Abstract
The vestibular system projects onto the cerebellum via three major pathways that are composed of primary and secondary vestibular mossy fiber afferents and vestibular climbing fibers. Vestibular primary afferent mossy fibers project to the ipsilateral vermal lobules IX–X and to the base of the sulci of several other vermal lobules. Secondary vestibular mossy fibers originate from the classic vestibular nuclei, lateral, medial, descending and superior vestibular nuclei (DVN, LVN, MVN, and SVN). These mossy fibers terminate in vermal lobules IX–X (uvula-nodulus) and hemispheric lobule X (flocculus). The vestibular nuclei receive convergent vestibular, optokinetic, and neck proprioceptive information. Vestibular afferents project to vermal lobules IX–X as climbing fibers that originate from two sub-nuclei of the inferior olive, the dorsomedial cell column (DMCC) and β-nucleus. These sub-nuclei receive secondary vestibular afferent projections from the ipsilateral parasolitary nucleus (Psol). The Psol receives primary afferent vestibular afferent projections from the ipsilateral vertical semicircular canals and otoliths, but not from the horizontal semicircular canals.
Functionally, vestibular climbing fiber projections are arrayed in sagittal zones, establishing a mediolateral map on vermal lobules IX–X that encodes all possible head angles during movement. Electrophysiological evidence shows that climbing fiber signals are preeminent in modulating both the CSs (complex spikes) and SSs (simple spikes) of cerebellar Purkinje cells. This discharge is fed back onto neurons in the dorsal aspect of the DVN, LVN, MVN, prepositus hypoglossal nucleus (NPH) and nuclei within the ventral brainstem. The vestibulocerebellum imposes a climbing fiber-constructed coordinate system on postural responses and permits adaptive guidance of movement.
References
Akaogi K-I, Sato Y, Ikarashi K, Kawasaki T (1994) Mossy fiber projections from the brain stem to the nodulus in the cat. An experimental study comparing the nodulus, the uvula and the flocculus. Brain Res 638:12–20
Alley K, Baker R, Simpson JI (1975) Afferents to the vestibulo-cerebellum and the origin of the visual climbing fibers in the rabbit. Brain Res 98:582–589
Andersen P, Eccles JC, Voorhoeve PE (1964) Postsynaptic inhibition of cerebellar Purkinje cells. J Neurophysiol 27:1138–1153
Apps R, Garwicz M (2005) Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci 6:297–311
Armstrong DM, Edgley SA (1988) Discharges of interpositus and Purkinje cells of the cat cerebellum during locomotion under different conditions. J Physiol 400:425–445
Badura A, Schonewille M, Voges K, Galliano E, Renier N, Gao Z, Witter L, Hoebeek FE, Chedotal A, De Zeeuw CI (2013) Climbing fiber input shapes reciprocity of Purkinje cell firing. Neuron 78:700–713
Barmack NH, Shojaku H (1992) Vestibularly induced slow oscillations in climbing fiber responses of Purkinje cells in the cerebellar nodulus of the rabbit. Neuroscience 50:1–5
Barmack NH, Shojaku H (1995) Vestibular and visual signals evoked in the uvula-nodulus of the rabbit cerebellum by natural stimulation. J Neurophysiol 74:2573–2589
Barmack NH, Yakhnitsa V (2000) Vestibular signals in the parasolitary nucleus. J Neurophysiol 83:3559–3569
Barmack NH, Yakhnitsa V (2003) Cerebellar climbing fibers modulate simple spikes in cerebellar Purkinje cells. J Neurosci 23:7904–7916
Barmack NH, Yakhnitsa V (2008a) Functions of interneurons in mouse cerebellum. J Neurosci 28:1140–1152
Barmack NH, Yakhnitsa V (2008b) Distribution of granule cells projecting to focal Purkinje cells in mouse uvula-nodulus. Neuroscience 156:216–221
Barmack NH, Yakhnitsa V (2011) Microlesions of the inferior olive reduce vestibular modulation of Purkinje cell complex and simple spikes in mouse cerebellum. J Neurosci 31:9824–9835
Barmack NH, Yakhnitsa V (2012) Vestibulocerebellar connections. In: Mantu M, Gruol DL, Schmahmann J, Koibuchi N, Rossi F (eds) Handbook of cerebellar disorders. Springer, Heidelberg, pp 357–376
Barmack NH, Yakhnitsa V (2013) Modulated discharge of Purkinje and stellate cells persists after unilateral loss of vestibular primary afferent mossy fibers in mice. J Neurophysiol 110:2257–2274
Barmack NH, Baughman RW, Eckenstein FP (1992a) Cholinergic innervation of the cerebellum of rat, rabbit, cat and monkey as revealed by choline acetyltransferase activity and immunohistochemistry. J Comp Neurol 317:233–249
Barmack NH, Baughman RW, Eckenstein FP (1992b) Cholinergic innervation of the cerebellum of the rat by secondary vestibular afferents. In: Cohen B, Tomko DL, Guedry F (eds) Sensing and controlling motion: vestibular and sensorimotor function. New York Academy of Sciences, New York, pp 566–579
Barmack NH, Baughman RW, Eckenstein FP, Shojaku H (1992c) Secondary vestibular cholinergic projection to the cerebellum of rabbit and rat as revealed by choline acetyltransferase immunohistochemistry, retrograde and orthograde tracers. J Comp Neurol 317:250–270
Barmack NH, Baughman RW, Errico P, Shojaku H (1993a) Vestibular primary afferent projection to the cerebellum of the rabbit. J Comp Neurol 327:521–534
Barmack NH, Fagerson M, Fredette BJ, Mugnaini E, Shojaku H (1993b) Activity of neurons in the beta nucleus of the inferior olive of the rabbit evoked by natural vestibular stimulation. Exp Brain Res 94:203–215
Barmack NH, Fredette BJ, Mugnaini E (1998) Parasolitary nucleus: a source of GABAergic vestibular information to the inferior olive of rat and rabbit. J Comp Neurol 392:352–372
Bishop GA, Ho RH (1986) Cell bodies of origin of serotonin-immunoreactive afferents to the inferior olivary complex of the rat. Brain Res 399:369–373
Blazquez P, Partsalis A, Gerrits NM, Highstein SM (2000) Input of anterior and posterior semicircular canal interneurons encoding head-velocity to the dorsal Y group of the vestibular nuclei. J Neurophysiol 83:2891–2904
Bloedel JR, Bracha V (2009) Cerebellar functions. In: Binder MD, Hirokawa N, Windhorst U (eds) Encyclopedic reference of neuroscience. Springer, Heidelberg, pp 667–671
Brand S, Dahl AL, Mugnaini E (1976) The length of parallel fibers in the cat cerebellar cortex. An experimental light and electron microscopic study. Exp Brain Res 26:39–58
Brodal A (1972) Anatomy of the vestibuloreticular connections and possible “ascending” vestibular pathways from the reticular formation. In: Brodal A, Pompeiano O (eds) Basic aspects of central vestibular mechanisms. Progress in brain research, vol 37. Elsevier, Amsterdam/London/New York
Brodal A, Brodal P (1985) Observations on the secondary vestibulocerebellar projections in the macaque monkey. Exp Brain Res 58:62–74
Brodal A, Pompeiano O (1957) The vestibular nuclei in the cat. J Anat 91:438–454
Brodal A, Torvik A (1957) The origin of secondary vestibulo-cerebellar fibers in cats; an experimental anatomical study. Arch Psychiatr Nervenkr Z Gesamte Neurol Psychiatr 195:550–567
Carter AG, Regehr WG (2000) Prolonged synaptic currents and glutamate spillover at the parallel fiber to stellate cell synapse. J Neurosci 20:4423–4434
Cavanagh JB (1994) Is Purkinje cell loss in Leigh’s disease an excitotoxic event secondary to damage to inferior olivary nuclei? Neuropathol Appl Neurobiol 20:599–603
Cha Y-H, Baloh RW, Cho C, Magnusson M, Song J-J, Strupp M, Wuyts F, Staab JP (2020) Mal de débarquement syndrome diagnostic criteria: consensus document of the classification Committee of the Bárány Society. J Vestib Res 30:285–293
Cohen D, Yarom Y (1998) Patches of synchronized activity in the cerebellar cortex evoked by mossy-fiber stimulation: questioning the role of parallel fibers. Proc Natl Acad Sci U S A 95:15032–15036
Crépel F, Jaillard D (1991) Pairing of pre- and postsynaptic activities in cerebellar Purkinje cells induces long-term changes in synaptic efficacy in vitro. J Physiol Lond 432:123–141
De Zeeuw CI, Wentzel P, Mugnaini E (1993) Fine structure of the dorsal cap of the inferior olive and its GABAergic and non-GABAergic input from the nucleus prepositus hypoglossi in rat and rabbit. J Comp Neurol 327:63–82
Desclin JC (1976) Early terminal degeneration of cerebellar climbing fibers after destruction of the inferior olive in the rat. Synaptic relationships in the molecular layer. Anat Embryol (Berl) 149:87–112
Diño MR, Schuerger RJ, Liu YB, Slater NT, Mugnaini E (2000) Unipolar brush cell: a potential feedforward excitatory interneuron of the cerebellum. Neuroscience 98:625–636
Diño MR, Perachio AA, Mugnaini E (2001) Cerebellar unipolar brush cells are targets of primary vestibular afferents: an experimental study in the gerbil. Exp Brain Res 140:162–170
Dugué GP, Dumoulin A, Triller A, Dieudonné S (2005) Target-dependent use of coreleased inhibitory transmitters at central synapses. J Neurosci 25:6490–6498
Dzubay JA, Jahr CE (1999) The concentration of synaptically released glutamate outside of the climbing fiber-Purkinje cell synaptic cleft. J Neurosci 19:5265–5274
Ebner TJ, Bloedel JR (1981) Role of climbing fiber afferent input in determining responsiveness of Purkinje cells to mossy fiber inputs. J Neurophysiol 45:962–971
Eccles JC, Llinás R, Sasaki K (1966a) The excitatory synaptic action of climbing fibers on the Purkinje cells of the cerebellum. J Physiol Lond 182:268–296
Eccles JC, Llinás R, Sasaki K (1966b) The mossy fibre-granule cell relay of the cerebellum and its inhibitory control by Golgi cells. Exp Brain Res 1:82–101
Eccles JC, Ito M, Szentágothai J (1967) The cerebellum as a neuronal machine. Springer, New York
Epema AH, Gerrits NM, Voogd J (1990) Secondary vestibulocerebellar projections to the flocculus and uvulo-nodular lobule of the rabbit: a study using HRP and double fluorescent tracer techniques. Exp Brain Res 80:72–82
Falk T, Garver WS, Erickson RP, Wilson JM, Yool AJ (1999) Expression of Niemann-Pick type C transcript in rodent cerebellum in vivo and in vitro. Brain Res 839:49–57
Fernandez C, Goldberg JM (1976) 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
Foster IZ, Hanes DA, Barmack NH, McCollum G (2007) Spatial symmetries in vestibular projections to the uvula-nodulus. Biol Cybern 96:439–453
Fox CA, Hillman DE, Siegesmund KA, Dutta CR (1967) The primate cerebellar cortex: a Golgi and electron microscopic study. In: Fox CA, Snider RS (eds) Progress in brain research, Vol. 25: the cerebellum. Elsevier, New York, pp 174–225
Fushiki H, Barmack NH (1997) Topography and reciprocal activity of cerebellar Purkinje cells in the uvula-nodulus modulated by vestibular stimulation. J Neurophysiol 78:3083–3094
Gerrits NM, Epema AH, Van Linge A, Dalm E (1989) The primary vestibulocerebellar projection in the rabbit: absence of primary afferents in the flocculus. Neurosci Lett 105:27–33
Ghez C, Thach WT (2000) The cerebellum. In: Kandel ER, Schwartz J, Jessel TM (eds) Principles of neuroscience, 4th edn. Elsevier, New York, pp 832–852
Goldberg JM, Fernandez C (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J Neurophysiol 34:635–660
Graf W, Simpson JI, Leonard CS (1988) Spatial organization of visual messages of the rabbit’s cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells. J Neurophysiol 60:2091–2121
Granit R, Phillips CG (1956) Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats. J Physiol Lond 133:520–547
Groenewegen HJ, Voogd J (1977) The parasagittal zonation within the olivocerebellar projection I. Climbing fiber distribution in the vermis of cat cerebellum. J Comp Neurol 174:417–488
Gundappa-Sulur G, De Schutter E, Bower JM (1999) Ascending granule cell axon: an important component of cerebellar cortical circuitry. J Comp Neurol 408:580–596
Hámori J, Szentágothai J (1966) Participation of Golgi neuron processes in the cerebellar glomeruli: an electron microscope study. Exp Brain Res 2:35–48
Hámori J, Szentágothai J (1980) Lack of evidence of synaptic contacts by climbing fibre collaterals to basket and stellate cells in developing rat cerebellar cortex. Brain Res 186:454–457
Hida C, Tsukamoto T, Awano H, Yamamoto T (1994) Ultrastructural localization of anti-Purkinje cell antibody-binding sites in paraneoplastic cerebellar degeneration. Arch Neurol 51:555–558
Hoddevik GH, Brodal A (1977) The olivocerebellar projection studied with the method of retrograde axonal transport of horseradish peroxidase. V. The projections to the flocculonodular lobe and the paraflocculus in the rabbit. J Comp Neurol 176:269–280
Ishikawa K, Watanabe M, Yoshizawa K, Fujita T, Iwamoto H, Yoshizawa T, Harada K, Nakamagoe K, Komatsuzaki Y, Satoh A, Doi M, Ogata T, Kanazawa I, Shoji S, Mizusawa H (1999) Clinical, neuropathological, and molecular study in two families with spinocerebellar ataxia type 6 (SCA6). J Neurol Neurosurg Psychiatry 67:86–89
Isope P, Barbour B (2002) Properties of unitary granule cell→Purkinje cell synapses in adult rat cerebellar slices. J Neurosci 22:9668–9678
Ito M (2002) The molecular organization of cerebellar long-term depression. Nat Rev Neurosci 3:896–902
Ito M, Karachot L (1989) Long-term desensitization of quisqualate-specific glutamate receptors in Purkinje cells investigated with wedge recording from rat cerebellar slices. Neurosci Res 7:168–171
Ito M, Sakurai M, Tongroach P (1982) Climbing fibre induced depression on both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J Physiol Lond 324:113–134
Johansson F, Jirenhed DA, Rasmussen A, Zucca R, Hesslow G (2014) Memory trace and timing mechanism localized to cerebellar Purkinje cells. Proc Natl Acad Sci U S A 111:14930–14934
Kano M, Kano M-S, Maekawa K (1991) Simple spike modulation of Purkinje cells in the cerebellar nodulus of the pigmented rabbit to optokinetic stimulation. Neurosci Lett 128:101–104
Kevetter GA, Perachio A (1986) Distribution of vestibular afferents that innervate the sacculus and posterior canal in the gerbil. J Comp Neurol 254:410–424
Kleinschmidt HJ, Collewijn H (1975) A search for habituation of vestibulo-ocular reactions to rotatory and linear sinusoidal accelerations in the rabbit. Exp Neurol 47:257–267
Koeppen AH (2005) The pathogenesis of spinocerebellar ataxia. Cerebellum 4:62–73
Korte G, Mugnaini E (1979) The cerebellar projection of the vestibular nerve in the cat. J Comp Neurol 184:265–278
Kotchabhakdi N, Walberg F (1978) Cerebellar afferent projections from the vestibular nuclei in the cat: an experimental study with the method of retrograde axonal transport of horseradish peroxidase. Exp Brain Res 31:591–604
Lisberger SG, Pavelko TA, Bronte-Stewart HM, Stone LS (1994) 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
Llinás R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol 305:197–213
Maklad A, Fritzsch B (2003) Partial segregation of posterior crista and saccular fibers to the nodulus and uvula of the cerebellum in mice, and its development. Dev Brain Res 140:223–236
McKay BE, Engbers JD, Mehaffey WH, Gordon GR, Molineux ML, Bains JS, Turner RW (2007) Climbing fiber discharge regulates cerebellar functions by controlling the intrinsic characteristics of Purkinje cell output. J Neurophysiol 97:2590–2604
Midtgaard J (1992a) Stellate cell inhibition of Purkinje cells in the turtle cerebellum in vitro. J Physiol Lond 457:355–367
Midtgaard J (1992b) Membrane properties and synaptic responses of Golgi cells and stellate cells in the turtle cerebellum in vitro. J Physiol Lond 457:329–354
Mugnaini E (1983) The length of cerebellar parallel fibers in chicken and Rhesus monkey. J Comp Neurol 220:7–15
Mugnaini E, Floris A (1994) The unipolar brush cell: a neglected neuron of the mammalian cerebellar cortex. J Comp Neurol 339:174–180
Nagao S (1989) Role of cerebellar flocculus in adaptive interaction between optokinetic eye movement response and vestibulo-ocular reflex in pigmented rabbits. Exp Brain Res 77:541–551
Napper RM, Harvey RJ (1988a) Quantitative study of the Purkinje cell dendritic spines in the rat cerebellum. J Comp Neurol 274:158–167
Napper RM, Harvey RJ (1988b) Number of parallel fiber synapses on an individual Purkinje cell in the cerebellum of the rat. J Comp Neurol 274:168–177
Narasimhan K, Linden DJ (1996) Defining a minimal computational unit for cerebellar long-term depression. Neuron 17:333–341
Nelson BJ, Adams JC, Barmack NH, Mugnaini E (1989) A comparative study of glutamate decarboxylase immunoreactive boutons in the mammalian inferior olive. J Comp Neurol 286:514–539
Newlands SD, Purcell IM, Kevetter GA, Perachio AA (2002) Central projections of the utricular nerve in the gerbil. J Comp Neurol 452:11–23
Newlands SD, Vrabec JT, Purcell IM, Stewart CM, Zimmerman BE, Perachio AA (2003) Central projections of the saccular and utricular nerves in macaques. J Comp Neurol 466:31–47
Palkovits M, Magyar P, Szentagothai J (1972) Quantitative histological analysis of the cerebellar cortex in the cat. IV. Mossy fiber-Purkinje cell numerical transfer. Brain Res 45:15–29
Pichitpornchai C, Rawson JA, Rees S (1994) Morphology of parallel fibers in the cerebellar cortex of the rat – an experimental light and electron-microscopic study with biocytin. J Comp Neurol 342:206–220
Pouzat C, Hestrin S (1997) Developmental regulation of basket/stellate cell → Purkinje cell synapses in the cerebellum. J Neurosci 17:9104–9112
Purcell IM, Perachio AA (2001) Peripheral patterns of terminal innervation of vestibular primary afferent neurons projecting to the vestibulocerebellum in the gerbil. J Comp Neurol 433:48–61
Raman IM, Bean BP (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19:1663–1674
Rossi DJ, Alford S, Mugnaini E, Slater NT (1995) Properties of transmission at a giant glutamatergic synapse in cerebellum: the mossy fiber-unipolar brush cell synapse. J Neurophysiol 74:24–42
Ruigrok TJ, Hensbroek RA, Simpson JI (2011) Spontaneous activity signatures of morphologically identified interneurons in the vestibulocerebellum. J Neurosci 31:712–724
Sakai K, Gofuku M, Kitagawa Y, Ogasawara T, Hirose G (1995) Induction of anti-Purkinje cell antibodies in vivo by immunizing with a recombinant 52-kDa paraneoplastic cerebellar degeneration-associated protein. J Neuroimmunol 60:135–141
Sakurai M (1987) Synaptic modification of parallel fibre-Purkinje cell transmission in in vitro Guinea-pig cerebellar slices. J Physiol Lond 394:463–480
Sato F, Sasaki H (1993) Morphological correlations between spontaneously discharging primary vestibular afferents and vestibular nucleus neurons in the cat. J Comp Neurol 333:554–556
Sato Y, Kanda K-I, Ikarashi K, Kawasaki T (1989) Differential mossy fiber projections to the dorsal and ventral uvula in the cat. J Comp Neurol 279:149–164
Schapiro MB, Rosman NP, Kemper TL (1984) Effects of chronic exposure to alcohol on the developing brain. Neurobehav Toxicol Teratol 6:351–356
Sugihara I, Wu HS, Shinoda Y (2001) The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to cerebellar compartmentalization. J Neurosci 21:7715–7723
Szapiro G, Barbour B (2007) Multiple climbing fibers signal to molecular layer interneurons exclusively via glutamate spillover. Nat Neurosci 10:735–742
Tago H, McGeer PL, McGeer EG, Akiyama H, Hersh LB (1989) Distribution of choline acetyltransferase immunopositive structures in the rat brainstem. Brain Res 495:271–297
Takeda T, Maekawa K (1989) Olivary branching projections to the flocculus, nodulus and uvula in the rabbit. II. Retrograde double labeling study with fluorescent dyes. Exp Brain Res 76:323–332
Takei A, Hamada T, Yabe I, Sasaki H (2005) Treatment of cerebellar ataxia with 5-HT1A agonist. Cerebellum 4:211–215
Tan J, Gerrits NM, Nanhoe R, Simpson JI, Voogd J (1995) Zonal organization of the climbing fiber projection to the flocculus and nodulus of the rabbit: a combined axonal tracing and acetylcholinesterase histochemical study. J Comp Neurol 356:23–50
Thunnissen IE, Epema AH, Gerrits NM (1989) Secondary vestibulocerebellar mossy fiber projection to the caudal vermis in the rabbit. J Comp Neurol 290:262–277
Voogd J, Barmack NH (2005) Oculomotor cerebellum. Prog Brain Res 151:231–268
Voogd J, Gerrits NM, Ruigrok TJ (1996) Organization of the vestibulocerebellum. Ann N Y Acad Sci 781:553–579
Walter JT, Khodakhah K (2006) The linear computational algorithm of cerebellar Purkinje cells. J Neurosci 26:12861–12872
Watase K, Barrett CF, Miyazaki T, Ishiguro T, Ishikawa K, Hu Y, Unno T, Sun Y, Kasai S, Watanabe M, Gomez CM, Mizusawa H, Tsien RW, Zoghbi HY (2008) Spinocerebellar ataxia type 6 knockin mice develop a progressive neuronal dysfunction with age-dependent accumulation of mutant CaV2.1 channels. Proc Natl Acad Sci U S A 105:11987–11992
Wentzel PR, Wylie DR, Ruigrok TJ, De Zeeuw CI (1995) Olivary projecting neurons in the nucleus prepositus hypoglossi, group y and ventral dentate nucleus do not project to the oculomotor complex in the rabbit and the rat. Neurosci Lett 190:45–48
Wu HS, Sugihara I, Shinoda Y (1999) Projection patterns of single mossy fibers originating from the lateral reticular nucleus in the rat cerebellar cortex and nuclei. J Comp Neurol 411:97–118
Wulff P, Schonewille M, Renzi M, Data L, Sassoe-Pognetto M, Data L, Data L, Hoebeek FE, Data L, Wisden W, Farrant M, De Zeeuw CI (2009) Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat Neurosci 12:1042–1049
Yakhnitsa V, Barmack NH (2006) Antiphasic Purkinje cell responses in mouse uvula-nodulus are sensitive to static roll-tilt and topographically organized. Neuroscience 143:615–626
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
Yamamoto M (1979) Topographical representation in rabbit cerebellar flocculus for various afferent inputs from the brainstem investigated by means of retrograde axonal transport of horseradish peroxidase. Neurosci Lett 12:29–34
Zee DS, Yee RD, Cogan DG, Robinson DA, Engel WK (1976) Ocular motor abnormalities in hereditary cerebellar ataxia. Brain 99:207–234
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Barmack, N.H., Yakhnitsa, V. (2022). Vestibulocerebellar Functional Connections. In: Manto, M.U., Gruol, D.L., Schmahmann, J.D., Koibuchi, N., Sillitoe, R.V. (eds) Handbook of the Cerebellum and Cerebellar Disorders. Springer, Cham. https://doi.org/10.1007/978-3-030-23810-0_18
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