fastigial deep cerebellar nuclei
- NU:
-
Nodulus and ventral uvula regions of the caudal cerebellar vermis
- PH–BT:
-
“Tonic” and “burst-tonic” neurons in the PH and adjacent medial VN
- PVP:
-
“Position-vestibular-pause” VN cell type
- EH:
-
“Eye-head” VN cell type
- VO:
-
“Vestibular-only” VN cell type
- FTN:
-
“Floccular-target-neuron” VN cell type
References
Ajemian R, Green A, Bullock D, Sergio L, Kalaska J, Grossberg S (2008) Assessing the function of motor cortex: single-neuron models of how neural response is modulated by limb biomechanics. Neuron 58:414–428
Allum JH, Honegger F (1998) Interactions between vestibular and proprioceptive inputs triggering and modulating human balance-correcting responses differ across muscles. Exp Brain Res 121:478–494
Andersen RA (1997) Multimodal integration for the representation of space in the posterior parietal cortex. Philos Trans R Soc Lond B Biol Sci 352:1421–1428
Angelaki DE (1998) Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. III. Responses to translation. J Neurophysiol 80:680–695
Angelaki DE (2004) Eyes on target: what neurons must do for the vestibuloocular reflex during linear motion. J Neurophysiol 92:20–35
Angelaki DE, Cullen KE (2008) Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31:125–150
Angelaki DE, Hess BJ (1994) Inertial representation of angular motion in the vestibular system of rhesus monkeys. I. Vestibuloocular reflex. J Neurophysiol 71:1222–1249
Angelaki DE, Hess BJ (1995) Inertial representation of angular motion in the vestibular system of rhesus monkeys. II. Otolith-controlled transformation that depends on an intact cerebellar nodulus. J Neurophysiol 73:1729–1751
Angelaki DE, Hess BJ (2005) Self-motion-induced eye movements: effects on visual acuity and navigation. Nat Rev Neurosci 6:966–976
Angelaki DE, Hess BJ, Arai Y, Suzuki J (1996) Adaptation of primate vestibuloocular reflex to altered peripheral vestibular inputs. I. Frequency-specific recovery of horizontal VOR after inactivation of the lateral semicircular canals. J Neurophysiol 76:2941–2953
Angelaki DE, McHenry MQ, Dickman JD, Newlands SD, Hess BJ (1999) Computation of inertial motion: neural strategies to resolve ambiguous otolith information. J Neurosci 19:316–327
Angelaki DE, Green AM, Dickman JD (2001) Differential sensorimotor processing of vestibulo-ocular signals during rotation and translation. J Neurosci 21:3968–3985
Angelaki DE, Shaikh AG, Green AM, Dickman JD (2004) Neurons compute internal models of the physical laws of motion. Nature 430:560–564
Angelaki DE, Gu Y, DeAngelis GC (2009) Multisensory integration: psychophysics, neurophysiology, and computation. Curr Opin Neurobiol 19(4):452–458
Angelaki DE, Klier EM, Snyder LH (2010) A vestibular sensation: probabilistic approaches to spatial perception. Neuron (in press)
Arnold DB, Robinson DA (1991) A learning network model of the neural integrator of the oculomotor system. Biol Cybern 64:447–454
Baker R, Berthoz A (1975) Is the prepositus hypoglossi nucleus the source of another vestibulo-ocular pathway? Brain Res 86:121–127
Balaban CD, Porter JD (1998) Neuroanatomic substrates for vestibulo-autonomic interactions. J Vestib Res 8:7–16
Barmack NH (2003) Central vestibular system: vestibular nuclei and posterior cerebellum. Brain Res Bull 60:511–541
Barmack NH, Shojaku H (1995) Vestibular and visual climbing fiber signals evoked in the uvula-nodulus of the rabbit cerebellum by natural stimulation. J Neurophysiol 74:2573–2589
Barnes GR (1993) Visual-vestibular interaction in the control of head and eye movement: the role of visual feedback and predictive mechanisms. Prog Neurobiol 41:435–472
Batista AP, Santhanam G, Yu BM, Ryu SI, Afshar A, Shenoy KV (2007) Reference frames for reach planning in macaque dorsal premotor cortex. J Neurophysiol 98:966–983
Belknap DB, McCrea RA (1988) Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey. J Comp Neurol 268:13–28
Bell CC (1981) An efference copy which is modified by reafferent input. Science 214:450–453
Bell CC, Han V, Sawtell NB (2008) Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci 31:1–24
Bent LR, McFadyen BJ, Inglis JT (2005) Vestibular contributions during human locomotor tasks. Exerc Sport Sci Rev 33:107–113
Berthoz A, Israel I, Georges-Francois P, Grasso R, Tsuzuku T (1995) Spatial memory of body linear displacement: what is being stored? Science 269:95–98
Blazquez PM, Hirata Y, Highstein SM (2004) The vestibulo-ocular reflex as a model system for motor learning: what is the role of the cerebellum? Cerebellum 3:188–192
Blohm G, Keith GP, Crawford JD (2009) Decoding the cortical transformations for visually guided reaching in 3D space. Cereb Cortex 19:1372–1393
Blouin J, Teasdale N, Mouchnino L (2007) Vestibular signal processing in a subject with somatosensory deafferentation: the case of sitting posture. BMC Neurol 7:25
Bockisch CJ, Haslwanter T (2007) Vestibular contribution to the planning of reach trajectories. Exp Brain Res 182:387–397
Bos JE, Bles W (2002) Theoretical considerations on canal-otolith interaction and an observer model. Biol Cybern 86:191–207
Boyden ES, Katoh A, Raymond JL (2004) Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu Rev Neurosci 27:581–609
Boyle R, Pompeiano O (1980) Responses of vestibulospinal neurons to sinusoidal rotation of neck. J Neurophysiol 44:633–649
Boyle R, Pompeiano O (1981) Convergence and interaction of neck and macular vestibular inputs on vestibulospinal neurons. J Neurophysiol 45:852–868
Boyle R, Buttner U, Markert G (1985) Vestibular nuclei activity and eye movements in the alert monkey during sinusoidal optokinetic stimulation. Exp Brain Res 57:362–369
Boyle R, Belton T, McCrea RA (1996) Responses of identified vestibulospinal neurons to voluntary eye and head movements in the squirrel monkey. Ann N Y Acad Sci 781:244–263
Brandt T, Schautzer F, Hamilton DA, Bruning R, Markowitsch HJ, Kalla R, Darlington C, Smith P, Strupp M (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128:2732–2741
Bremmer F (2005) Navigation in space—the role of the macaque ventral intraparietal area. J Physiol 566:29–35
Bresciani JP, Gauthier GM, Vercher JL, Blouin J (2005) On the nature of the vestibular control of arm-reaching movements during whole-body rotations. Exp Brain Res 164:431–441
Brooks J, Cullen KE (2007) Reference frames and reafference in the rostral fastigial nucleus. Soc Neurosci Abstr 33
Brooks JX, Cullen KE (2009) Multimodal integration in rostral fastigial nucleus provides an estimate of body movement. J Neurosci 29:10499–10511
Bruschini L, Andre P, Pompeiano O, Manzoni D (2006) Responses of Purkinje-cells of the cerebellar anterior vermis to stimulation of vestibular and somatosensory receptors. Neuroscience 142:235–245
Bryan AS, Angelaki DE (2009) Optokinetic and vestibular responsiveness in the macaque rostral vestibular and fastigial nuclei. J Neurophysiol 101:714–720
Buchanan JJ, Horak FB (2001) Vestibular loss disrupts control of head and trunk on a sinusoidally moving platform. J Vestib Res 11:371–389
Buettner UW, Henn V, Young LR (1981) Frequency response of the vestibulo-ocular reflex (VOR) in the monkey. Aviat Space Environ Med 52:73–77
Buneo CA, Andersen RA (2006) The posterior parietal cortex: sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 44:2594–2606
Buneo CA, Soechting JF, Flanders M (1997) Postural dependence of muscle actions: implications for neural control. J Neurosci 17:2128–2142
Buttner U, Fuchs AF, Markert-Schwab G, Buckmaster P (1991) Fastigial nucleus activity in the alert monkey during slow eye and head movements. J Neurophysiol 65:1360–1371
Buttner-Ennever JA, Horn AK, Schmidtke K (1989) Cell groups of the medial longitudinal fasciculus and paramedian tracts. Rev Neurol (Paris) 145:533–539
Cannon SC, Robinson DA (1985) An improved neural-network model for the neural integrator of the oculomotor system: more realistic neuron behavior. Biol Cybern 53:93–108
Cannon SC, Robinson DA (1987) Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J Neurophysiol 57:1383–1409
Cannon SC, Robinson DA, Shamma S (1983) A proposed neural network for the integrator of the oculomotor system. Biol Cybern 49:127–136
Cathers I, Day BL, Fitzpatrick RC (2005) Otolith and canal reflexes in human standing. J Physiol 563:229–234
Chen-Harris H, Joiner WM, Ethier V, Zee DS, Shadmehr R (2008) Adaptive control of saccades via internal feedback. J Neurosci 28:2804–2813
Chen-Huang C, McCrea RA (1999a) Effects of viewing distance on the responses of horizontal canal-related secondary vestibular neurons during angular head rotation. J Neurophysiol 81:2517–2537
Chen-Huang C, McCrea RA (1999b) Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation. J Neurophysiol 81:2538–2557
Chubb MC, Fuchs AF, Scudder CA (1984) Neuron activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements. J Neurophysiol 52:724–742
Cohen B, Matsuo V, Raphan T (1977) Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. J Physiol 270:321–344
Cohen B, Henn V, Raphan T, Dennett D (1981) Velocity storage, nystagmus, and visual-vestibular interactions in humans. Ann N Y Acad Sci 374:421–433
Cothros N, Wong JD, Gribble PL (2006) Are there distinct neural representations of object and limb dynamics? Exp Brain Res 173:689–697
Cova AC, Galiana HL (1996) A bilateral model integrating vergence and the vestibulo-ocular reflex. Exp Brain Res 107:435–452
Cullen KE, McCrea RA (1993) Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex. I. Secondary vestibular neurons. J Neurophysiol 70:828–843
Cullen KE, Minor LB (2002) Semicircular canal afferents similarly encode active and passive head-on-body rotations: implications for the role of vestibular efference. J Neurosci 22:RC226
Cullen KE, Roy JE (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91:1919–1933
Cullen KE, Chen-Huang C, McCrea RA (1993) Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex. II. Eye movement related neurons. J Neurophysiol 70:844–856
Curthoys IS, Halmagyi GM (1995) Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss. J Vestib Res 5:67–107
Curthoys IS, Halmagyi GM, Dai MJ (1991) The acute effects of unilateral vestibular neurectomy on sensory and motor tests of human otolithic function. Acta Otolaryngol Suppl 481:5–10
Dai MJ, Raphan T, Cohen B (1991) Spatial orientation of the vestibular system: dependence of optokinetic after-nystagmus on gravity. J Neurophysiol 66:1422–1439
Day BL, Fitzpatrick RC (2005) Virtual head rotation reveals a process of route reconstruction from human vestibular signals. J Physiol 567:591–597
Decety J (1996) Neural representations for action. Rev Neurosci 7:285–297
Deliagina TG, Beloozerova IN, Zelenin PV, Orlovsky GN (2008) Spinal and supraspinal postural networks. Brain Res Rev 57:212–221
Demer JL, Oh SY, Poukens V (2000) Evidence for active control of rectus extraocular muscle pulleys. Invest Ophthalmol Vis Sci 41:1280–1290
Dieterich M (2007) Central vestibular disorders. J Neurol 254:559–568
DiZio P, Lackner JR (2001) Coriolis-force-induced trajectory and endpoint deviations in the reaching movements of labyrinthine-defective subjects. J Neurophysiol 85:784–789
Driver J, Noesselt T (2008) Multisensory interplay reveals crossmodal influences on ‘sensory-specific’ brain regions, neural responses, and judgments. Neuron 57:11–23
du Lac S, Raymond JL, Sejnowski TJ, Lisberger SG (1995) Learning and memory in the vestibulo-ocular reflex. Annu Rev Neurosci 18:409–441
Einstein A (1908) Uber das Relativitätsprinzip und die aus demselben gezogenen Folgerungen. Jahrb Radioakt 4:411–462
Escudero M, de la Cruz RR, Delgado-Garcia JM (1992) A physiological study of vestibular and prepositus hypoglossi neurones projecting to the abducens nucleus in the alert cat. J Physiol 458:539–560
Escudero M, Cheron G, Godaux E (1996) Discharge properties of brain stem neurons projecting to the flocculus in the alert cat. II. Prepositus hypoglossal nucleus. J Neurophysiol 76:1775–1785
Ethier V, Zee DS, Shadmehr R (2008) Changes in control of saccades during gain adaptation. J Neurosci 28:13929–13937
Farrer C, Franck N, Paillard J, Jeannerod M (2003) The role of proprioception in action recognition. Conscious Cogn 12:609–619
Fernandez C, Goldberg JM (1976a) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J Neurophysiol 39:970–984
Fernandez C, Goldberg JM (1976b) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. J Neurophysiol 39:996–1008
Fukushima K (1997) Corticovestibular interactions: anatomy, electrophysiology, and functional considerations. Exp Brain Res 117:1–16
Galiana HL (1991) A nystagmus strategy to linearize the vestibulo-ocular reflex. IEEE Trans Biomed Eng 38:532–543
Galiana HL, Outerbridge JS (1984) A bilateral model for central neural pathways in vestibuloocular reflex. J Neurophysiol 51:210–241
Gdowski GT, McCrea RA (2000) Neck proprioceptive inputs to primate vestibular nucleus neurons. Exp Brain Res 135:511–526
Ghasia FF, Angelaki DE (2005) Do motoneurons encode the noncommutativity of ocular rotations? Neuron 47:281–293
Ghasia FF, Meng H, Angelaki DE (2008) Neural correlates of forward and inverse models for eye movements: evidence from three-dimensional kinematics. J Neurosci 28:5082–5087
Glasauer S (2003) Cerebellar contribution to saccades and gaze holding: a modeling approach. Ann N Y Acad Sci 1004:206–219
Glasauer S, Merfeld D (eds) (1997) Modelling three-dimensional vestibular responses during complex motion stimulation. Harwood Academic, Amsterdam
Godaux E, Mettens P, Cheron G (1993) Differential effect of injections of kainic acid into the prepositus and the vestibular nuclei of the cat. J Physiol 472:459–482
Gomi H, Shidara M, Takemura A, Inoue Y, Kawano K, Kawato M (1998) Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys. I. Simple spikes. J Neurophysiol 80:818–831
Green AM, Angelaki DE (2003) Resolution of sensory ambiguities for gaze stabilization requires a second neural integrator. J Neurosci 23:9265–9275
Green AM, Angelaki DE (2004) An integrative neural network for detecting inertial motion and head orientation. J Neurophysiol 92:905–925
Green AM, Angelaki DE (2007) Coordinate transformations and sensory integration in the detection of spatial orientation and self-motion: from models to experiments. Prog Brain Res 165:155–180
Green A, Galiana HL (1996) Exploring sites for short-term VOR modulation using a bilateral model. Ann N Y Acad Sci 781:625–628
Green AM, Galiana HL (1998) Hypothesis for shared central processing of canal and otolith signals. J Neurophysiol 80:2222–2228
Green AM, Shaikh AG, Angelaki DE (2005) Sensory vestibular contributions to constructing internal models of self-motion. J Neural Eng 2:S164–S179
Green AM, Meng H, Angelaki DE (2007) A reevaluation of the inverse dynamic model for eye movements. J Neurosci 27:1346–1355
Gu Y, DeAngelis GC, Angelaki DE (2007) A functional link between area MSTd and heading perception based on vestibular signals. Nat Neurosci 10:1038–1047
Guldin WO, Grusser OJ (1998) Is there a vestibular cortex? Trends Neurosci 21:254–259
Guthrie BL, Porter JD, Sparks DL (1983) Corollary discharge provides accurate eye position information to the oculomotor system. Science 221:1193–1195
Halmagyi GM, Curthoys IS, Todd MJ, D’Cruz DM, Cremer PD, Henderson CJ, Staples MJ (1991) Unilateral vestibular neurectomy in man causes a severe permanent horizontal vestibulo-ocular reflex deficit in response to high-acceleration ampullofugal stimulation. Acta Otolaryngol Suppl 481:411–414
Harris LR (1987) Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis. Exp Brain Res 66:522–532
Haruno M, Wolpert DM, Kawato M (2001) Mosaic model for sensorimotor learning and control. Neural Comput 13:2201–2220
Hazel TR, Sklavos SG, Dean P (2002) Estimation of premotor synaptic drives to simulated abducens motoneurons for control of eye position. Exp Brain Res 146:184–196
Hess BJ, Angelaki DE (1997) Inertial vestibular coding of motion: concepts and evidence. Curr Opin Neurobiol 7:860–866
Horak FB, Earhart GM, Dietz V (2001) Postural responses to combinations of head and body displacements: vestibular-somatosensory interactions. Exp Brain Res 141:410–414
Inglis JT, Shupert CL, Hlavacka F, Horak FB (1995) Effect of galvanic vestibular stimulation on human postural responses during support surface translations. J Neurophysiol 73:896–901
Israel I, Grasso R, Georges-Francois P, Tsuzuku T, Berthoz A (1997) Spatial memory and path integration studied by self-driven passive linear displacement. I. Basic properties. J Neurophysiol 77:3180–3192
Ito M (1970) Neurophysiological aspects of the cerebellar motor control system. Int J Neurol 7:162–176
Jamali M, Sadeghi SG, Cullen KE (2009) Response of vestibular nerve afferents innervating utricle and saccule during passive and active translations. J Neurophysiol 101:141–149
Kaneko CR (1997) Eye movement deficits after ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys. I. Saccades and fixation. J Neurophysiol 78:1753–1768
Kaneko CR (1999) Eye movement deficits following ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys. II. Pursuit, vestibular, and optokinetic responses. J Neurophysiol 81:668–681
Karnath HO, Dieterich M (2006) Spatial neglect–a vestibular disorder? Brain 129:293–305
Kasper J, Schor RH, Wilson VJ (1988) Response of vestibular neurons to head rotations in vertical planes. II. Response to neck stimulation and vestibular-neck interaction. J Neurophysiol 60:1765–1778
Katz E, Vianney de Jong JM, Buettner-Ennever J, Cohen B (1991) Effects of midline medullary lesions on velocity storage and the vestibulo-ocular reflex. Exp Brain Res 87:505–520
Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727
Kawato M, Kuroda T, Imamizu H, Nakano E, Miyauchi S, Yoshioka T (2003) Internal forward models in the cerebellum: fMRI study on grip force and load force coupling. Prog Brain Res 142:171–188
Keller EL, Robinson DA (1971) Absence of a stretch reflex in extraocular muscles of the monkey. J Neurophysiol 34:908–919
King WM, Lisberger SG, Fuchs AF (1976) Responses of fibers in medial longitudinal fasciculus (MLF) of alert monkeys during horizontal and vertical conjugate eye movements evoked by vestibular or visual stimuli. J Neurophysiol 39:1135–1149
Kleine JF, Guan Y, Kipiani E, Glonti L, Hoshi M, Buttner U (2004) Trunk position influences vestibular responses of fastigial nucleus neurons in the alert monkey. J Neurophysiol 91:2090–2100
Klier EM, Angelaki DE (2008) Spatial updating and the maintenance of visual constancy. Neuroscience 156:801–818
Klier EM, Angelaki DE, Hess BJ (2005) Roles of gravitational cues and efference copy signals in the rotational updating of memory saccades. J Neurophysiol 94:468–478
Klier EM, Meng H, Angelaki DE (2006) Three-dimensional kinematics at the level of the oculomotor plant. J Neurosci 26:2732–2737
Kluzik J, Diedrichsen J, Shadmehr R, Bastian AJ (2008) Reach adaptation: what determines whether we learn an internal model of the tool or adapt the model of our arm? J Neurophysiol 100:1455–1464
Kono R, Poukens V, Demer JL (2002) Quantitative analysis of the structure of the human extraocular muscle pulley system. Invest Ophthalmol Vis Sci 43:2923–2932
Langer T, Fuchs AF, Chubb MC, Scudder CA, Lisberger SG (1985a) Floccular efferents in the rhesus macaque as revealed by autoradiography and horseradish peroxidase. J Comp Neurol 235:26–37
Langer T, Fuchs AF, Scudder CA, Chubb MC (1985b) Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. J Comp Neurol 235:1–25
Laurens J, Droulez J (2007) Bayesian processing of vestibular information. Biol Cybern 96:389–404
Lewis RF, Haburcakova C, Merfeld DM (2008) Roll tilt psychophysics in rhesus monkeys during vestibular and visual stimulation. J Neurophysiol 100:140–153
Li N, Angelaki DE (2005) Updating visual space during motion in depth. Neuron 48:149–158
Li CS, Padoa-Schioppa C, Bizzi E (2001) Neuronal correlates of motor performance and motor learning in the primary motor cortex of monkeys adapting to an external force field. Neuron 30:593–607
Lisberger SG (1988) The neural basis for motor learning in the vestibulo-ocular reflex in monkeys. Trends Neurosci 11:147–152
Lisberger SG (2009) Internal models of eye movement in the floccular complex of the monkey cerebellum. Neuroscience 162(3):763–776
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 41:733–763
Lisberger SG, Miles FA (1980) Role of primate medial vestibular nucleus in long-term adaptive plasticity of vestibuloocular reflex. J Neurophysiol 43:1725–1745
Lisberger SG, Pavelko TA, Bronte-Stewart HM, Stone LS (1994a) 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
Lisberger SG, Pavelko TA, Broussard DM (1994b) 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
Lisberger SG, Pavelko TA, Broussard DM (1994c) Responses during eye movements of brain stem neurons that receive monosynaptic inhibition from the flocculus and ventral paraflocculus in monkeys. J Neurophysiol 72:909–927
Lopez-Barneo J, Darlot C, Berthoz A, Baker R (1982) Neuronal activity in prepositus nucleus correlated with eye movement in the alert cat. J Neurophysiol 47:329–352
MacNeilage PR, Banks MS, Berger DR, Bulthoff HH (2007) A Bayesian model of the disambiguation of gravitoinertial force by visual cues. Exp Brain Res 179:263–290
Macpherson JM, Everaert DG, Stapley PJ, Ting LH (2007) Bilateral vestibular loss in cats leads to active destabilization of balance during pitch and roll rotations of the support surface. J Neurophysiol 97:4357–4367
Manzoni D, Andre P, Pompeiano O (1997) Changes in gain and spatiotemporal properties of the vestibulospinal reflex after injection of a GABA-A agonist in the cerebellar anterior vermis. J Vestib Res 7:7–20
Manzoni D, Pompeiano O, Bruschini L, Andre P (1999) Neck input modifies the reference frame for coding labyrinthine signals in the cerebellar vermis: a cellular analysis. Neuroscience 93:1095–1107
Mars F, Archambault PS, Feldman AG (2003) Vestibular contribution to combined arm and trunk motion. Exp Brain Res 150:515–519
Maurer C, Mergner T, Peterka RJ (2006) Multisensory control of human upright stance. Exp Brain Res 171:231–250
Mayne RA (1974) A systems concept of the vestibular organs. In: Kornhuber HH (ed) Handbook of sensory physiology: the vestibular system. Springer, New York, pp 493–580
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 76:3136–3148
McCrea RA, Baker R (1985) Anatomical connections of the nucleus prepositus of the cat. J Comp Neurol 237:377–407
McCrea RA, Yoshida K, Berthoz A, Baker R (1980) Eye movement related activity and morphology of second order vestibular neurons terminating in the cat abducens nucleus. Exp Brain Res 40:468–473
McCrea RA, Strassman A, May E, Highstein SM (1987) Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey. J Comp Neurol 264:547–570
McCrea RA, Gdowski GT, Boyle R, Belton T (1999) Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. J Neurophysiol 82:416–428
McFarland JL, Fuchs AF (1992) Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques. J Neurophysiol 68:319–332
Meng H, Angelaki DE (2006) Neural correlates of the dependence of compensatory eye movements during translation on target distance and eccentricity. J Neurophysiol 95:2530–2540
Meng H, Green AM, Dickman JD, Angelaki DE (2005) Pursuit–vestibular interactions in brain stem neurons during rotation and translation. J Neurophysiol 93:3418–3433
Merfeld DM (1995) Modeling the vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt. Exp Brain Res 106:123–134
Merfeld DM, Young LR (1995) The vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt. Exp Brain Res 106:111–122
Merfeld DM, Zupan LH (2002) Neural processing of gravitoinertial cues in humans. III. Modeling tilt and translation responses. J Neurophysiol 87:819–833
Merfeld DM, Young LR, Oman CM, Shelhamer MJ (1993a) A multidimensional model of the effect of gravity on the spatial orientation of the monkey. J Vestib Res 3:141–161
Merfeld DM, Young LR, Paige GD, Tomko DL (1993b) Three dimensional eye movements of squirrel monkeys following postrotatory tilt. J Vestib Res 3:123–139
Merfeld DM, Zupan L, Peterka RJ (1999) Humans use internal models to estimate gravity and linear acceleration. Nature 398:615–618
Merfeld DM, Zupan LH, Gifford CA (2001) Neural processing of gravito-inertial cues in humans. II. Influence of the semicircular canals during eccentric rotation. J Neurophysiol 85:1648–1660
Merfeld DM, Park S, Gianna-Poulin C, Black FO, Wood S (2005a) Vestibular perception and action employ qualitatively different mechanisms. I. Frequency response of VOR and perceptual responses during Translation and Tilt. J Neurophysiol 94:186–198
Merfeld DM, Park S, Gianna-Poulin C, Black FO, Wood S (2005b) Vestibular perception and action employ qualitatively different mechanisms. II. VOR and perceptual responses during combined Tilt&Translation. J Neurophysiol 94:199–205
Mergner T, Anastasopoulos D, Becker W, Deecke L (1981) Discrimination between trunk and head rotation; a study comparing neuronal data from the cat with human psychophysics. Acta Psychol (Amst) 48:291–301
Mergner T, Siebold C, Schweigart G, Becker W (1991) Human perception of horizontal trunk and head rotation in space during vestibular and neck stimulation. Exp Brain Res 85:389–404
Mettens P, Godaux E, Cheron G, Galiana HL (1994) Effect of muscimol microinjections into the prepositus hypoglossi and the medial vestibular nuclei on cat eye movements. J Neurophysiol 72:785–802
Miall RC, Weir DJ, Wolpert DM, Stein JF (1993) Is the cerebellum a Smith predictor? J Mot Behav 25:203–216
Miles FA, Fuller JH, Braitman DJ, Dow BM (1980) Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. J Neurophysiol 43:1437–1476
Miller JM (1989) Functional anatomy of normal human rectus muscles. Vision Res 29:223–240
Mizukoshi K, Kobayashi H, Ohashi N, Watanabe Y (1983) Quantitative analysis of the human visual vestibulo-ocular reflex in sinusoidal rotation. Acta Otolaryngol Suppl 393:58–64
Mohr C, Roberts PD, Bell CC (2003) The mormyromast region of the mormyrid electrosensory lobe. I. Responses to corollary discharge and electrosensory stimuli. J Neurophysiol 90:1193–1210
Musallam WS, Tomlinson RD (1999) Model for the translational vestibuloocular reflex (VOR). J Neurophysiol 82:2010–2014
Nakamagoe K, Iwamoto Y, Yoshida K (2000) Evidence for brainstem structures participating in oculomotor integration. Science 288:857–859
Padoa-Schioppa C, Li CS, Bizzi E (2002) Neuronal correlates of kinematics-to-dynamics transformation in the supplementary motor area. Neuron 36:751–765
Page WK, Duffy CJ (2003) Heading representation in MST: sensory interactions and population encoding. J Neurophysiol 89:1994–2013
Paige GD, Sargent EW (1991) Visually-induced adaptive plasticity in the human vestibulo-ocular reflex. Exp Brain Res 84:25–34
Paige GD, Tomko DL (1991a) Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. J Neurophysiol 65:1170–1182
Paige GD, Tomko DL (1991b) Eye movement responses to linear head motion in the squirrel monkey. II. Visual-vestibular interactions and kinematic considerations. J Neurophysiol 65:1183–1196
Raphan T, Cohen B (1988) Organizational principles of velocity storage in three dimensions. The effect of gravity on cross-coupling of optokinetic after-nystagmus. Ann N Y Acad Sci 545:74–92
Raphan T, Cohen B (2002) The vestibulo-ocular reflex in three dimensions. Exp Brain Res 145:1–27
Raphan T, Matsuo V, Cohen B (eds) (1977) A velocity storage mechanism responsible for optokinetic nystagmus (OKN), optokinetic after-nystagmus (OKAN) and vestibular nystagmus. Elsevier, Amsterdam
Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35:229–248
Raphan T, Cohen B, Henn V (1981) Effects of gravity on rotatory nystagmus in monkeys. Ann N Y Acad Sci 374:44–55
Raptis HA, Dannenbaum E, Paquet N, Feldman AG (2007) Vestibular system may provide equivalent motor actions regardless of the number of body segments involved in the task. J Neurophysiol 97:4069–4078
Raymond JL, Lisberger SG, Mauk MD (1996) The cerebellum: a neuronal learning machine? Science 272:1126–1131
Reisine H, Raphan T (1992) Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation. Exp Brain Res 92:209–226
Robinson DA (1963) A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Eng 10:137–145
Robinson DA (1964) The mechanics of human saccadic eye movement. J Physiol 174:245–264
Robinson DA (1965) The mechanics of human smooth pursuit eye movement. J Physiol 180:569–591
Robinson DA (1970) Oculomotor unit behavior in the monkey. J Neurophysiol 33:393–403
Robinson DA (ed) (1977) Vestibular and optokinetic symbiosis: an example of explaining by modeling. Elsevier, Amsterdam
Robinson DA (1981) The use of control systems analysis in the neurophysiology of eye movements. Annu Rev Neurosci 4:463–503
Roy JE, Cullen KE (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21:2131–2142
Roy JE, Cullen KE (2004) Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci 24:2102–2111
Sadeghi SG, Minor LB, Cullen KE (2007) Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy. J Neurophysiol 97:1503–1514
Salinas E, Abbott LF (1995) Transfer of coded information from sensory to motor networks. J Neurosci 15:6461–6474
Sandeman DC, Okajima A (1972) Statocyst-induced eye movement in the crab Scylla serrata. I. The sensory input from the statocyst. J Exp Biol 57:187–204
Sawtell NB, Williams A, Bell CC (2007) Central control of dendritic spikes shapes the responses of Purkinje-like cells through spike timing-dependent synaptic plasticity. J Neurosci 27:1552–1565
Scott SH, Kalaska JF (1997) Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. J Neurophysiol 77:826–852
Scott SH, Sergio LE, Kalaska JF (1997) Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. J Neurophysiol 78:2413–2426
Scudder CA, Fuchs AF (1992) Physiological and behavioral identification of vestibular nucleus neurons mediating the horizontal vestibuloocular reflex in trained rhesus monkeys. J Neurophysiol 68:244–264
Sergio LE, Kalaska JF (2003) Systematic changes in motor cortex cell activity with arm posture during directional isometric force generation. J Neurophysiol 89:212–228
Shadmehr R (2004) Generalization as a behavioral window to the neural mechanisms of learning internal models. Hum Mov Sci 23:543–568
Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14:3208–3224
Shaikh AG, Meng H, Angelaki DE (2004) Multiple reference frames for motion in the primate cerebellum. J Neurosci 24:4491–4497
Shaikh AG, Green AM, Ghasia FF, Newlands SD, Dickman JD, Angelaki DE (2005) Sensory convergence solves a motion ambiguity problem. Curr Biol 15:1657–1662
Shidara M, Kawano K, Gomi H, Kawato M (1993) Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum. Nature 365:50–52
Singla CL (1975) Staocysts of hydromedusae. Cell Tissue Res 158:391–407
Skavenski AA, Robinson DA (1973) Role of abducens neurons in vestibuloocular reflex. J Neurophysiol 36:724–738
Smith MA, Crawford JD (2005) Distributed population mechanism for the 3-D oculomotor reference frame transformation. J Neurophysiol 93:1742–1761
Smith PF, Darlington CL, Zheng Y (2009) Move it or lose it—is stimulation of the vestibular system necessary for normal spatial memory? Hippocampus (in press)
Sommer MA, Wurtz RH (2002) A pathway in primate brain for internal monitoring of movements. Science 296:1480–1482
Sommer MA, Wurtz RH (2008) Brain circuits for the internal monitoring of movements. Annu Rev Neurosci 31:317–338
Stackman RW, Taube JS (1997) Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J Neurosci 17:4349–4358
Stackman RW, Clark AS, Taube JS (2002) Hippocampal spatial representations require vestibular input. Hippocampus 12:291–303
Stapley PJ, Ting LH, Kuifu C, Everaert DG, Macpherson JM (2006) Bilateral vestibular loss leads to active destabilization of balance during voluntary head turns in the standing cat. J Neurophysiol 95:3783–3797
Stein BE, Stanford TR (2008) Multisensory integration: current issues from the perspective of the single neuron. Nat Rev Neurosci 9:255–266
Stone LS, Lisberger SG (1990) Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. J Neurophysiol 63:1241–1261
Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181–207
Telford L, Seidman SH, Paige GD (1997) Dynamics of squirrel monkey linear vestibuloocular reflex and interactions with fixation distance. J Neurophysiol 78:1775–1790
Tomlinson RD, Robinson DA (1984) Signals in vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol 51:1121–1136
Tweed D, Vilis T (1990) Geometric relations of eye position and velocity vectors during saccades. Vision Res 30:111–127
Van Beuzekom AD, Medendorp WP, Van Gisbergen JA (2001) The subjective vertical and the sense of self orientation during active body tilt. Vision Res 41:3229–3242
Vingerhoets RA, Medendorp WP, Van Gisbergen JA (2008) Body-tilt and visual verticality perception during multiple cycles of roll rotation. J Neurophysiol 99:2264–2280
von Helmholtz H (1925) Handbuch der Physiologischen Optik [Treatise on physiological optics]. Optical Society of America, JPC Southall, Rochester
von Holst E, Mittelstaedt H (1950) Das reafferenzprinzip. Naturwissenschaften 37:464–476
Voogd J, Glickstein M (1998) The anatomy of the cerebellum. Trends Neurosci 21:370–375
Waespe W, Henn V (1977) Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp Brain Res 27:523–538
Waespe W, Henn V (1981) Visual-vestibular interaction in the flocculus of the alert monkey. II. Purkinje cell activity. Exp Brain Res 43:349–360
Wagner MJ, Smith MA (2008) Shared internal models for feedforward and feedback control. J Neurosci 28:10663–10673
Wearne S, Raphan T, Cohen B (1997a) Contribution of vestibular commissural pathways to spatial orientation of the angular vestibuloocular reflex. J Neurophysiol 78:1193–1197
Wearne S, Raphan T, Waespe W, Cohen B (1997b) Control of the three-dimensional dynamic characteristics of the angular vestibulo-ocular reflex by the nodulus and uvula. Prog Brain Res 114:321–334
Wearne S, Raphan T, Cohen B (1998) Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula. J Neurophysiol 79:2690–2715
Wilson VJ, Yamagata Y, Yates BJ, Schor RH, Nonaka S (1990) Response of vestibular neurons to head rotations in vertical planes. III. Response of vestibulocollic neurons to vestibular and neck stimulation. J Neurophysiol 64:1695–1703
Wolpert DM, Kawato M (1998) Multiple paired forward and inverse models for motor control. Neural Netw 11:1317–1329
Wolpert DM, Miall RC (1996) Forward models for physiological motor control. Neural Netw 9:1265–1279
Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science 269:1880–1882
Wylie DR, Frost BJ (1999) Complex spike activity of Purkinje cells in the ventral uvula and nodulus of pigeons in response to translational optic flow. J Neurophysiol 81:256–266
Yakusheva TA, Shaikh AG, Green AM, Blazquez PM, Dickman JD, Angelaki DE (2007) Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame. Neuron 54:973–985
Yates BJ (1992) Vestibular influences on the sympathetic nervous system. Brain Res Brain Res Rev 17:51–59
Yates BJ, Bronstein AM (2005) The effects of vestibular system lesions on autonomic regulation: observations, mechanisms, and clinical implications. J Vestib Res 15:119–129
Yokota J, Reisine H, Cohen B (1992) Nystagmus induced by electrical stimulation of the vestibular and prepositus hypoglossi nuclei in the monkey: evidence for site of induction of velocity storage. Exp Brain Res 92:123–138
Zago M, Bosco G, Maffei V, Iosa M, Ivanenko YP, Lacquaniti F (2004) Internal models of target motion: expected dynamics overrides measured kinematics in timing manual interceptions. J Neurophysiol 91:1620–1634
Zago M, McIntyre J, Senot P, Lacquaniti F (2009) Visuo-motor coordination and internal models for object interception. Exp Brain Res 192:571–604
Zee DS, Yamazaki A, Butler PH, Gucer G (1981) Effects of ablation of flocculus and paraflocculus of eye movements in primate. J Neurophysiol 46:878–899
Zupan LH, Peterka RJ, Merfeld DM (2000) Neural processing of gravito-inertial cues in humans. I. Influence of the semicircular canals following post-rotatory tilt. J Neurophysiol 84:2001–2015
Zupan LH, Merfeld DM, Darlot C (2002) Using sensory weighting to model the influence of canal, otolith and visual cues on spatial orientation and eye movements. Biol Cybern 86:209–230
Acknowledgments
Supported by NIH grants DC04260 and EY12814 and a chercheur boursier salary award from the Fonds de la recherche en santé du Québec (FRSQ).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Green, A.M., Angelaki, D.E. Internal models and neural computation in the vestibular system. Exp Brain Res 200, 197–222 (2010). https://doi.org/10.1007/s00221-009-2054-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-009-2054-4