Skip to main content
Top
Published in:

Open Access 01-04-2023 | Nystagmus | Original Article

In Vivo Localization of the Human Velocity Storage Mechanism and Its Core Cerebellar Networks by Means of Galvanic-Vestibular Afternystagmus and fMRI

Authors: Maxine Rühl, Rebecca Kimmel, Matthias Ertl, Julian Conrad, Peter zu Eulenburg

Published in: The Cerebellum | Issue 2/2023

Login to get access

Abstract

Humans are able to estimate head movements accurately despite the short half-life of information coming from our inner ear motion sensors. The observation that the central angular velocity estimate outlives the decaying signal of the semicircular canal afferents led to the concept of a velocity storage mechanism (VSM). The VSM can be activated via visual and vestibular modalities and becomes manifest in ocular motor responses after sustained stimulation like whole-body rotations, optokinetic or galvanic vestibular stimulation (GVS). The VSM has been the focus of many computational modelling approaches; little attention though has been paid to discover its actual structural correlates. Animal studies localized the VSM in the medial and superior vestibular nuclei. A significant modulation by cerebellar circuitries including the uvula and nodulus has been proposed. Nevertheless, the corresponding neuroanatomical structures in humans have not been identified so far. The aim of the present study was to delineate the neural substrates of the VSM using high-resolution infratentorial fMRI with a fast T2* sequence optimized for infratentorial neuroimaging and via video-oculography (VOG). The neuroimaging experiment (n=20) gave first in vivo evidence for an involvement of the vestibular nuclei in the VSM and substantiate a crucial role for cerebellar circuitries. Our results emphasize the importance of cerebellar feedback loops in VSM most likely represented by signal increases in vestibulo-cerebellar hubs like the uvula and nodulus and lobule VIIIA. The delineated activation maps give new insights regarding the function and embedment of Crus I, Crus II, and lobule VII and VIII in the human vestibular system.
Appendix
Available only for authorised users
Literature
1.
go back to reference Raphan, T., Cohen, B., Matsuo, V. A velocity-storage mechanism responsible for optokinetic nystagmus (OKN), optokinetic after-nystagmus (OKAN) and vestibular nystagmus: In: Control of Gaze by Brainstem Neurons. (eds. A. Berthoz and R. Baker). Amsterdam: Elsevier. 1978;37–47 Raphan, T., Cohen, B., Matsuo, V. A velocity-storage mechanism responsible for optokinetic nystagmus (OKN), optokinetic after-nystagmus (OKAN) and vestibular nystagmus: In: Control of Gaze by Brainstem Neurons. (eds. A. Berthoz and R. Baker). Amsterdam: Elsevier. 1978;37–47
2.
go back to reference Robinson DA. Linear addition of optokinetic and vestibular signals in the vestibular nucleus. Exp Brain Res. 1977;30:447–50.PubMed Robinson DA. Linear addition of optokinetic and vestibular signals in the vestibular nucleus. Exp Brain Res. 1977;30:447–50.PubMed
3.
go back to reference Raphan T, Matsuo V, Cohen B. Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res. 1979;35:229–48.PubMedCrossRef Raphan T, Matsuo V, Cohen B. Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res. 1979;35:229–48.PubMedCrossRef
4.
go back to reference Leigh RJ, Zee DS. The neurology of eye movements. Oxford: Oxford Univ Press, 2006, p. X, 763 S. Leigh RJ, Zee DS. The neurology of eye movements. Oxford: Oxford Univ Press, 2006, p. X, 763 S.
5.
go back to reference Reisine H, Raphan T. Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation. Exp Brain Res. 1992;92:209–26.PubMedCrossRef Reisine H, Raphan T. Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation. Exp Brain Res. 1992;92:209–26.PubMedCrossRef
7.
go back to reference Katz E, de Jong JMBV, Buettner-Ennever J, Cohen B. Effects of midline medullary lesions on velocity storage and the vestibulo-ocular reflex. Exp Brain Res. 1991;87:505–20.PubMedCrossRef Katz E, de Jong JMBV, Buettner-Ennever J, Cohen B. Effects of midline medullary lesions on velocity storage and the vestibulo-ocular reflex. Exp Brain Res. 1991;87:505–20.PubMedCrossRef
8.
go back to reference Raphan T, Matsuo V, and Cohen B. Control of gaze by brain stem neurons. 1977. Raphan T, Matsuo V, and Cohen B. Control of gaze by brain stem neurons. 1977.
9.
go back to reference Wearne S, Raphan T, Cohen B. Contribution of vestibular commissural pathways to spatial orientation of the angular vestibuloocular reflex. J Neurophysiol. 1997;78:1193–7.PubMedCrossRef Wearne S, Raphan T, Cohen B. Contribution of vestibular commissural pathways to spatial orientation of the angular vestibuloocular reflex. J Neurophysiol. 1997;78:1193–7.PubMedCrossRef
10.
go back to reference Yokota J-I, Reisine H, Cohen B. 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. 1992;92:123–38.PubMedCrossRef Yokota J-I, Reisine H, Cohen B. 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. 1992;92:123–38.PubMedCrossRef
11.
go back to reference Waespe W, Cohen B, Raphan T. Dynamic modification of the vestibulo-ocular reflex by the nodulus and uvula. Science. 1985;228:199–202.PubMedCrossRef Waespe W, Cohen B, Raphan T. Dynamic modification of the vestibulo-ocular reflex by the nodulus and uvula. Science. 1985;228:199–202.PubMedCrossRef
12.
go back to reference Shaikh AG, Palla A, Marti S, Olasagasti I, Optican LM, Zee DS, Straumann D. Role of cerebellum in motion perception and vestibulo-ocular reflex—similarities and disparities. Cerebellum. 2013;12:97–107.PubMedPubMedCentralCrossRef Shaikh AG, Palla A, Marti S, Olasagasti I, Optican LM, Zee DS, Straumann D. Role of cerebellum in motion perception and vestibulo-ocular reflex—similarities and disparities. Cerebellum. 2013;12:97–107.PubMedPubMedCentralCrossRef
13.
go back to reference Dai M, Raphan T, Cohen B. Effects of baclofen on the angular vestibulo-ocular reflex. Exp Brain Res. 2006;171:262–71.PubMedCrossRef Dai M, Raphan T, Cohen B. Effects of baclofen on the angular vestibulo-ocular reflex. Exp Brain Res. 2006;171:262–71.PubMedCrossRef
14.
go back to reference MacDougall HG, Brizuela AE, Burgess AM, Curthoys IS, Halmagyi GM. Patient and normal three-dimensional eye-movement responses to maintained (DC) surface galvanic vestibular stimulation. Otol Neurotol. 2005;26:500–11.PubMedCrossRef MacDougall HG, Brizuela AE, Burgess AM, Curthoys IS, Halmagyi GM. Patient and normal three-dimensional eye-movement responses to maintained (DC) surface galvanic vestibular stimulation. Otol Neurotol. 2005;26:500–11.PubMedCrossRef
15.
go back to reference Krstulovic C, Atrache Al Attrache N, Pérez Garrigues H, Argente-Escrig H, Bataller Alberola L, and Morera Pérez C. Increased velocity storage in subjects with Meniere’s disease. J Int Adv Otol 12:87–91, 2016. Krstulovic C, Atrache Al Attrache N, Pérez Garrigues H, Argente-Escrig H, Bataller Alberola L, and Morera Pérez C. Increased velocity storage in subjects with Meniere’s disease. J Int Adv Otol 12:87–91, 2016.
16.
go back to reference Gensberger KD, Kaufmann AK, Dietrich H, Branoner F, Banchi R, Chagnaud BP, Straka H. Galvanic vestibular stimulation: cellular substrates and response patterns of neurons in the vestibulo-ocular network. J Neurosci. 2016;36:9097–110.PubMedPubMedCentralCrossRef Gensberger KD, Kaufmann AK, Dietrich H, Branoner F, Banchi R, Chagnaud BP, Straka H. Galvanic vestibular stimulation: cellular substrates and response patterns of neurons in the vestibulo-ocular network. J Neurosci. 2016;36:9097–110.PubMedPubMedCentralCrossRef
17.
go back to reference Goldberg JM, Smith CE, Fernández C. Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol. 1984;51:1236–56.PubMedCrossRef Goldberg JM, Smith CE, Fernández C. Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol. 1984;51:1236–56.PubMedCrossRef
18.
go back to reference Kwan A, Forbes PA, Mitchell DE, Blouin J-S, Cullen KE. Neural substrates, dynamics and thresholds of galvanic vestibular stimulation in the behaving primate. Nat Commun. 2019;10:1904.PubMedPubMedCentralCrossRef Kwan A, Forbes PA, Mitchell DE, Blouin J-S, Cullen KE. Neural substrates, dynamics and thresholds of galvanic vestibular stimulation in the behaving primate. Nat Commun. 2019;10:1904.PubMedPubMedCentralCrossRef
19.
go back to reference Fitzpatrick RC, Marsden J, Lord SR, Day BL. Galvanic vestibular stimulation evokes sensations of body rotation. Neuroreport. 2002;13:2379–83.PubMedCrossRef Fitzpatrick RC, Marsden J, Lord SR, Day BL. Galvanic vestibular stimulation evokes sensations of body rotation. Neuroreport. 2002;13:2379–83.PubMedCrossRef
20.
go back to reference Schneider E, Glasauer S, Dieterich M. Comparison of human ocular torsion patterns during natural and galvanic vestibular stimulation. J Neurophysiol. 2002;87:2064–73.PubMedCrossRef Schneider E, Glasauer S, Dieterich M. Comparison of human ocular torsion patterns during natural and galvanic vestibular stimulation. J Neurophysiol. 2002;87:2064–73.PubMedCrossRef
21.
go back to reference MacDougall HG, Brizuela AE, Burgess AM, Curthoys IS. Between-subject variability and within-subject reliability of the human eye-movement response to bilateral galvanic (DC) vestibular stimulation. Exp Brain Res. 2002;144:69–78.PubMedCrossRef MacDougall HG, Brizuela AE, Burgess AM, Curthoys IS. Between-subject variability and within-subject reliability of the human eye-movement response to bilateral galvanic (DC) vestibular stimulation. Exp Brain Res. 2002;144:69–78.PubMedCrossRef
22.
go back to reference SéveracCauquil A, Faldon M, Popov K, Day BL, Bronstein AM. Short-latency eye movements evoked by near-threshold galvanic vestibular stimulation. Exp Brain Res. 2003;148:414–8.CrossRef SéveracCauquil A, Faldon M, Popov K, Day BL, Bronstein AM. Short-latency eye movements evoked by near-threshold galvanic vestibular stimulation. Exp Brain Res. 2003;148:414–8.CrossRef
23.
go back to reference Ruehl RM, Stephan T, Dieterich M, Eulenburg P. P 11 Towards a human vestibular cortex@ Manifold confounders hamper the delineation of vestibular responses in functional neuroimaging. Clin Neurophysiol. 2017;128:e331–2.CrossRef Ruehl RM, Stephan T, Dieterich M, Eulenburg P. P 11 Towards a human vestibular cortex@ Manifold confounders hamper the delineation of vestibular responses in functional neuroimaging. Clin Neurophysiol. 2017;128:e331–2.CrossRef
25.
go back to reference Poldrack RA, Fletcher PC, Henson RN, Worsley KJ, Brett M, Nichols TE. Guidelines for reporting an fMRI study. NeuroImage. 2008;40:409–14.PubMedCrossRef Poldrack RA, Fletcher PC, Henson RN, Worsley KJ, Brett M, Nichols TE. Guidelines for reporting an fMRI study. NeuroImage. 2008;40:409–14.PubMedCrossRef
26.
go back to reference Schneider E, Villgrattner T, Vockeroth J, Bartl K, Kohlbecher S, Bardins S, Ulbrich H, Brandt T. EyeSeeCam: an eye movement-driven head camera for the examination of natural visual exploration. Ann N Y Acad Sci. 2009;1164:461–7.PubMedCrossRef Schneider E, Villgrattner T, Vockeroth J, Bartl K, Kohlbecher S, Bardins S, Ulbrich H, Brandt T. EyeSeeCam: an eye movement-driven head camera for the examination of natural visual exploration. Ann N Y Acad Sci. 2009;1164:461–7.PubMedCrossRef
27.
go back to reference Ruehl RM, Stephan T, Dieterich M, Eulenburg PZ. Voxel-based morphometry delineates the role of the cerebellar tonsil in physiological upbeat nystagmus. J Neurol. 2017;264:13–5.PubMedCrossRef Ruehl RM, Stephan T, Dieterich M, Eulenburg PZ. Voxel-based morphometry delineates the role of the cerebellar tonsil in physiological upbeat nystagmus. J Neurol. 2017;264:13–5.PubMedCrossRef
28.
29.
go back to reference Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith C, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp. 1995;2:189–210.CrossRef Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith C, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp. 1995;2:189–210.CrossRef
30.
go back to reference Friston KJ, Frith C, Turner R, Frackowiak RSJ. Characterizing evoked hemodynamics with fMRI. NeuroImage. 1995;2:157–65.PubMedCrossRef Friston KJ, Frith C, Turner R, Frackowiak RSJ. Characterizing evoked hemodynamics with fMRI. NeuroImage. 1995;2:157–65.PubMedCrossRef
31.
go back to reference Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage. 2009;44:83–98.PubMedCrossRef Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage. 2009;44:83–98.PubMedCrossRef
32.
go back to reference Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage. 2005;25:1325–35.PubMedCrossRef Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage. 2005;25:1325–35.PubMedCrossRef
33.
go back to reference Naidich T, Duvernoy H, Delman B, Sorensen A, Kollias S, and Haacke M. Duvernoy’s atlas of the human brain stem and cerebellum: high-field MRI, surface anatomy, internal structure, vascularization and 3D sectional anatomy. 2009. Naidich T, Duvernoy H, Delman B, Sorensen A, Kollias S, and Haacke M. Duvernoy’s atlas of the human brain stem and cerebellum: high-field MRI, surface anatomy, internal structure, vascularization and 3D sectional anatomy. 2009.
34.
go back to reference Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. NeuroImage. 2006;33:127–38.PubMedCrossRef Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. NeuroImage. 2006;33:127–38.PubMedCrossRef
35.
go back to reference Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL, Smoller JW, Zollei L, Polimeni JR, Fischl B, Liu H, Buckner RL. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106:1125–65.PubMedCrossRef Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL, Smoller JW, Zollei L, Polimeni JR, Fischl B, Liu H, Buckner RL. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106:1125–65.PubMedCrossRef
36.
go back to reference Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BTT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106:2322–45.PubMedPubMedCentralCrossRef Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BTT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106:2322–45.PubMedPubMedCentralCrossRef
37.
go back to reference Yakushin SB, Raphan T, and Cohen B. Coding of velocity storage in the vestibular nuclei. Front Neurol 8:2017. Yakushin SB, Raphan T, and Cohen B. Coding of velocity storage in the vestibular nuclei. Front Neurol 8:2017.
38.
go back to reference Solomon D, Cohen B. Stimulation of the nodulus and uvula discharges velocity storage in the vestibulo-ocular reflex. Exp Brain Res. 1994;102:57–68.PubMedCrossRef Solomon D, Cohen B. Stimulation of the nodulus and uvula discharges velocity storage in the vestibulo-ocular reflex. Exp Brain Res. 1994;102:57–68.PubMedCrossRef
39.
go back to reference Waespe W, Cohen B, Raphan T. Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: effects of lesions. Exp Brain Res. 1983;50:9–33.PubMedCrossRef Waespe W, Cohen B, Raphan T. Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: effects of lesions. Exp Brain Res. 1983;50:9–33.PubMedCrossRef
40.
go back to reference Angelaki DE, Hess BJ. Lesion of the nodulus and ventral uvula abolish steady-state off-vertical axis otolith response. J Neurophysiol. 1995;73:1716–20.PubMedCrossRef Angelaki DE, Hess BJ. Lesion of the nodulus and ventral uvula abolish steady-state off-vertical axis otolith response. J Neurophysiol. 1995;73:1716–20.PubMedCrossRef
41.
go back to reference Angelaki DE, Hess BJ. The cerebellar nodulus and ventral uvula control the torsional vestibulo-ocular reflex. J Neurophysiol. 1994;72:1443–7.PubMedCrossRef Angelaki DE, Hess BJ. The cerebellar nodulus and ventral uvula control the torsional vestibulo-ocular reflex. J Neurophysiol. 1994;72:1443–7.PubMedCrossRef
42.
go back to reference Wearne S, Raphan T, Cohen B. Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula. J Neurophysiol. 1998;79:2690–715.PubMedCrossRef Wearne S, Raphan T, Cohen B. Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula. J Neurophysiol. 1998;79:2690–715.PubMedCrossRef
43.
go back to reference Brodal A, Brodal P. Observations on the secondary vestibulocerebellar projections in the macaque monkey. Exp Brain Res. 1985;58:62–74.PubMedCrossRef Brodal A, Brodal P. Observations on the secondary vestibulocerebellar projections in the macaque monkey. Exp Brain Res. 1985;58:62–74.PubMedCrossRef
44.
go back to reference Coffman KA, Dum RP, Strick PL. Cerebellar vermis is a target of projections from the motor areas in the cerebral cortex. Proc Natl Acad Sci. 2011;108:16068–73.PubMedPubMedCentralCrossRef Coffman KA, Dum RP, Strick PL. Cerebellar vermis is a target of projections from the motor areas in the cerebral cortex. Proc Natl Acad Sci. 2011;108:16068–73.PubMedPubMedCentralCrossRef
45.
go back to reference Luo Y, Onozato T, Wu X, Sasamura K, Sakimura K, Sugihara I. Dense projection of Stilling’s nucleus spinocerebellar axons that convey tail proprioception to the midline area in lobule VIII of the mouse cerebellum. Brain Struct Funct. 2020;225:621–38.PubMedCrossRef Luo Y, Onozato T, Wu X, Sasamura K, Sakimura K, Sugihara I. Dense projection of Stilling’s nucleus spinocerebellar axons that convey tail proprioception to the midline area in lobule VIII of the mouse cerebellum. Brain Struct Funct. 2020;225:621–38.PubMedCrossRef
46.
go back to reference Ruehl RM, Hinkel C, Bauermann T, Eulenburg PZ. Delineating function and connectivity of optokinetic hubs in the cerebellum and the brainstem. Brain Struct Funct. 2017;222:4163–85.PubMedCrossRef Ruehl RM, Hinkel C, Bauermann T, Eulenburg PZ. Delineating function and connectivity of optokinetic hubs in the cerebellum and the brainstem. Brain Struct Funct. 2017;222:4163–85.PubMedCrossRef
47.
go back to reference van Broekhoven PC, Schraa-Tam CK, van der Lugt A, Smits M, Frens MA, van der Geest JN. Cerebellar contributions to the processing of saccadic errors. Cerebellum (London, England). 2009;8:403–15.PubMedCrossRef van Broekhoven PC, Schraa-Tam CK, van der Lugt A, Smits M, Frens MA, van der Geest JN. Cerebellar contributions to the processing of saccadic errors. Cerebellum (London, England). 2009;8:403–15.PubMedCrossRef
48.
go back to reference Bukowska D. Cerebellovestibular projection from the posterior lobe cortex in the rabbit: an experimental study with the retrograde HRP method. I. Topographical relationships. Acta Neurobiol Exp (Wars). 1995;55:23–34.PubMed Bukowska D. Cerebellovestibular projection from the posterior lobe cortex in the rabbit: an experimental study with the retrograde HRP method. I. Topographical relationships. Acta Neurobiol Exp (Wars). 1995;55:23–34.PubMed
49.
go back to reference Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. NeuroImage. 2009;44:489–501.PubMedCrossRef Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. NeuroImage. 2009;44:489–501.PubMedCrossRef
50.
go back to reference Iglói K, Doeller CF, Paradis AL, Benchenane K, Berthoz A, Burgess N, Rondi-Reig L. Interaction between hippocampus and cerebellum Crus I in sequence-based but not place-based navigation. Cereb Cortex. 2015;25:4146–54.PubMedCrossRef Iglói K, Doeller CF, Paradis AL, Benchenane K, Berthoz A, Burgess N, Rondi-Reig L. Interaction between hippocampus and cerebellum Crus I in sequence-based but not place-based navigation. Cereb Cortex. 2015;25:4146–54.PubMedCrossRef
51.
go back to reference Guell X, Schmahmann JD, Gabrieli JDE, and Ghosh SS. Functional gradients of the cerebellum. eLife 7: e36652, 2018. Guell X, Schmahmann JD, Gabrieli JDE, and Ghosh SS. Functional gradients of the cerebellum. eLife 7: e36652, 2018.
53.
go back to reference Rondi-Reig L, Paradis A-L, Lefort JM, Babayan BM, and Tobin C. How the cerebellum may monitor sensory information for spatial representation. Frontiers in systems neuroscience 8: 2014. Rondi-Reig L, Paradis A-L, Lefort JM, Babayan BM, and Tobin C. How the cerebellum may monitor sensory information for spatial representation. Frontiers in systems neuroscience 8: 2014.
54.
go back to reference Yakusheva TA, Blazquez PM, Chen A, Angelaki DE. Spatiotemporal properties of optic flow and vestibular tuning in the cerebellar nodulus and uvula. J Neurosci. 2013;33:15145.PubMedPubMedCentralCrossRef Yakusheva TA, Blazquez PM, Chen A, Angelaki DE. Spatiotemporal properties of optic flow and vestibular tuning in the cerebellar nodulus and uvula. J Neurosci. 2013;33:15145.PubMedPubMedCentralCrossRef
55.
go back to reference Stephan T, Deutschländer A, Nolte A, Schneider E, Wiesmann M, Brandt T, Dieterich M. Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. NeuroImage. 2005;26:721–32.PubMedCrossRef Stephan T, Deutschländer A, Nolte A, Schneider E, Wiesmann M, Brandt T, Dieterich M. Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. NeuroImage. 2005;26:721–32.PubMedCrossRef
56.
go back to reference Helmchen C, Rother M, Spliethoff P, Sprenger A. Increased brain responsivity to galvanic vestibular stimulation in bilateral vestibular failure. NeuroImage Clin. 2019;24:101942–101942.PubMedPubMedCentralCrossRef Helmchen C, Rother M, Spliethoff P, Sprenger A. Increased brain responsivity to galvanic vestibular stimulation in bilateral vestibular failure. NeuroImage Clin. 2019;24:101942–101942.PubMedPubMedCentralCrossRef
57.
go back to reference Walker MF, Tian J, Shan X, Tamargo RJ, Ying H, and Zee DS. The cerebellar nodulus/uvula integrates otolith signals for the translational vestibulo-ocular reflex. PloS One 5:e13981, 2010. Walker MF, Tian J, Shan X, Tamargo RJ, Ying H, and Zee DS. The cerebellar nodulus/uvula integrates otolith signals for the translational vestibulo-ocular reflex. PloS One 5:e13981, 2010.
58.
go back to reference Barmack NH, Shojaku H. Vestibular and visual climbing fiber signals evoked in the uvula-nodulus of the rabbit cerebellum by natural stimulation. J Neurophysiol. 1995;74:2573–89.PubMedCrossRef Barmack NH, Shojaku H. Vestibular and visual climbing fiber signals evoked in the uvula-nodulus of the rabbit cerebellum by natural stimulation. J Neurophysiol. 1995;74:2573–89.PubMedCrossRef
59.
go back to reference Wylie DR, De Zeeuw CI, Digiorgi PL, Simpson JI. Projections of individual Purkinje cells of identified zones in the ventral nodulus to the vestibular and cerebellar nuclei in the rabbit. J Comp Neurol. 1994;349:448–63.PubMedCrossRef Wylie DR, De Zeeuw CI, Digiorgi PL, Simpson JI. Projections of individual Purkinje cells of identified zones in the ventral nodulus to the vestibular and cerebellar nuclei in the rabbit. J Comp Neurol. 1994;349:448–63.PubMedCrossRef
61.
go back to reference Fukuda J, Highstein SM, Ito M. Cerebellar inhibitory control of the vestibulo-ocular reflex investigated in rabbit IIIrd nucleus. Exp Brain Res. 1972;14:511–26.PubMedCrossRef Fukuda J, Highstein SM, Ito M. Cerebellar inhibitory control of the vestibulo-ocular reflex investigated in rabbit IIIrd nucleus. Exp Brain Res. 1972;14:511–26.PubMedCrossRef
62.
64.
go back to reference Shojaku H, Grudt TJ, Barmack NH. Vestibular and visual signals in the ventral paraflocculus of the cerebellum in rabbits. Neurosci Lett. 1990;108:99–104.PubMedCrossRef Shojaku H, Grudt TJ, Barmack NH. Vestibular and visual signals in the ventral paraflocculus of the cerebellum in rabbits. Neurosci Lett. 1990;108:99–104.PubMedCrossRef
65.
go back to reference Pierrot-Deseilligny C. Effect of gravity on vertical eye position. Ann N Y Acad Sci. 2009;1164:155–65.PubMedCrossRef Pierrot-Deseilligny C. Effect of gravity on vertical eye position. Ann N Y Acad Sci. 2009;1164:155–65.PubMedCrossRef
66.
go back to reference Stoodley CJ, MacMore JP, Makris N, Sherman JC, and Schmahmann JD. Location of lesion determines motor vs. cognitive consequences in patients with cerebellar stroke. NeuroImage Clin 12:765–775, 2016. Stoodley CJ, MacMore JP, Makris N, Sherman JC, and Schmahmann JD. Location of lesion determines motor vs. cognitive consequences in patients with cerebellar stroke. NeuroImage Clin 12:765–775, 2016.
67.
go back to reference Kröller J, Behrens F, Marlinsky VV. The velocity storage mechanism of the optokinetic nystagmus under apparent stimulus movements in squirrel monkeys. J Vestib Res. 1997;7:441–51.PubMedCrossRef Kröller J, Behrens F, Marlinsky VV. The velocity storage mechanism of the optokinetic nystagmus under apparent stimulus movements in squirrel monkeys. J Vestib Res. 1997;7:441–51.PubMedCrossRef
Metadata
Title
In Vivo Localization of the Human Velocity Storage Mechanism and Its Core Cerebellar Networks by Means of Galvanic-Vestibular Afternystagmus and fMRI
Authors
Maxine Rühl
Rebecca Kimmel
Matthias Ertl
Julian Conrad
Peter zu Eulenburg
Publication date
01-04-2023
Publisher
Springer US
Keyword
Nystagmus
Published in
The Cerebellum / Issue 2/2023
Print ISSN: 1473-4222
Electronic ISSN: 1473-4230
DOI
https://doi.org/10.1007/s12311-022-01374-8

Other articles of this Issue 2/2023

The Cerebellum 2/2023 Go to the issue

Advances in Alzheimer's

Alzheimer's research and care is changing rapidly. Keep up with the latest developments from key international conferences, together with expert insights on how to integrate these advances into practice.

This content is intended for healthcare professionals outside of the UK.

Supported by:
  • Lilly
Developed by: Springer Healthcare IME
Learn more