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Plastic Events of the Vestibular Nucleus: the Initiation of Central Vestibular Compensation

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Abstract

Vestibular compensation is a physiological response of the vestibular organs within the inner ear. This adaptation manifests during consistent exposure to acceleration or deceleration, with the vestibular organs incrementally adjusting to such changes. The molecular underpinnings of vestibular compensation remain to be fully elucidated, yet emerging studies implicate associations with neuroplasticity and signal transduction pathways. Throughout the compensation process, the vestibular sensory neurons maintain signal transmission to the central equilibrium system, facilitating adaptability through alterations in synaptic transmission and neuronal excitability. Notable molecular candidates implicated in this process include variations in ion channels and neurotransmitter profiles, as well as neuronal and synaptic plasticity, metabolic processes, and electrophysiological modifications. This study consolidates the current understanding of the molecular events in vestibular compensation, augments the existing research landscape, and evaluates contemporary therapeutic strategies. Furthermore, this review posits potential avenues for future research that could enhance our comprehension of vestibular compensation mechanisms.

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Abbreviations

ACh:

Acetylcholine

AchE:

Acetylcholinesterase

ACTH:

Adrenocorticotropic hormone

AraC:

Cytosine-β-D arabinofuranoside

AVP:

Arginine vasopressin

BDNF:

Brain-derived neurotrophic factor

BK:

Calcium-activated K+ Big conductance

BrdU:

Bromodeoxyuridine

CAMKII:

Calmodulin-dependent kinase II

CNS,:

Central nervous system

CO:

Cytochrome oxygenase

CRH,:

Corticotropin-releasing hormone

ENS:

Enteric nervous system

HCN:

Hyperpolarization-activated cyclic nucleotide-gated

HPA:

Hypothalamus-pituitary-adrenal

IEGs:

Immediate early genes

IO:

Inferior olive

KCC2:

K(+)-Cl(-) cotransporter isoform 2

L-T4:

L-Thyroxine

LVN:

Lateral vestibular nucleus

MnSOD:

Manganese superoxide dismutase

MVN:

Medial vestibular nucleus

NF-κB:

Nuclear factor kappa B

NGF:

Nerve growth factor

NPH:

Nucleus prepositus hypoglossi

NT:

Nerve growth factor

NT3:

Neurotrophic factor 3

NT4:

Neurotrophic factor 4

NT5:

Neurotrophic factor 5

NTs:

Neurotrophins

PKC:

Protein kinase C

PNS:

Peripheral nervous system

PVN:

Paraventricular nucleus

SK:

Calcium-activated K+ small conductance

TH:

Thyroid hormone

TNF-α:

Tumor necrosis factor alpha

TrkB:

Tyrosine receptor kinase B

UBCs:

Unipolar brush cells

UL:

Unilateral labyrinthectomy

UVD:

Unilateral vestibular deafferentation

UVL:

Unilateral vestibular lesion

UVN:

Unilateral vestibular neurectomy

VN:

Vestibular nucleus

VNCs:

Vestibular nucleus complexes

VOR:

Vestibular-ocular reflex

2DG:

2-deoxyglucose

References

  1. Ferrè ER, Longo MR, Fiori F et al (2013) Vestibular modulation of spatial perception. Front Hum Neurosci 7:660

    Article  PubMed  PubMed Central  Google Scholar 

  2. Angelaki DE, Klier EM, Snyder LH (2009) A vestibular sensation: probabilistic approaches to spatial perception. Neuron 64:448–461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Lacour M, Borel L (1993) Vestibular control of posture and gait. Arch Ital Biol 131:81–104

    CAS  PubMed  Google Scholar 

  4. Lacour M, Tighilet B (2010) Plastic events in the vestibular nuclei during vestibular compensation: the brain orchestration of a “deafferentation” code. Restor Neurol Neurosci 28:19–35

    PubMed  Google Scholar 

  5. Ris L, de Waele C, Serafin M et al (1995) Neuronal activity in the ipsilateral vestibular nucleus following unilateral labyrinthectomy in the alert guinea pig. J Neurophysiol 74:2087–2099

    Article  CAS  PubMed  Google Scholar 

  6. Smith PF, Curthoys IS (1989) Mechanisms of recovery following unilateral labyrinthectomy: a review. Brain Res Brain Res Rev 14:155–180

    Article  CAS  PubMed  Google Scholar 

  7. Curthoys IS (2000) Vestibular compensation and substitution. Curr Opin Neurol 13:27–30

    Article  CAS  PubMed  Google Scholar 

  8. Straka H, Vibert N, Vidal PP et al (2005) Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity. Prog Neurobiol 76:349–392

    Article  CAS  PubMed  Google Scholar 

  9. Dugas JC, Cuellar TL, Scholze A et al (2010) Dicer1 and miR-219 Are required for normal oligodendrocyte differentiation and myelination. Neuron 65:597–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Beraneck M, Idoux E (2012) Reconsidering the role of neuronal intrinsic properties and neuromodulation in vestibular homeostasis. Front Neurol 3:25

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kaufman GD, Anderson JH, Beitz AJ (1992) Brainstem Fos expression following acute unilateral labyrinthectomy in the rat. Neuroreport 3:829–832

    Article  CAS  PubMed  Google Scholar 

  12. Kitahara T, Takeda N, Saika T et al (1995) Effects of MK801 on Fos expression in the rat brainstem after unilateral labyrinthectomy. Brain Res 700:182–190

    Article  CAS  PubMed  Google Scholar 

  13. Cirelli C, Pompeiano M, D’Ascanio P et al (1996) c-fos Expression in the rat brain after unilateral labyrinthectomy and its relation to the uncompensated and compensated stages. Neuroscience 70:515–546

    Article  CAS  PubMed  Google Scholar 

  14. Darlington CL, Lawlor P, Smith PF et al (1996) Temporal relationship between the expression of fos, jun and krox-24 in the guinea pig vestibular nuclei during the development of vestibular compensation for unilateral vestibular deafferentation. Brain Res 735:173–176

    Article  CAS  PubMed  Google Scholar 

  15. Gustave Dit Duflo S, Gestreau C, Tighilet B et al (1999) Fos expression in the cat brainstem after unilateral vestibular neurectomy. Brain Res 824:1–17

    Article  CAS  PubMed  Google Scholar 

  16. Kitahara T, Fukushima M, Takeda N et al (2000) Effects of pre-flocculectomy on Fos expression and NMDA receptor-mediated neural circuits in the central vestibular system after unilateral labyrinthectomy. Acta Otolaryngol 120:866–871

    Article  CAS  PubMed  Google Scholar 

  17. Kim MS, Kim JH, Jin Y-Z et al (2002) Temporal changes of cFos-like protein expression in medial vestibular nuclei following arsanilate-induced unilateral labyrinthectomy in rats. Neurosci Lett 319:9–12

    Article  CAS  PubMed  Google Scholar 

  18. El Mahmoudi N, Marouane E, Rastoldo G et al (2022) Microglial dynamics modulate vestibular compensation in a rodent model of vestibulopathy and condition the expression of plasticity mechanisms in the deafferented vestibular nuclei. Cells 11:2693

    Article  PubMed  PubMed Central  Google Scholar 

  19. El Mahmoudi N, Rastoldo G, Marouane E et al (2021) Breaking a dogma: acute anti-inflammatory treatment alters both post-lesional functional recovery and endogenous adaptive plasticity mechanisms in a rodent model of acute peripheral vestibulopathy. J Neuroinflammation 18:183

    Article  PubMed  PubMed Central  Google Scholar 

  20. Baizer JS, Corwin WL, Baker JF (2010) Otolith stimulation induces c-Fos expression in vestibular and precerebellar nuclei in cats and squirrel monkeys. Brain Res 1351:64–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Liberge M, Manrique C, Bernard-Demanze L et al (2010) Changes in TNFα, NFκB and MnSOD protein in the vestibular nuclei after unilateral vestibular deafferentation. J Neuroinflammation 7:91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Bolger C, Sansom AJ, Smith PF et al (1999) An antisense oligonucleotide to brain-derived neurotrophic factor delays postural compensation following unilateral labyrinthectomy in guinea pig. Neuroreport 10:1485–1488

    Article  CAS  PubMed  Google Scholar 

  23. Montcouquiol ME, Sans NA, Travo C et al (2000) Detection and localization of BDNF in vestibular nuclei during the postnatal development of the rat. Neuroreport 11:1401–1405

    Article  CAS  PubMed  Google Scholar 

  24. Maingay MG, Sansom AJ, Kerr DR et al (2000) The effects of intra-vestibular nucleus administration of brain-derived neurotrophic factor (BDNF) on recovery from peripheral vestibular damage in guinea pig. Neuroreport 11:2429–2432

    Article  CAS  PubMed  Google Scholar 

  25. Dutheil S, Watabe I, Sadlaoud K et al (2016) BDNF signaling promotes vestibular compensation by increasing neurogenesis and remodeling the expression of potassium-chloride cotransporter KCC2 and GABAA receptor in the vestibular nuclei. J Neurosci 36:6199–6212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Mao D, He Z, Xuan W et al (2021) Effect and mechanism of BDNF/TrkB signaling on vestibular compensation. Bioengineered 12:11823–11836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Dutheil S, Escoffier G, Gharbi A et al (2013) GABA(A) receptor agonist and antagonist alter vestibular compensation and different steps of reactive neurogenesis in deafferented vestibular nuclei of adult cats. J Neurosci 33:15555–15566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Yamanaka T, Him A, Cameron SA et al (2000) Rapid compensatory changes in GABA receptor efficacy in rat vestibular neurones after unilateral labyrinthectomy. J Physiol 523(Pt 2):413–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gliddon CM, Darlington CL, Smith PF (2005) GABAergic systems in the vestibular nucleus and their contribution to vestibular compensation. Prog Neurobiol 75:53–81

    Article  CAS  PubMed  Google Scholar 

  30. Heskin-Sweezie R, Titley HK, Baizer JS et al (2010) Type B GABA receptors contribute to the restoration of balance during vestibular compensation in mice. Neuroscience 169:302–314

    Article  CAS  PubMed  Google Scholar 

  31. Shao M, Reddaway R, Hirsch JC et al (2012) Presynaptic GABA(B) receptors decrease neurotransmitter release in vestibular nuclei neurons during vestibular compensation. Neuroscience 223:333–354

    Article  CAS  PubMed  Google Scholar 

  32. Phelan KD, Gallagher JP (1992) Direct muscarinic and nicotinic receptor-mediated excitation of rat medial vestibular nucleus neurons in vitro. Synapse 10:349–358

    Article  CAS  PubMed  Google Scholar 

  33. Sun Y, Waller HJ, Godfrey DA et al (2002) Spontaneous activity in rat vestibular nuclei in brain slices and effects of acetylcholine agonists and antagonists. Brain Res 934:58–68

    Article  CAS  PubMed  Google Scholar 

  34. Tighilet B, Trottier S, Mourre C et al (2006) Changes in the histaminergic system during vestibular compensation in the cat. J Physiol 573:723–739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Tighilet B, Mourre C, Trottier S et al (2007) Histaminergic ligands improve vestibular compensation in the cat: behavioural, neurochemical and molecular evidence. Eur J Pharmacol 568:149–163

    Article  CAS  PubMed  Google Scholar 

  36. Tighilet B, Mourre C, Lacour M (2014) Plasticity of the histamine H3 receptors after acute vestibular lesion in the adult cat. Front Integr Neurosci 7:87

    Article  PubMed  PubMed Central  Google Scholar 

  37. Tighilet B, Lacour M (2001) Gamma amino butyric acid (GABA) immunoreactivity in the vestibular nuclei of normal and unilateral vestibular neurectomized cats. Eur J Neurosci 13:2255–2267

    Article  CAS  PubMed  Google Scholar 

  38. Tighilet B, Brezun JM, Sylvie GDD et al (2007) New neurons in the vestibular nuclei complex after unilateral vestibular neurectomy in the adult cat. Eur J Neurosci 25:47–58

    Article  PubMed  Google Scholar 

  39. Bergquist F, Ruthven A, Ludwig M et al (2006) Histaminergic and glycinergic modulation of GABA release in the vestibular nuclei of normal and labyrinthectomised rats. J Physiol 577:857–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Chen Z-P, Zhang X-Y, Peng S-Y et al (2019) Histamine H1 receptor contributes to vestibular compensation. J Neurosci 39:420–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Alice C, Paul AE, Sansom AJ et al (1998) The effects of steroids on vestibular compensation and vestibular nucleus neuronal activity in the guinea pig. J Vestib Res 8:201–207

    Article  CAS  PubMed  Google Scholar 

  42. Yamamoto T, Yamanaka T, Matsunaga T (2000) The effect of stress application on vestibular compensation. Acta Otolaryngol 120:504–507

    Article  CAS  PubMed  Google Scholar 

  43. Licata F, Li Volsi G, Maugeri G et al (1993) Effects of noradrenaline on the firing rate of vestibular neurons. Neuroscience 53:149–158

    Article  CAS  PubMed  Google Scholar 

  44. Podda MV, Johnston AR, Tolu E et al (2001) Modulation of rat medial vestibular nucleus neurone activity by vasopressin and noradrenaline in vitro. Neurosci Lett 298:91–94

    Article  CAS  PubMed  Google Scholar 

  45. Di Mauro M, Bronzi D, Li Volsi G et al (2008) Noradrenaline modulates neuronal responses to GABA in vestibular nuclei. Neuroscience 153:1320–1331

    Article  PubMed  Google Scholar 

  46. Cai J, Li J, Mao Y et al (2013) Immunohistochemical localization of α2-adrenergic receptors in the neonatal rat cochlea and the vestibular labyrinth. J Mol Neurosci 51:1010–1020

    Article  CAS  PubMed  Google Scholar 

  47. Wersinger E, Gaboyard-Niay S, Travo C et al (2013) Symptomatic treatment of vestibular deficits: therapeutic potential of histamine H4 receptors. J Vestib Res 23:153–159

    Article  PubMed  Google Scholar 

  48. Sadlaoud K, Tazerart S, Brocard C et al (2010) Differential plasticity of the GABAergic and glycinergic synaptic transmission to rat lumbar motoneurons after spinal cord injury. J Neurosci 30:3358–3369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Nelson AB, Faulstich M, Moghadam S et al (2017) BK channels are required for multisensory plasticity in the oculomotor system. Neuron 93:211–220

    Article  CAS  PubMed  Google Scholar 

  50. van Welie I, du Lac S (2011) Bidirectional control of BK channel open probability by CAMKII and PKC in medial vestibular nucleus neurons. J Neurophysiol 105:1651–1659

    Article  PubMed  PubMed Central  Google Scholar 

  51. Tighilet B, Bourdet A, Péricat D et al (2021) SK channels modulation accelerates equilibrium recovery in unilateral vestibular neurectomized rats. Pharmaceuticals:14. https://doi.org/10.3390/ph14121226

  52. Tighilet B, Leonard J, Mourre C et al (2019) Apamin treatment accelerates equilibrium recovery and gaze stabilization in unilateral vestibular neurectomized cats: cellular and behavioral aspects. Neuropharmacology. 144:133–142

    Article  CAS  PubMed  Google Scholar 

  53. Tighilet B, Chabbert C (2019) Adult neurogenesis promotes balance recovery after vestibular loss. Prog Neurobiol 174:28–35

    Article  PubMed  Google Scholar 

  54. Campos-Torres A, Touret M, Vidal PP et al (2005) The differential response of astrocytes within the vestibular and cochlear nuclei following unilateral labyrinthectomy or vestibular afferent activity blockade by transtympanic tetrodotoxin injection in the rat. Neuroscience 130:853–865

    Article  CAS  PubMed  Google Scholar 

  55. Dutheil S, Lacour M, Tighilet B (2011) Neurogenic potential of the vestibular nuclei and behavioural recovery time course in the adult cat are governed by the nature of the vestibular damage. PLoS One 6:e22262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Dutheil S, Brezun JM, Leonard J et al (2009) Neurogenesis and astrogenesis contribution to recovery of vestibular functions in the adult cat following unilateral vestibular neurectomy: cellular and behavioral evidence. Neuroscience 164:1444–1456

    Article  CAS  PubMed  Google Scholar 

  57. Rastoldo G, El Mahmoudi N, Marouane E et al (2021) Adult and endemic neurogenesis in the vestibular nuclei after unilateral vestibular neurectomy. Prog Neurobiol 196:101899

    Article  CAS  PubMed  Google Scholar 

  58. Raymond J, Ez-Zaher L, Demêmes D et al (1991) Quantification of synaptic density changes in the medial vestibular nucleus of the cat following vestibular neurectomy. Restor Neurol Neurosci 3:197–203

    CAS  PubMed  Google Scholar 

  59. Li H, Dokas LA, Godfrey DA et al (2002) Remodeling of synaptic connections in the deafferented vestibular nuclear complex. J Vestib Res 12:167–183

    Article  PubMed  Google Scholar 

  60. C T, S G-N, C C. (2012) Plasticity of Scarpa’s ganglion neurons as a possible basis for functional restoration within vestibular endorgans. Front Neurol:3. https://doi.org/10.3389/fneur.2012.00091

  61. Curran T, Abate C, Cohen DR et al (1990) Inducible proto-oncogene transcription factors: third messengers in the brain? Cold Spring Harb Symp Quant Biol 55:225–234

    Article  CAS  PubMed  Google Scholar 

  62. Klein RL, Muir D, King MA et al (1999) Long-term actions of vector-derived nerve growth factor or brain-derived neurotrophic factor on choline acetyltransferase and Trk receptor levels in the adult rat basal forebrain. Neuroscience 90:815–821

    Article  CAS  PubMed  Google Scholar 

  63. Zhang J, Zhang D, McQuade JS et al (2002) c-fos regulates neuronal excitability and survival. Nat Genet 30:416–420

    Article  CAS  PubMed  Google Scholar 

  64. Robertson HA (1992) Immediate-early genes, neuronal plasticity, and memory. Biochem Cell Biol 70:729–737

    Article  CAS  PubMed  Google Scholar 

  65. Ito T, Tatsumi K, Takimoto Y et al (2019) Vestibular compensation after vestibular dysfunction induced by arsanilic acid in mice. Brain Sci 9:329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Fukuda J, Matsuda K, Sato G et al (2021) Effects of betahistine on the development of vestibular compensation after unilateral labyrinthectomy in rats. Brain Sci 11:360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. von Bartheld CS, Fritzsch B (2006) Comparative analysis of neurotrophin receptors and ligands in vertebrate neurons: tools for evolutionary stability or changes in neural circuits? Brain Behav Evol 68:157–172

    Article  Google Scholar 

  68. Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4:299–309

    Article  CAS  PubMed  Google Scholar 

  69. Guo W, Nagappan G, Lu B (2018) Differential effects of transient and sustained activation of BDNF-TrkB signaling. Dev Neurobiol 78:647–659

    Article  CAS  PubMed  Google Scholar 

  70. Johnstone A, Mobley W (2020) Local TrkB signaling: themes in development and neural plasticity. Cell Tissue Res 382:101–111

    Article  PubMed  Google Scholar 

  71. Benítez-Temiño B, Morcuende S, Mentis GZ et al (2004) Expression of Trk receptors in the oculomotor system of the adult cat. J Comp Neurol 473:538–552

    Article  PubMed  Google Scholar 

  72. Zhang FX, Lai CH, Lai SK et al (2003) Neurotrophin receptor immunostaining in the vestibular nuclei of rats. Neuroreport 14:851–855

    Article  CAS  PubMed  Google Scholar 

  73. Zhou L, Zhou W, Zhang S et al (2015) BDNF signaling in the rat cerebello-vestibular pathway during vestibular compensation: BDNF signaling in vestibular compensation. FEBS J 282:3579–3591

    Article  CAS  PubMed  Google Scholar 

  74. Ernfors P, Van De Water T, Loring J, Jaenisch R et al (1995) Complementary roles of BDNF and NT-3 in vestibular and auditory development. Neuron 14:1153–1164. https://doi.org/10.1016/0896-6273(95)90263-5

    Article  CAS  PubMed  Google Scholar 

  75. Johnston AR, Him A, Dutia MB (2001) Differential regulation of GABA(A) and GABA(B) receptors during vestibular compensation. Neuroreport 12:597–600

    Article  CAS  PubMed  Google Scholar 

  76. Bergquist F, Ludwig M, Dutia MB (2008) Role of the commissural inhibitory system in vestibular compensation in the rat. J Physiol 586:4441–4452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Cm G, Cl D, Pf S (2005) Effects of chronic infusion of a GABAA receptor agonist or antagonist into the vestibular nuclear complex on vestibular compensation in the guinea pig. J Pharmacol Exp Ther 313:1126–1135. https://doi.org/10.1124/jpet.104.082172

    Article  CAS  Google Scholar 

  78. de Waele C, Mühlethaler M, Vidal PP (1995) Neurochemistry of the central vestibular pathways. Brain Res Brain Res Rev 20:24–46

    Article  PubMed  Google Scholar 

  79. Torte-Hoba MP, Courjon JH, Leroy MH et al (1996) Acetylcholinesterase activity changes in medial vestibular complex after hemilabyrinthectomy in the rat. J Vestib Res 6:61–70

    Article  CAS  PubMed  Google Scholar 

  80. Monzani D, Genovese E, Marrara A et al (2010) Stimulation of the cholinergic neurotransmissions enhances the efficacy of vestibular rehabilitation. Acta Otorhinolaryngol Ital 30:11–19

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Herman JP, Figueiredo H, Mueller NK et al (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151–180

    Article  CAS  PubMed  Google Scholar 

  82. Cm G, Cl D, Pf S (2003) Activation of the hypothalamic-pituitary-adrenal axis following vestibular deafferentation in pigmented guinea pig. Brain Res 964:306–310. https://doi.org/10.1016/s0006-8993(02)04086-6

    Article  Google Scholar 

  83. Tighilet B, Manrique C, Lacour M (2009) Stress axis plasticity during vestibular compensation in the adult cat. Neuroscience 160:716–730

    Article  CAS  PubMed  Google Scholar 

  84. Johnston AR, Seckl JR, Dutia MB (2002) Role of the flocculus in mediating vestibular nucleus neuron plasticity during vestibular compensation in the rat. J Physiol 545:903–911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Zhang X-Y, Yu L, Zhuang Q-X et al (2013) Postsynaptic mechanisms underlying the excitatory action of histamine on medial vestibular nucleus neurons in rats. Br J Pharmacol 170:156–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. B T, S T, M L. (2005) Dose- and duration-dependent effects of betahistine dihydrochloride treatment on histamine turnover in the cat. Eur J Pharmacol:523. https://doi.org/10.1016/j.ejphar.2005.09.017

  87. Zhuang Q-X, Wu Y-H, Wu G-Y et al (2013) Histamine excites rat superior vestibular nuclear neurons via postsynaptic H1 and H2 receptors in vitro. Neurosignals. 21:174–183

    Article  CAS  PubMed  Google Scholar 

  88. Horii A, Takeda N, Matsunaga T et al (1993) Effect of unilateral vestibular stimulation on histamine release from the hypothalamus of rats in vivo. J Neurophysiol 70:1822–1826

    Article  CAS  PubMed  Google Scholar 

  89. Yabe T, de Waele C, Serafin M et al (1993) Medial vestibular nucleus in the guinea-pig: histaminergic receptors. II. An in vivo study. Exp Brain Res 93:249–258

    Article  CAS  PubMed  Google Scholar 

  90. Li B, Zhang X-Y, Yang A-H et al (2016) Histamine increases neuronal excitability and sensitivity of the lateral vestibular nucleus and promotes motor behaviors via HCN channel coupled to H2 receptor. Front Cell Neurosci 10:300

    PubMed  Google Scholar 

  91. Kokaia M (2011) Seizure-induced neurogenesis in the adult brain. Eur J Neurosci 33:1133–1138

    Article  PubMed  Google Scholar 

  92. Coull JAM, Beggs S, Boudreau D et al (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438:1017–1021

    Article  CAS  PubMed  Google Scholar 

  93. Li X, Tayoun AA, Song Z et al (2018) Ca2+-activated K+ channels reduce network excitability, improving adaptability and energetics for transmitting and perceiving sensory information. J Neurosci 39:7132–7154

    Article  Google Scholar 

  94. Tighilet B, Bourdet A, Péricat D et al (2021) SK channels modulation accelerates equilibrium recovery in unilateral vestibular neurectomized rats. Pharmaceuticals (Basel) 14:1226

    Article  CAS  PubMed  Google Scholar 

  95. Gonzalez-Perez O, Quiñones-Hinojosa A (2012) Astrocytes as neural stem cells in the adult brain. J Stem Cells 7:181–188

    PubMed  PubMed Central  Google Scholar 

  96. Chung W-S, Clarke LE, Wang GX et al (2013) Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature. 504:394–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Chung W-S, Allen NJ, Eroglu C (2015) Astrocytes control synapse formation, function, and elimination. Cold Spring Harb Perspect Biol 7:a020370

    Article  PubMed  PubMed Central  Google Scholar 

  98. Lacour M, Dutheil S, Tighilet B et al (2009) Tell me your vestibular deficit, and I’ll tell you how you’ll compensate. Ann N Y Acad Sci 1164:268–278

    Article  PubMed  Google Scholar 

  99. Sochocka M, Diniz BS, Leszek J (2017) Inflammatory response in the CNS: friend or foe? Mol Neurobiol 54:8071–8089

    Article  CAS  PubMed  Google Scholar 

  100. Russo MV, McGavern DB (2016) Inflammatory neuroprotection following traumatic brain injury. Science. 353:783–785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Jurga AM, Paleczna M, Kuter KZ (2020) Overview of general and discriminating markers of differential microglia phenotypes. Front Cell Neurosci 14:198

    Article  PubMed  PubMed Central  Google Scholar 

  102. Tanaka T, Murakami K, Bando Y et al (2017) Microglia support ATF3-positive neurons following hypoglossal nerve axotomy. Neurochem Int 108:332–342

    Article  CAS  PubMed  Google Scholar 

  103. Clark AK, Gruber-Schoffnegger D, Drdla-Schutting R et al (2015) Selective activation of microglia facilitates synaptic strength. J Neurosci 35:4552–4570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Sienko KH, Whitney SL, Carender WJ et al (2017) The role of sensory augmentation for people with vestibular deficits: real-time balance aid and/or rehabilitation device? J Vestib Res 27:63–76

    Article  CAS  PubMed  Google Scholar 

  105. Chaisuksunt V, Zhang Y, Anderson PN et al (2000) Axonal regeneration from CNS neurons in the cerebellum and brainstem of adult rats: correlation with the patterns of expression and distribution of messenger RNAs for L1, CHL1, c-jun and growth-associated protein-43. Neuroscience 100:87–108

    Article  CAS  PubMed  Google Scholar 

  106. Dyhrfjeld-Johnsen J, Gaboyard-Niay S, Broussy A et al (2013) Ondansetron reduces lasting vestibular deficits in a model of severe peripheral excitotoxic injury. J Vestib Res 23:177–186

    Article  PubMed  Google Scholar 

  107. Gaboyard-Niay S, Travo C, Saleur A et al (2016) Correlation between afferent rearrangements and behavioral deficits after local excitotoxic insult in the mammalian vestibule: a rat model of vertigo symptoms. Dis Model Mech 9:1181–1192

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Genovese T, Impellizzeri D, Ahmad A et al (2013) Post-ischaemic thyroid hormone treatment in a rat model of acute stroke. Brain Res 1513:92–102

    Article  CAS  PubMed  Google Scholar 

  109. Shulga A, Blaesse A, Kysenius K et al (2009) Thyroxin regulates BDNF expression to promote survival of injured neurons. Mol Cell Neurosci 42:408–418

    Article  CAS  PubMed  Google Scholar 

  110. Liu Y-Y, Brent GA (2021) The role of thyroid hormone in neuronal protection. Compr Physiol 11:2075–2095

    Article  PubMed  Google Scholar 

  111. Talhada D, Santos CRA, Gonçalves I et al (2019) Thyroid hormones in the brain and their impact in recovery mechanisms after stroke. Front Neurol 10:1103

    Article  PubMed  PubMed Central  Google Scholar 

  112. Rastoldo G, Marouane E, El-Mahmoudi N et al (2022) L-thyroxine improves vestibular compensation in a rat model of acute peripheral vestibulopathy: cellular and behavioral aspects. Cells 11:684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Bringuier CM, Hatat B, Boularand R et al (2022) Characterization of thyroid hormones antivertigo effects in a rat model of excitotoxically-induced vestibulopathy. Front Neurol 13:877319

    Article  PubMed  PubMed Central  Google Scholar 

  114. Wong-Riley MT (1989) Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12:94–101

    Article  CAS  PubMed  Google Scholar 

  115. Tighilet B, Leonard J, Bernard-Demanze L et al (2015) Comparative analysis of pharmacological treatments with N-acetyl-DL-leucine (Tanganil) and its two isomers (N-acetyl-L-leucine and N-acetyl-D-leucine) on vestibular compensation: behavioral investigation in the cat. Eur J Pharmacol 769:342–349

    Article  CAS  PubMed  Google Scholar 

  116. Günther L, Beck R, Xiong G et al (2015) N-acetyl-L-leucine accelerates vestibular compensation after unilateral labyrinthectomy by action in the cerebellum and thalamus. PLoS One 10:e0120891

    Article  PubMed  PubMed Central  Google Scholar 

  117. Vibert N, Vidal PP (2001) In vitro effects of acetyl-DL-leucine (tanganil) on central vestibular neurons and vestibulo-ocular networks of the guinea-pig. Eur J Neurosci 13:735–748

    Article  CAS  PubMed  Google Scholar 

  118. Marouane E, El Mahmoudi N, Rastoldo G et al (2021) Sensorimotor rehabilitation promotes vestibular compensation in a rodent model of acute peripheral vestibulopathy by promoting microgliogenesis in the deafferented vestibular nuclei. Cells 10:3377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Santos-Pata D, Bellmunt A, Mozo RMSS et al (2022) Impaired reaching adaptation links to vestibular symptoms. medRxiv. https://doi.org/10.1101/2022.02.07.22270496

  120. Beraneck M, Mckee JL, Aleisa M et al (2008) Asymmetric recovery in cerebellar-deficient mice following unilateral labyrinthectomy. J Neurophysiol 100(2):945–958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Menzies JRW, Porrill J, Dutia M et al (2010) Synaptic plasticity in medial vestibular nucleus neurons: comparison with computational requirements of VOR adaptation. PLoS One 5:e13182

    Article  PubMed  PubMed Central  Google Scholar 

  122. McCabe BF, Ryu JH (1969) Experiments on vestibular compensation. Laryngoscope 79:1728–1736

    Article  CAS  PubMed  Google Scholar 

  123. Smith PF (2020) Why the cerebellar shutdown/clampdown hypothesis of vestibular compensation is inconsistent with neurophysiological evidence. J Vestib Res 30:295–303

    Article  PubMed  Google Scholar 

  124. Liu D, Wang J, Zhou L et al (2023) Differential modulation of cerebellar flocculus unipolar brush cells during vestibular compensation. Biomedicines 11:1298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Liu D, Wang J, Tian E et al (2024) mGluR1/IP3/ERK signaling pathway regulates vestibular compensation in ON UBCs of the cerebellar flocculus. CNS Neurosci Ther 30:e14419

    Article  CAS  PubMed  Google Scholar 

  126. Lacour M (2006) Restoration of vestibular function: basic aspects and practical advances for rehabilitation. Curr Med Res Opin 22:1651–1659

    Article  PubMed  Google Scholar 

  127. Newlands SD, Dara S, Kaufman GD (2005) Relationship of static and dynamic mechanisms in vestibuloocular reflex compensation. Laryngoscope 115:191–204

    Article  PubMed  Google Scholar 

  128. Rogge A-K, Röder B, Zech A et al (2018) Exercise-induced neuroplasticity: balance training increases cortical thickness in visual and vestibular cortical regions. Neuroimage 179:471–479

    Article  PubMed  Google Scholar 

  129. Facchini J, Rastoldo G, Xerri C et al (2021) Unilateral vestibular neurectomy induces a remodeling of somatosensory cortical maps. Prog Neurobiol 205:102119

    Article  PubMed  Google Scholar 

  130. Raiser TM, Flanagin VL, Duering M et al (2020) The human corticocortical vestibular network. Neuroimage 223:117362

    Article  CAS  PubMed  Google Scholar 

  131. Li F, Feng Y, Liu H et al (2022) Gut microbiome and metabolome changes in mice with acute vestibular deficit. Front Cell Infect Microbiol 12:821780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Erny D, Hrabě de Angelis AL, Jaitin D et al (2015) Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 18:965–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Matcovitch-Natan O, Winter DR, Giladi A et al (2016) Microglia development follows a stepwise program to regulate brain homeostasis. Science 353:aad8670

    Article  PubMed  Google Scholar 

  134. Han RT, Kim RD, Molofsky AV et al (2021) Astrocyte-immune cell interactions in physiology and pathology. Immunity 54:211–224

    Article  CAS  PubMed  Google Scholar 

  135. Kingsley TR, Nekvasil NP, Snyder DL (1991) The influence of dietary restriction, germ-free status, and aging on adrenal catecholamines in Lobund-Wistar rats. J Gerontol 46:B135–B141

    Article  CAS  PubMed  Google Scholar 

  136. Smith DK, Kassam T, Singh B et al (1992) Escherichia coli has two homologous glutamate decarboxylase genes that map to distinct loci. J Bacteriol 174:5820–5826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. O’Mahony SM, Clarke G, Borre YE et al (2015) Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res 277:32–48

    Article  PubMed  Google Scholar 

  138. Hata T, Asano Y, Yoshihara K et al (2017) Regulation of gut luminal serotonin by commensal microbiota in mice. PLoS One 12:e0180745

    Article  PubMed  PubMed Central  Google Scholar 

  139. Strandwitz P, Kim KH, Terekhova D et al (2019) GABA-modulating bacteria of the human gut microbiota. Nat Microbiol 4:396–403

    Article  CAS  PubMed  Google Scholar 

  140. Chen H-L, Tan C-T, Wu C-C et al (2022) Effects of diet and lifestyle on audio-vestibular dysfunction in the elderly: a literature review. Nutrients 14:4720

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This study was supported by grants from National Natural Science Foundation of China (82271410), Guangzhou Science and Technology Program key projects (202206010097)

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Authors and Affiliations

  1. Department of Neurology, The First Affiliated Hospital, Sun Yat-sen University, Guangdong Provincial Key Laboratory of Diagnosis and Treatment of Major Neurological Diseases, National Key Clinical Department and Key Discipline of Neurology, No.58 Zhongshan Road 2, Guangzhou, 510080, China

    Junyu Wu, Xue Xu, Shifeng Zhang, Minping Li, Yuemin Qiu, Gengxin Lu, Zhihui Zheng & Haiwei Huang

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  1. Junyu Wu
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  2. Xue Xu
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  3. Shifeng Zhang
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  4. Minping Li
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  6. Gengxin Lu
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  7. Zhihui Zheng
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  8. Haiwei Huang
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Junyu Wu, Xue Xu, Shifeng Zhang, Minping Li, Yuemin Qiu, Gengxin Lu, and Zhihui Zheng. The first draft of the manuscript was written by Junyu Wu, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Haiwei Huang.

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Wu, J., Xu, X., Zhang, S. et al. Plastic Events of the Vestibular Nucleus: the Initiation of Central Vestibular Compensation. Mol Neurobiol (2024). https://doi.org/10.1007/s12035-024-04208-2

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