Vestibular compensation is the process by which the central nervous system (CNS) attempts to adapt to the loss of vestibular sensory inputs. As such, the compensation process is critically involved in the vestibular rehabilitation programs that are implemented by physical therapists for patients with vestibular disorders. One hypothesis regarding vestibular compensation, which has persisted in some of the published vestibular compensation literature and particularly on some vestibular and physical therapy websites, is the ‘cerebellar shutdown’ or ‘cerebellar clampdown’ hypothesis proposed by McCabe and Ryu in 1969. This hypothesis proposes that the cerebellum inhibits neuronal activity in the bilateral vestibular nuclei (VN) following unilateral vestibular loss (UVL), causing the VN contralateral to the UVL to be electrically silent during the early phases of vestibular compensation. Despite a wealth of evidence against this idea, it has gained traction amongst some physical therapists and has implications for vestibular rehabilitation early in the compensation process.
CONCLUSIONS:
In this paper it is argued that the ‘cerebellar shutdown’ or ‘clampdown’ hypothesis is inconsistent with well accepted neurophysiological and imaging evidence and that it is also logically flawed.
McCabeB.F. and RyuJ.H., Experiments on vestibular compensation, Laryng79 (1969), 1728–1736.
2.
SchaeferK.-P. and Meyer.D.L., Compensation of vestibular lesions. In H.H. Kornhuber (Ed.), Handbook of Sensory Physiology. Vol. Vl/2. Springer. Berlin, (1974), pp. 463–490.
3.
VidalP.P., de WaeleC., VibertN. and MühlethalerM., Vestibular compensation revisited, Otolaryngol Head Neck Surg119 (1998), 34–42.
4.
BrandtT., Vertigo: Its Multisensory Syndromes. 2nd Edition. Springer, NY. 2003
5.
TjernströmF., FranssonPA., KahlonB., KarlbergM., LindbergS., SiesjöP. and MagnussonM., Different visual weighting due to fast or slow vestibular deafferentation: Before and after schwannoma surgery, Neural Plast2019 (2019), 4826238.
BerthozA., The role of gaze in compensation of vestibular disfunction: the gaze substitution hypothesis, Prog Brain Res76 (1988), 411–420.
11.
MaedaM., Mechanisms of vestibular compensation in the unilateral labyrinthectomized cat, Prog Brain Res76 (1988), 385–394.
12.
SmithP.F. and CurthoysI.S., Mechanisms of recovery from unilateral labyrinthectomy: A review, Brain Res Revs14 (1989), 155–180.
13.
CurthoysI.S. and HalmagyiG.M., Vestibular compensation: A review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss, J Vestib Res5 (1995), 67–107.
14.
DieringerN., “Vestibular compensation”: neural plasticity and its relations to functional recovery after labyrinthine lesions in frogs and other vertebrates, Prog Neurobiol46 (1995), 97–129.
15.
CurthoysI.S., Vestibular compensation and substitution, Curr Opin Neurol13(1) (2000), 27–30.
16.
DarlingtonC.L., DutiaM.B. and SmithP.F., The contribution of the intrinsic properties of vestibular nucleus neurones to recovery from vestibular damage, Eur J Neurosci15 (2002), 1719–1727.
17.
CullenK.E., MinorL.B., BeraneckM. and SadeghiS.G., Neural substrates underlying vestibular compensation: contribution of peripheral versus central processing, J Vestib Res19 (2009), 171–182.
McCallA.A. and YatesB.J., Compensation following bilateral vestibular damage, Front Neurol2 (2011), 88.
20.
LacourM., HelmchenC. and VidalP.P., Vestibular compensation: the neuro-otologist’s best friend, J Neurol263(Suppl 1) (2016), S54–64.
21.
SmithP.F., Vestibular compensation as a distributed process. In: Reference Module in Neuroscience and Biobehavioral Psychology. Ed (H. Straka), Elsevier, NY. https://doi.org/10.1016/B978-0-12-809324-5.23820-0. pp. 1–17. 2019.
22.
McCabeB.F., RyuJ.H. and SekitaniT., Further experiments on vestibular compensation, Laryng82 (1972), 381–396.
23.
LacourM., RollJ.P. and AppaixM., Modifications and development of spinal reflexes in the alert baboon () following a unilateral vestibular neurotomy, Brain Res113 (1976), 255–269.
24.
GrestyM.A., HessK. and LeechJ., Disorders of the vestibulo-ocular reflex producing oscillopsia and mechanisms compensating for loss of labyrinthine function, Brain100 (1977), 693–716.
25.
BorelL., HarlayF., LopezC., MagnanJ., ChaysA. and LacourM., Walking performance in vestibular-defective patients before and after unilateral vestibular neurectomy, Behav Brain Res150 (2004), 191–200.
26.
PeterkaR.J., StatlerK.D., WrisleyD.M. and HorakF.B., Postural compensation for unilateral vestibular loss, Front Neurol2 (2011), 57.
27.
PrechtW., ShimazuH. and MarkhamC.H., A mechanism of central compensation of vestibular function following hemilabyrinthectomy, J Neurophysiol29 (1966), 996–1010.
28.
ReidS., MaoiliC. and PrechtW., Vestibular nuclear neuron activity in chronically hemilabyrinthectomzed cats, Acta Otolaryngol (Stockh.)98 (1984), 1–13.
29.
YagiT. and MarkhamC.H., Neural correlates of compensation after hemimlabyrinthectomy, Exp Neurol84(1) (1984), 98–108.
30.
HamannK.F. and LannouJ., Dynamic characteristics of vestibular nuclear neurons responses to vestibular and optokinetic stimulation during vestibular compensation in the rat, Acta OtolaryngolSuppl 455 (1987), 1–19.
31.
SmithP.F. and CurthoysI.S., Neuronal activity in the contralateral medial vestibular nucleus of the guinea pig following unilateral labyrinthectomy, Brain Res444 (1988), 295–307.
32.
SmithP.F. and CurthoysI.S., Neuronal activity in the ipsilateral medial vestibular nucleus of the guinea pig following unilateral labyrinthectomy, Brain Res444 (1988), 308–319.
33.
NewlandsS.D. and PerachioA.A., Compensation of horizontal canal related activity in the medial vestibular nucleus following unilateral labyrinth ablation in the decerebrate gerbil. I. Type I neurons, Exp Brain Res82(2) (1990), 359–372.
34.
RisL., CapronB., de WaeleC., VidalP.P. and GodauxE., Dissociations between behavioural recovery and restoration of vestibular activity in the unilabyrinthectomized guinea-pig, J Physiol500(Pt 2) (1997), 509–522.
35.
RisL., De WaeleC., SerafinM., VidalP.P. and GodauxE., Neuronal activity in the ipsilateral vestibular nucleus following unilateral labyrinthectomy in the alert guinea pig, J Neurophysiol74 (1995), 2087–2099.
36.
RisL. and GodauxE., Neuronal activity in the vestibular nuclei after contralateral or bilateral labyrinthectomy in the alert guinea pig, J Neurophysiol80 (1998), 2352–2367.
37.
BeraneckM., HachemaouiM., IdouxE., RisL., UnoA. and GodauxE., Long-term plasticity of ipsilesional medial vestibular nucleus neurons after unilateral labyrinthectomy, J Neurophysiol90 (2003), 184–203.
38.
BeraneckM. and IdouxE., Reconsidering the role of neuronal intrinsic properties and neuromodulation in vestibular homeostasis, Front Neurol3 (2012), 25.
39.
BeraneckM., IdouxE., UnoA., VidalP.P., MooreL.E. and VibertN., Unilateral labyrinthectomy modifies the membrane properties of contralesional vestibular neurones, J Neurophysiol92 (2004), 1668–1684.
40.
SadeghiS.G., MinorL.B. and CullenK.E., Neural correlates of sensory substitution in vestibular pathways following complete vestibular loss, J Neurosci32(42) (2012), 14685–14695.
41.
NewlandsS.D., LinN. and WeiM., Responses of non-eye movement central vestibular neurons to sinusoidal horizontal translation in compensated macaques after unilateral labyrinthectomy, J Neurophysiol112(1) (2014), 9–21.
42.
NewlandsS.D. and WeiM., Responses of central vestibular neurons to sinusoidal yaw rotation in compensated macaques after unilateral labyrinthectomy, J Neurophysiol110(8) (2013), 1822–1836.
43.
LacourM., ManzoniD., PompeianoO. and XerriC., Central compensation of vestibular deficits. III. Response characteristics of lateral vestibular neurons to roll tilt after contralateral labyrinth deafferentation, J Neurophysiol54(4) (1985), 988–1005.
44.
ShimazuH. and PrechtW., Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway, J Neurophysiol29(3) (1966), 467–492.
45.
StrakaH., FritzschB. and GloverJ.C., Connecting ears to eye muscles: evolution of a ‘simple’ reflex arc, Brain Behav Evol83(2) (2014), 162–175.
46.
LlinasR. and WaltonK., Vestibular compensation: a distributed property of the central nervous system. In H. Asanuma and V.J.Wilson (Eds.), Integration in the Nervous System, Igaku-Shon, Tokyo, (1979), pp. 145–166.
47.
FlohrH., BienholdH., AbelnW. and MacskovicsI., Concepts of vestibular compensation. In H. Flohr andW. Precht (Eds.), Lesion-Induced Neuronal Plasticity in Sensorimotor Systems, Springer, Amsterdam, (1981), pp. 153–172.
48.
PatricksonJ.W., BryantH.J., KaderkaroM. and KutynaF.A., A quantitative [14C]2-deoxy-D-glucose study of brainstem nuclei during horizontal nystagmus induced by lesioning the lateral crista ampullaris of the rat, Exp Brain Res60 (1985), 227–234.
49.
LuytenW.H.M.L., SharpF.R. and RyanA.F., Regional differences of brain glucose metabolic compensation after unilateral labyrinthectomy in rats: a [14C)2-deoxy- glucose study, Brain Res373 (1986), 68–80.
50.
GliddonC., DarlingtonC.L. and SmithP.F., Rapid vestibular compensation in guinea pig even with prolonged anesthesia, Neurosci Letts371 (2004), 138–141.
51.
YuX.J., ThomassenJ.S., DickmanJ.D., NewlandsS.D. and AngelakiD.E., Long-term deficits in motion detection thresholds and spike count variability after unilateral vestibular lesion, J Neurophysiol112(4) (2014), 870–89.
52.
HalmagyiG.M., ChenL., MacDougallH.G., WeberK.P., McGarvieL.A. and CurthoysI.S., The video head impulse test, Front Neurol8 (2017), 258.
53.
HübnerP.P., KhanS.I. and MigliaccioA.A., The mammalian efferent vestibular system plays a crucial role in vestibulo-ocular reflex compensation after unilateral labyrinthectomy, J Neurophysiol117(4) (2017), 1553–1568.
54.
SadeghiS.G., MinorL.B. and CullenK.E., Response of vestibular nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy, J Neurophysiol97 (2007), 1503–1514.
55.
CurthoysI.S., HarrisR.A. and SmithP.F., The effect of unilateral labyrinthectomy on neural activity in the guinea pig vestibular nuclei. In M.D. Graham and J.L. Kemink (Eds.), The Vestibular System: Neurophysiologic and Clinical Research, Raven, New York, (1987), pp. 677–687.
56.
BalabanC.D. and RomeroG.G., A role of climbing fibers in regulation of flocculonodular lobe protein kinase C expression during vestibular compensation, Brain Res804(2) (1998), 253–265.
57.
CirelliC., PompeianoM., D’AscanioP., ArrighiP. and PompeianoO., c-Fos expression in the rat brain after unilateral labyrinthectomy and its relation to the uncompensated and compensated stages, Neurosci70(2) (1996), 515–546.
58.
GotoM.M., RomeroG.G. and BalabanC.D., Transient changes in flocculonodular lobe protein kinase C expression during vestibular compensation, J Neurosci17(11) (1997), 4367–4381.
59.
KimH.J., CokerN.J. and HenleyC.M., Polyamines increase in the brainstem and cerebellum following labyrinthectomy, Am J Otol18(2) (1997), 214–222.
60.
KimM.S., JinB.K., ChunS.W., LeeM.Y, LeeS.H., KimJ.H. and ParkB.R., Role of vestibulocerebellar N-methyl-D-aspartate receptors for behavioral recovery following unilateral labyrinthectomy in rats, Neurosci Letts222(3) (1997), 171–174.
61.
KitaharaT., TakedaN., EmsonP.C., KuboT. and KiyamaH., Changes in nitric oxide synthase-like immunoreactivities in unipolar brush cells in the rat cerebellar flocculus after unilateral labyrinthectomy, Brain Res765(1) (1997), 1–6.
62.
KitaharaT., TakedaN., SaikaT., KuboT. and KiyamaH., Role of the flocculus in the development of vestibular compensation: immunohistochemical studies with retrograde tracing and flocculectomy using Fos expression as a marker in the rat brainstem, Neurosci76(2) (1997), 571–580.
63.
KitaharaT., TakedaN., KuboT. and KiyamaH., Nitric oxide in the flocculus works the inhibitory neural circuits after unilateral labyrinthectomy, Brain Res815(2) (1999), 405–409.
64.
KitaharaT., TakedaN., UnoA., KuboT., MishinaM. and KiyamaH., Unilateral labyrinthectomy downregulates glutamate receptor delta-2 expression in the rat vestibulocerebellum, Mol Brain Res61(1-2) (1998), 170–178.
65.
D’AscanioP., ArrighiP., FascettiF. and PompeianoO., Effects of unilateral labyrinthectomy on the norepinephrine content in forebrain and cerebellar structures of albino rats, Arch Ital Biol138(3) (2000), 241–270.
66.
NecchilD., ScheriniE., BottaL., SoldaniC., ValliP. and BernocchiG., Morphological changes in the frog cerebellar cortex after unilateral section of the statoacustic nerve, Eur J Histochem46(4) (2002), 317–328.
67.
PisuM.B., ConfortiE., BottaL., ValliP. and BernocchiG., Nitric oxide synthase in the frog cerebellum: response of Purkinje neurons to unilateral eighth nerve transection, Anat Rec268(1) (2002), 73–83.
68.
ShinderM.E., PerachioA.A. and KaufmanG.D., Fos responses to short-term adaptation of the horizontal vestibuloocular reflex before and after vestibular compensation in the Mongolian gerbil, Brain Res1050(1-2) (2005), 79–93.
69.
ShinderM.E., RamanathanM.Jr and KaufmanG.D., Asymmetric gene expression in the brain during acute compensation to unilateral vestibular labyrinthectomy in the Mongolian gerbil, J Vestib Res16(4-5) (2006), 147–169.
70.
FukasawaM., OkamotoK., NakamuraM., MikamiK., ShimadaS., TanakaY., NagaiK., AritoM., KurokawaM.S., MasukoK., SuematsuN., KoizukaI. and KatoT., Proteomic analysis of the rat cerebellar flocculus during vestibular compensation, J Vestib Res19(3-4) (2009), 83–94.
71.
ParkB.R., ChoiM.A. and HongS.M., Temporal changes of calbindin expression in the nodulus following unilateral labyrinthectomy in rats, Neurosci Letts555 (2013), 47–50.
72.
ZhouW., ZhouL.Q., ZhangS.L., LiuB., LengY.M., ZhouR.H. and KongW.J., The changes in mGluR2 and mGluR7 expression in rat medial vestibular nucleus and flocculus following unilateral labyrinthectomy, Int J Mol Sci14(11) (2013), 22857–22875.
73.
ZhouL., ZhouW., ZhangS., LiuB., LiangP., ZhouY., ZhouT., ZhangK., LengY. and KongW., BDNF signaling in the rat cerebello-vestibular pathway during vestibular compensation: BDNF signaling in vestibular compensation, FEBS J282(18) (2015), 3579–3591.
74.
ZhouL., ZhouW., ZhangS., LiuB., LengY., ZhouR. and KongW., Changes in histamine receptors (H1, H2, and H3) expression in rat medial vestibular nucleus and flocculus after unilateral labyrinthectomy: Histamine receptors in vestibular compensation, PLoS One8(6) (2013), e66684.
75.
CourjonJ.H., FlandrinJ.M., JeannerodM. and SchmidR., The role of the flocculus in vestibular compensation after hemilabyrinthectomy, Brain Res239 (1982), 251–257.
76.
JeannerodM., CourjonJ.H., FlandrinJ.M. and SchmidR., Supravestibular control of vestibular compensation after hemilabyrinthectomy in the cat. In H. Flohr and W. Precht (Eds.), Lesion-Induced Neuronal Plasticity in Sensorimotor Systems, Springer, Berlin, (1981), pp. 208–220.
77.
KitaharaT., FukushimaM., TakedaN., SaikaT. and KuboT., Effects of pre-flocculectomy on Fos expression and NMDA receptor-mediated neural circuits in the central vestibular system after unilateral labyrinthectomy, Acta Otolaryngol120(7) (2000), 866–871.
78.
IgarashiM. and IshikawaK., Post-labyrinthectomy balance compensation and preplacement of cerebellar vermis lesion, Acta Otolaryngol99 (1985), 452–458.
79.
HaddadG.M., FriendlichA.R. and RobinsonD.A., Compensation of nystagmus after Vlllth nerve lesions in vestibulo-cerebellectomized cats, Brain Res135 (1977), 192–196.
80.
AleisaM., ZeitouniA.G. and CullenK.E., Vestibular compensation after unilateral labyrinthectomy: normal versus cerebellar dysfunctional mice, J Otolaryngol36(6) (2007), 315–321.
81.
BeraneckM., McKeeJ.L., AleisaM. and CullenK.E., Asymmetric recovery in cerebellar-deficient mice following unilateral labyrinthectomy, J Neurophysiol100 (2008), 945–958.
82.
MarkhamC.H., YagiT. and CurthoysI.S., The contribution of the contralateral labyrinth to second order vestibular neuronal activity in the cat, Brain Res138(1) (1977), 99–109.
83.
BenseS., DieterichM., BuchholzH.G., BartensteinP., SchreckenbergerM. and BrandtT., The differential effects of acute right- vs. left-sided vestibular failure on brain metabolism, Brain Struct Funct219(4) (2014), 1355–1367.
84.
zu EulenburgP., StoeterP. and DieterichM., Voxel-based morphometry depicts central compensation after vestibular neuritis, Ann Neurol68(2) (2010), 241–249.
85.
ZwergalA., SchlichtigerJ., XiongG., BeckR., GüntherL., SchnieppR., SchöberlF., JahnK., BrandtT., StruppM., BartensteinP., DieterichM., DutiaM.B. and la FougèreC., Sequential (18)F]FDG μPET whole-brain imaging of central vestibular compensation: a model of deafferentation-induced brain plasticity, Brain Struct Funct221(1) (2016), 159–170.
86.
AllumJ.H.J., SchetingaA. and HonnegerF., The effect of peripheral vestibular recovery on improvements in vestibulo-ocular reflexes and balance control after acute unilateral peripheral vestibular loss, Otol Neurotol38 (2017), e531–e538.
