Top

Published in:

Open Access 01-12-2021 | Vestibulopathy | Research

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

Authors: Nada El Mahmoudi, Guillaume Rastoldo, Emna Marouane, David Péricat, Isabelle Watabe, Alain Tonetto, Charlotte Hautefort, Christian Chabbert, Francesca Sargolini, Brahim Tighilet

Published in: Journal of Neuroinflammation | Issue 1/2021

Abstract

Background

Due to their anti-inflammatory action, corticosteroids are the reference treatment for brain injuries and many inflammatory diseases. However, the benefits of acute corticotherapy are now being questioned, particularly in the case of acute peripheral vestibulopathies (APV), characterized by a vestibular syndrome composed of sustained spinning vertigo, spontaneous ocular nystagmus and oscillopsia, perceptual-cognitive, posturo-locomotor, and vegetative disorders. We assessed the effectiveness of acute corticotherapy, and the functional role of acute inflammation observed after sudden unilateral vestibular loss.

Methods

We used the rodent model of unilateral vestibular neurectomy, mimicking the syndrome observed in patients with APV. We treated the animals during the acute phase of the vestibular syndrome, either with placebo or methylprednisolone, an anti-inflammatory corticosteroid. At the cellular level, impacts of methylprednisolone on endogenous plasticity mechanisms were assessed through analysis of cell proliferation and survival, glial reactions, neuron’s membrane excitability, and stress marker. At the behavioral level, vestibular and posturo-locomotor functions’ recovery were assessed with appropriate qualitative and quantitative evaluations.

Results

We observed that acute treatment with methylprednisolone significantly decreases glial reactions, cell proliferation and survival. In addition, stress and excitability markers were significantly impacted by the treatment. Besides, vestibular syndrome’s intensity was enhanced, and vestibular compensation delayed under acute methylprednisolone treatment.

Conclusions

We show here, for the first time, that acute anti-inflammatory treatment alters the expression of the adaptive plasticity mechanisms in the deafferented vestibular nuclei and generates enhanced and prolonged vestibular and postural deficits. These results strongly suggest a beneficial role for acute endogenous neuroinflammation in vestibular compensation. They open the way to a change in dogma for the treatment and therapeutic management of vestibular patients.

Allum JH, Shepard NT. An overview of the clinical use of dynamic posturography in the differential diagnosis of balance disorders. J Vestib Res. 1999;9:223–52.PubMed

Anacker C, Cattaneo A, Luoni A, Musaelyan K, Zunszain PA, Milanesi E, Rybka J, Berry A, Cirulli F, Thuret S, Price J, Riva MA, Gennarelli M, Pariante CM. Glucocorticoid-related molecular signaling pathways regulating hippocampal neurogenesis. Neuropsychopharmacol. 2013;38:872–83. https://doi.org/10.1038/npp.2012.253.CrossRef

Ariyasu L, Byl FM, Sprague MS, Adour KK. The beneficial effect of methylprednisolone in acute vestibular vertigo. Arch Otolaryngol Head Neck Surg. 1990;116:700–3. https://doi.org/10.1001/archotol.1990.01870060058010.CrossRefPubMed

Bath KG, Akins MR, Lee FS. BDNF control of adult SVZ neurogenesis. Dev Psychobiol. 2012;54:578–89. https://doi.org/10.1002/dev.20546.CrossRefPubMed

Bellot-Saez A, Kékesi O, Morley JW, Buskila Y. Astrocytic modulation of neuronal excitability through K+ spatial buffering. Neurosci Biobehav Rev. 2017;77:87–97. https://doi.org/10.1016/j.neubiorev.2017.03.002.CrossRefPubMed

Beraneck M, Hachemaoui M, Idoux E, Ris L, Uno A, Godaux E, Vidal P-P, Moore LE, Vibert N. Long-term plasticity of ipsilesional medial vestibular nucleus neurons after unilateral labyrinthectomy. J Neurophysiol. 2003;90:184–203. https://doi.org/10.1152/jn.01140.2002.CrossRefPubMed

Bos R, Sadlaoud K, Boulenguez P, Buttigieg D, Liabeuf S, Brocard C, Haase G, Bras H, Vinay L. Activation of 5-HT2A receptors upregulates the function of the neuronal K-Cl cotransporter KCC2. Proc Natl Acad Sci. 2013;110:348–53. https://doi.org/10.1073/pnas.1213680110.CrossRefPubMed

Bracken MB, Collins WF, Freeman DF, Shepard MJ, Wagner FW, Silten RM, Hellenbrand KG, Ransohoff J, Hunt WE, Perot PL, Grossman RG, Green BA, Eisenberg HM, Rifkinson N, Goodman JH, Meagher JN, Fischer B, Clifton GL, Flamm ES, Rawe SE. Efficacy of methylprednisolone in acute spinal cord injury. JAMA. 1984;251:45–52. https://doi.org/10.1001/jama.1984.03340250025015.CrossRefPubMed

Bronstein AM, Dieterich M. Long-term clinical outcome in vestibular neuritis: current opinion in neurology. 2019;32:174–80. https://doi.org/10.1097/WCO.0000000000000652.CrossRefPubMed

10.

Cameron SA, Dutia MB. Lesion-induced plasticity in rat vestibular nucleus neurones dependent on glucocorticoid receptor activation. J Physiol. 1999;518:151–8. https://doi.org/10.1111/j.1469-7793.1999.0151r.x.CrossRefPubMedPubMedCentral

11.

Campos Torres A, Vidal PP, de Waele C. Evidence for a microglial reaction within the vestibular and cochlear nuclei following inner ear lesion in the rat. Neuroscience. 1999;92:1475–90. https://doi.org/10.1016/S0306-4522(99)00078-0.CrossRefPubMed

12.

Campos-Torres A, Touret M, Vidal PP, Barnum S, de Waele C. 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. 2005;130:853–65. https://doi.org/10.1016/j.neuroscience.2004.08.052.CrossRefPubMed

13.

Cassel, R., Bordiga, P., Carcaud, J., Simon, F., Beraneck, M., Gall, A.L., Benoit, A., Bouet, V., Philoxene, B., Besnard, S., Watabe, I., Pericat, D., Hautefort, C., Assie, A., Tonetto, A., Dyhrfjeld-Johnsen, J., Llorens, J., Tighilet, B., Chabbert, C., 2019. Morphological and functional correlates of vestibular synaptic deafferentation and repair in a mouse model of acute-onset vertigo. Disease Models & Mechanisms 12. https://doi.org/10.1242/dmm.039115

14.

Cassel R, Bordiga P, Pericat D, Hautefort C, Tighilet B, Chabbert C. New mouse model for inducing and evaluating unilateral vestibular deafferentation syndrome. J Neurosci Methods. 2018;293:128–35. https://doi.org/10.1016/j.jneumeth.2017.09.002.CrossRefPubMed

15.

Cherry JD, Olschowka JA, O’Banion M. Neuroinflammation and M2 microglia: the good, the bad, and the inflamed. J Neuroinflammation. 2014;11:98. https://doi.org/10.1186/1742-2094-11-98.CrossRefPubMedPubMedCentral

16.

Coull JAM, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature. 2005;438:1017–21. https://doi.org/10.1038/nature04223.CrossRefPubMed

17.

Coull JAM, Boudreau D, Bachand K, Prescott SA, Nault F, Sík A, Koninck PD, Koninck YD. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature. 2003;424:938–42. https://doi.org/10.1038/nature01868.CrossRefPubMed

18.

Dai S, Qi Y, Fu J, Li N, Zhang X, Zhang J, Zhang W, Xu H, Zhou H, Ma Z. Dexmedetomidine attenuates persistent postsurgical pain by upregulating K⁺–Cl^− cotransporter-2 in the spinal dorsal horn in rats. JPR. 2018;11:993–1004. https://doi.org/10.2147/JPR.S158737.CrossRef

19.

Darlington CL, Smith PF. Molecular mechanisms of recovery from vestibular damage in mammals: recent advances. Prog Neurobiol. 2000;62:313–25. https://doi.org/10.1016/S0301-0082(00)00002-2.CrossRefPubMed

20.

Deliagina TG, Orlovsky GN, Zelenin PV, Beloozerova IN. Neural bases of postural control. Physiology. 2006;21:216–25. https://doi.org/10.1152/physiol.00001.2006.CrossRefPubMed

21.

Deliagina TG, Popova LB, Grant G. The role of tonic vestibular input for postural control in rats. Arch Ital Biol. 1997;135:239–61.PubMed

22.

Dutheil S, Brezun JM, Leonard J, Lacour M, Tighilet B. Neurogenesis and astrogenesis contribution to recovery of vestibular functions in the adult cat following unilateral vestibular neurectomy: cellular and behavioral evidence. Neuroscience. 2009;164:1444–56. https://doi.org/10.1016/j.neuroscience.2009.09.048.CrossRefPubMed

23.

Dutheil S, Escoffier G, Gharbi A, Watabe I, Tighilet B. GABA _A receptor agonist and antagonist alter vestibular compensation and different steps of reactive neurogenesis in deafferented vestibular nuclei of adult cats. J Neurosci. 2013;33:15555–66. https://doi.org/10.1523/JNEUROSCI.5691-12.2013.CrossRefPubMedPubMedCentral

24.

Dutheil S, Lacour M, Tighilet B. 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. 2011;6: e22262. https://doi.org/10.1371/journal.pone.0022262.CrossRefPubMedPubMedCentral

25.

Dutheil S, Watabe I, Sadlaoud K, Tonetto A, Tighilet B. BDNF signaling promotes vestibular compensation by increasing neurogenesis and remodeling the expression of potassium-chloride cotransporter KCC2 and GABA _A receptor in the vestibular nuclei. J Neurosci. 2016;36:6199–212. https://doi.org/10.1523/JNEUROSCI.0945-16.2016.CrossRefPubMedPubMedCentral

26.

Dutia MB. Mechanisms of vestibular compensation: recent advances: current opinion in otolaryngology & head and neck surgery. 2010;18:420–4. https://doi.org/10.1097/MOO.0b013e32833de71f.CrossRef

27.

Ekdahl CT, Kokaia Z, Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience, Brain - Immune Interactions in Acute and Chronic Brain Disorders. 2009;158:1021–9. https://doi.org/10.1016/j.neuroscience.2008.06.052.CrossRef

28.

Eliezer M, Maquet C, Horion J, Gillibert A, Toupet M, Bolognini B, Magne N, Kahn L, Hautefort C, Attyé A. Detection of intralabyrinthine abnormalities using post-contrast delayed 3D-FLAIR MRI sequences in patients with acute vestibular syndrome. Eur Radiol. 2019;29:2760–9. https://doi.org/10.1007/s00330-018-5825-0.CrossRefPubMed

29.

Fabre-Adinolfi D, Parietti-Winkler C, Pierret J, Lassalle-Kinic B, Frère J. You are better off running than walking revisited: Does an acute vestibular imbalance affect muscle synergies? Hum Mov Sci. 2018;62:150–60. https://doi.org/10.1016/j.humov.2018.10.010.CrossRefPubMed

30.

Fehlings MG, Wilson JR, Cho N. Methylprednisolone for the Treatment of Acute Spinal Cord Injury: Counterpoint. Neurosurgery. 2014;61:36–42. https://doi.org/10.1227/NEU.0000000000000412.CrossRefPubMed

31.

Ferrini F, De Koninck Y. Microglia control neuronal network excitability via BDNF signalling. Neural Plast. 2013;2013:1–11. https://doi.org/10.1155/2013/429815.CrossRef

32.

Fishman JM, Burgess C, Waddell A. Corticosteroids for the treatment of idiopathic acute vestibular dysfunction (vestibular neuritis). Cochrane Database Syst Rev. 2011. https://doi.org/10.1002/14651858.CD008607.pub2.CrossRefPubMed

33.

Flook M, Frejo L, Gallego-Martinez A, Martin-Sanz E, Rossi-Izquierdo M, Amor-Dorado JC, Soto-Varela A, Santos-Perez S, Batuecas-Caletrio A, Espinosa-Sanchez JM, Pérez-Carpena P, Martinez-Martinez M, Aran I, Lopez-Escamez JA. Differential proinflammatory signature in vestibular migraine and Meniere disease. Front Immunol. 2019;10:1229. https://doi.org/10.3389/fimmu.2019.01229.CrossRefPubMedPubMedCentral

34.

Gliddon CM, Darlington CL, Smith PF. Activation of the hypothalamic–pituitary–adrenal axis following vestibular deafferentation in pigmented guinea pig. Brain Res. 2003;964:306–10. https://doi.org/10.1016/S0006-8993(02)04086-6.CrossRefPubMed

35.

Golia, M.T., Poggini, S., Alboni, S., Garofalo, S., Ciano Albanese, N., Viglione, A., Ajmone-Cat, M.A., St-Pierre, A., Brunello, N., Limatola, C., Branchi, I., Maggi, L., 2019. Interplay between inflammation and neural plasticity: both immune activation and suppression impair LTP and BDNF expression. Brain, Behavior, and Immunity S0889159118312388. https://doi.org/10.1016/j.bbi.2019.07.003

36.

Goudakos JK, Markou KD, Franco-Vidal V, Vital V, Tsaligopoulos M, Darrouzet V. Corticosteroids in the treatment of vestibular neuritis: a systematic review and meta-analysis. 2010;31:7.

37.

Goudakos JK, Markou KD, Psillas G, Vital V, Tsaligopoulos M. Corticosteroids and vestibular exercises in vestibular neuritis: single-blind randomized clinical trial. JAMA Otolaryngol Head Neck Surg. 2014;140:434. https://doi.org/10.1001/jamaoto.2014.48.CrossRefPubMed

38.

Goulton, C.S., Watanabe, M., Cheung, D.L., Wang, K.W., Oba, T., Khoshaba, A., Lai, D., Inada, H., Eto, K., Nakamura, K., Power, J.M., Lewis, T.M., Housley, G.D., Wake, H., Nabekura, J., Moorhouse, A.J., 2018. Conditional Upregulation of KCC2 selectively enhances neuronal inhibition during seizures. bioRxiv 253831. https://doi.org/10.1101/253831

39.

Grosch M, Lindner M, Bartenstein P, Brandt T, Dieterich M, Ziegler S, Zwergal A. Dynamic whole-brain metabolic connectivity during vestibular compensation in the rat. Neuroimage. 2021;226: 117588. https://doi.org/10.1016/j.neuroimage.2020.117588.CrossRefPubMed

40.

Haghighi SS, Agrawal SK, Surdell D, Plambeck R, Agrawal S, Johnson GC, Walker A. Effects of methylprednisolone and MK-801 on functional recovery after experimental chronic spinal cord injury. Spinal Cord. 2000;38:733–40. https://doi.org/10.1038/sj.sc.3101074.CrossRefPubMed

41.

Halliday J, Rutherford SA, McCabe MG, Evans DG. An update on the diagnosis and treatment of vestibular schwannoma. Expert Rev Neurother. 2018;18:29–39. https://doi.org/10.1080/14737175.2018.1399795.CrossRefPubMed

42.

Hegemann SCA, Wenzel A. Diagnosis and treatment of vestibular neuritis/neuronitis or peripheral vestibulopathy (PVP)? Open Questions and Possible Answers: Otology & Neurotology. 2017;38:626–31. https://doi.org/10.1097/MAO.0000000000001396.CrossRef

43.

Hurlbert RJ. Methylprednisolone for acute spinal cord injury: an inappropriate standard of care. J Neurosurg Spine. 2000;93:1–7. https://doi.org/10.3171/spi.2000.93.1.0001.CrossRef

44.

Jamali M, Mitchell DE, Dale A, Carriot J, Sadeghi SG, Cullen KE. Neuronal detection thresholds during vestibular compensation: contributions of response variability and sensory substitution: Neuronal detection thresholds during vestibular compensation. J Physiol. 2014;592:1565–80. https://doi.org/10.1113/jphysiol.2013.267534.CrossRefPubMedPubMedCentral

45.

Jassam YN, Izzy S, Whalen M, McGavern DB, El Khoury J. Neuroimmunology of traumatic brain injury: time for a paradigm shift. Neuron. 2017;95:1246–65. https://doi.org/10.1016/j.neuron.2017.07.010.CrossRefPubMedPubMedCentral

46.

Karve IP, Taylor JM, Crack PJ. The contribution of astrocytes and microglia to traumatic brain injury: Neuroinflammation and TBI. Br J Pharmacol. 2016;173:692–702. https://doi.org/10.1111/bph.13125.CrossRefPubMed

47.

Kassner SS, Schöttler S, Bonaterra GA, Stern-Straeter J, Hormann K, Kinscherf R, Gössler UR. Proinflammatory activation of peripheral blood mononuclear cells in patients with vestibular neuritis. Audiology and Neurotology. 2011;16:242–7. https://doi.org/10.1159/000320839.CrossRefPubMed

48.

Lacour M, Helmchen C, Vidal P-P. Vestibular compensation: the neuro-otologist’s best friend. J Neurol. 2016;263:54–64. https://doi.org/10.1007/s00415-015-7903-4.CrossRefPubMedCentral

49.

Lacour M, Tighilet B. Plastic events in the vestibular nuclei during vestibular compensation: The brain orchestration of a "deafferentation" code. Restor Neurol Neurosci. 2010;28:19–35. https://doi.org/10.3233/RNN-2010-0509.CrossRefPubMed

50.

Lacour M, Xerri C. Compensation of postural reactions to free-fall in the vestibular neurectomized monkey. Exp Brain Res. 1980;40:103–10. https://doi.org/10.1007/BF00236668.CrossRefPubMed

51.

Li H, Godfrey DA, Rubin AM. Comparison of surgeries for removal of primary vestibular inputs: A combined anatomical and behavioral study in rats. Laryngoscope. 1995;105:417–24. https://doi.org/10.1288/00005537-199504000-00015.CrossRefPubMed

52.

Liberge, M., Manrique, C., Bernard-Demanze, L., Lacour, M., 2010. Changes in TNFa, NF B and MnSOD protein in the vestibular nuclei after unilateral vestibular deafferentation 16.

53.

Liddelow SA, Barres BA. Reactive Astrocytes: Production, Function, and Therapeutic Potential. Immunity. 2017;46:957–67. https://doi.org/10.1016/j.immuni.2017.06.006.CrossRefPubMed

54.

Lindner M, Gosewisch A, Eilles E, Branner C, Krämer A, Oos R, Wolf E, Ziegler S, Bartenstein P, Brandt T, Dieterich M, Zwergal A. Ginkgo biloba extract EGb 761 improves vestibular compensation and modulates cerebral vestibular networks in the rat. Front Neurol. 2019;10:147. https://doi.org/10.3389/fneur.2019.00147.CrossRefPubMedPubMedCentral

55.

Liu T, Zhang L, Joo D, Sun S-C. NF-κB signaling in inflammation. Sig Transduct Target Ther. 2017;2:17023. https://doi.org/10.1038/sigtrans.2017.23.CrossRef

56.

Lorenzo L-E, Godin AG, Ferrini F, Bachand K, Plasencia-Fernandez I, Labrecque S, Girard AA, Boudreau D, Kianicka I, Gagnon M, Doyon N, Ribeiro-da-Silva A, De Koninck Y. Enhancing neuronal chloride extrusion rescues α2/α3 GABA A -mediated analgesia in neuropathic pain. Nat Commun. 2020;11:869. https://doi.org/10.1038/s41467-019-14154-6.CrossRefPubMedPubMedCentral

57.

Löscher W. Abnormal circling behavior in rat mutants and its relevance to model specific brain dysfunctions. Neurosci Biobehav Rev. 2010;34:31–49. https://doi.org/10.1016/j.neubiorev.2009.07.001.CrossRefPubMed

58.

Lucas S-M, Rothwell NJ, Gibson RM. The role of inflammation in CNS injury and disease. Br J Pharmacol. 2006;147:S232–40. https://doi.org/10.1038/sj.bjp.0706400.CrossRefPubMedPubMedCentral

59.

Marouane, E., Rastoldo, G., El Mahmoudi, N., Péricat, D., Chabbert, C., Artzner, V., Tighilet, B., 2020. Identification of new biomarkers of posturo-locomotor instability in a rodent model of vestibular pathology. Front Neurol 11. https://doi.org/10.3389/fneur.2020.00470

60.

Mccabe BF, Ryu JH. Experiments on vestibular compensation. Laryngoscope. 1969;79:1728–36. https://doi.org/10.1288/00005537-196910000-00004.CrossRefPubMed

61.

McCall, A.A., Miller, D.M., Yates, B.J., 2017. Descending influences on vestibulospinal and vestibulosympathetic reflexes. Front. Neurol. 8. https://doi.org/10.3389/fneur.2017.00112

62.

Miyazaki H, Nomura Y, Mardassi A, Deveze A, Miura M, Jike M, Magnan J. How minimally invasive vestibular neurotomy for incapacitating Meniere’s disease improves dizziness and anxiety. Acta Otolaryngol. 2017;137:707–11. https://doi.org/10.1080/00016489.2017.1278790.CrossRefPubMed

63.

Myer DJ. Essential protective roles of reactive astrocytes in traumatic brain injury. Brain. 2006;129:2761–72. https://doi.org/10.1093/brain/awl165.CrossRefPubMed

64.

Nevoux, J., Franco-Vidal, V., Bouccara, D., Parietti-Winkler, C., Uziel, A., Chays, A., Dubernard, X., Couloigner, V., Darrouzet, V., Mom, T., Groupe de Travail de la SFORL. Diagnostic and therapeutic strategy in Menière’s disease. Guidelines of the French Otorhinolaryngology-Head and Neck Surgery Society (SFORL). Eur Ann Otorhinolaryngol Head Neck Dis. 2017;134:441–4. https://doi.org/10.1016/j.anorl.2016.12.003.CrossRef

65.

Numakawa T, Kumamaru E, Adachi N, Yagasaki Y, Izumi A, Kunugi H. Glucocorticoid receptor interaction with TrkB promotes BDNF-triggered PLC- signaling for glutamate release via a glutamate transporter. Proc Natl Acad Sci. 2009;106:647–52. https://doi.org/10.1073/pnas.0800888106.CrossRefPubMedPubMedCentral

66.

Paragliola RM, Papi G, Pontecorvi A, Corsello SM. Treatment with synthetic glucocorticoids and the hypothalamus-pituitary-adrenal axis. IJMS. 2017;18:2201. https://doi.org/10.3390/ijms18102201.CrossRefPubMedCentral

67.

Paxinos G, Watson C. The rat brain in stereotaxic coordinates. Boston: Elsevier, Amsterdam; 2009.

68.

Payne DNR, Adcock IM. Molecular mechanisms of corticosteroid actions. Paediatr Respir Rev. 2001;2:145–50. https://doi.org/10.1053/prrv.2000.0122.CrossRefPubMed

69.

Pereira JE, Costa LM, Cabrita AM, Couto PA, Filipe VM, Magalhães LG, Fornaro M, Di Scipio F, Geuna S, Maurício AC, Varejão ASP. Methylprednisolone fails to improve functional and histological outcome following spinal cord injury in rats. Exp Neurol. 2009;220:71–81. https://doi.org/10.1016/j.expneurol.2009.07.030.CrossRefPubMed

70.

Péricat D, Farina A, Agavnian-Couquiaud E, Chabbert C, Tighilet B. Complete and irreversible unilateral vestibular loss: A novel rat model of vestibular pathology. J Neurosci Methods. 2017;283:83–91. https://doi.org/10.1016/j.jneumeth.2017.04.001.CrossRefPubMed

71.

Precht W, Shimazu H, Markham CH. A mechanism of central compensation of vestibular function following hemilabyrinthectomy. J Neurophysiol. 1966;29:996–1010. https://doi.org/10.1152/jn.1966.29.6.996.CrossRefPubMed

72.

Quax RA, Manenschijn L, Koper JW, Hazes JM, Lamberts SWJ, van Rossum EFC, Feelders RA. Glucocorticoid sensitivity in health and disease. Nat Rev Endocrinol. 2013;9:670–86. https://doi.org/10.1038/nrendo.2013.183.CrossRefPubMed

73.

Quintana, F.J., 2017. Astrocytes to the rescue! Glia limitans astrocytic endfeet control CNS inflammation. Journal of Clinical Investigation 127, 2897–2899.https://doi.org/10.1172/JCI95769

74.

Rastoldo, G., 2021. Adult and endemic neurogenesis in the vestibular nuclei after unilateral vestibular neurectomy. Progress in Neurobiology 11.

75.

Rastoldo G, El Mahmoudi N, Marouane E, Pericat D, Watabe I, Toneto A, López-Juárez A, Chabbert C, Tighilet B. Adult and endemic neurogenesis in the vestibular nuclei after unilateral vestibular neurectomy. Prog Neurobiol. 2021;196: 101899. https://doi.org/10.1016/j.pneurobio.2020.101899.CrossRefPubMed

76.

Rastoldo, G., Marouane, E., El Mahmoudi, N., Péricat, D., Bourdet, A., Timon-David, E., Dumas, O., Chabbert, C., Tighilet, B., 2020. Quantitative evaluation of a new posturo-locomotor phenotype in a rodent model of acute unilateral vestibulopathy. Front. Neurol. 11.https://doi.org/10.3389/fneur.2020.00505

77.

Rhen T, Cidlowski JA. Antiinflammatory action of glucocorticoids — new mechanisms for old drugs. N Engl J Med. 2005;353:1711–23. https://doi.org/10.1056/NEJMra050541.CrossRefPubMed

78.

Rivera C. Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J Neurosci. 2004;24:4683–91. https://doi.org/10.1523/JNEUROSCI.5265-03.2004.CrossRefPubMedPubMedCentral

79.

Rivera C, Li H, Thomas-Crusells J, Lahtinen H, Viitanen T, Nanobashvili A, Kokaia Z, Airaksinen MS, Voipio J, Kaila K, Saarma M. BDNF-induced TrkB activation down-regulates the K+–Cl− cotransporter KCC2 and impairs neuronal Cl− extrusion. J Cell Biol. 2002;159:747–52. https://doi.org/10.1083/jcb.200209011.CrossRefPubMedPubMedCentral

80.

Russo MV, McGavern DB. Inflammatory neuroprotection following traumatic brain injury. Science. 2016;353:783–5. https://doi.org/10.1126/science.aaf6260.CrossRefPubMedPubMedCentral

81.

Russo MV, McGavern DB. Immune Surveillance of the CNS following Infection and Injury. Trends Immunol. 2015;36:637–50. https://doi.org/10.1016/j.it.2015.08.002.CrossRefPubMedPubMedCentral

82.

Sadeghi SG, Minor LB, Cullen KE. Multimodal integration after unilateral labyrinthine lesion: single vestibular nuclei neuron responses and implications for postural compensation. J Neurophysiol. 2011;105:661–73. https://doi.org/10.1152/jn.00788.2010.CrossRefPubMed

83.

Saman, Y., Bamiou, D.E., Gleeson, M., Dutia, M.B., 2012. Interactions between Stress and Vestibular Compensation – A Review. Front. Neur. 3. https://doi.org/10.3389/fneur.2012.00116

84.

Santa-Cecília FV, Socias B, Ouidja MO, Sepulveda-Diaz JE, Acuña L, Silva RL, Michel PP, Del-Bel E, Cunha TM, Raisman-Vozari R. Doxycycline suppresses microglial activation by inhibiting the p38 MAPK and NF-kB signaling pathways. Neurotox Res. 2016;29:447–59. https://doi.org/10.1007/s12640-015-9592-2.CrossRefPubMed

85.

Shupak A, Issa A, Golz A, Kaminer M, Braverman I. Prednisone treatment for vestibular neuritis. Otol Neurotol. 2008;29:368–74. https://doi.org/10.1097/MAO.0b013e3181692804.CrossRefPubMed

86.

Simon F, Pericat D, Djian C, Fricker D, Denoyelle F, Beraneck M. Surgical techniques and functional evaluation for vestibular lesions in the mouse: unilateral labyrinthectomy (UL) and unilateral vestibular neurectomy (UVN). J Neurol. 2020. https://doi.org/10.1007/s00415-020-09960-8.CrossRefPubMedPubMedCentral

87.

Smith PF, Curthoys IS. Mechanisms of recovery following unilateral labyrinthectomy: a review. Brain Res Rev. 1989;14:155–80. https://doi.org/10.1016/0165-0173(89)90013-1.CrossRefPubMed

88.

Sochocka M, Diniz BS, Leszek J. Inflammatory response in the CNS: friend or foe? Mol Neurobiol. 2017;54:8071–89. https://doi.org/10.1007/s12035-016-0297-1.CrossRefPubMed

89.

Solis RN, Sun DQ, Tatro E, Hansen MR. Do steroids improve recovery in vestibular neuritis?: Steroids for Vestibular Neuritis. Laryngoscope. 2019;129:288–90. https://doi.org/10.1002/lary.27278.CrossRefPubMed

90.

Stephenson J, Nutma E, van der Valk P, Amor S. Inflammation in CNS neurodegenerative diseases Immunology. 2018;154:204–19. https://doi.org/10.1111/imm.12922.CrossRefPubMed

91.

Stiles L, Smith PF. The vestibular–basal ganglia connection: Balancing motor control. Brain Res. 2015;1597:180–8. https://doi.org/10.1016/j.brainres.2014.11.063.CrossRefPubMed

92.

Streit WJ, Mrak RE, Griffin WST. No title found. J Neuroinflammation. 2004;1:14. https://doi.org/10.1186/1742-2094-1-14.CrossRefPubMedPubMedCentral

93.

Strupp M, Brandt T. Vestibular Neuritis. Semin Neurol. 2009;29:509–19. https://doi.org/10.1055/s-0029-1241040.CrossRefPubMed

94.

Strupp M, Brandt T. Review: Current treatment of vestibular, ocular motor disorders and nystagmus. Ther Adv Neurol Disord. 2009;2:223–39. https://doi.org/10.1177/1756285609103120.CrossRefPubMedPubMedCentral

95.

Strupp M, Dieterich M, Brandt T. The treatment and natural course of peripheral and central vertigo. Deutsches Aerzteblatt Online. 2013. https://doi.org/10.3238/arztebl.2013.0505.CrossRef

96.

Strupp M, Mandalà M, López-Escámez JA. Peripheral vestibular disorders: an update. Curr Opin Neurol. 2019;32:165–73. https://doi.org/10.1097/WCO.0000000000000649.CrossRefPubMed

97.

Strupp M, Zingler VC, Arbusow V, Niklas D, Maag KP, Dieterich M, Bense S, Theil D, Jahn K, Brandt T. Methylprednisolone, valacyclovir, or the combination for vestibular neuritis. N Engl J Med. 2004;351:354–61. https://doi.org/10.1056/NEJMoa033280.CrossRefPubMed

98.

Takeda K, Sawamura S, Sekiyama H, Tamai H, Hanaoka K. Effect of methylprednisolone on neuropathic pain and spinal glial activation in rats: anesthesiology. 2004;100:1249–57. https://doi.org/10.1097/00000542-200405000-00029.CrossRefPubMed

99.

Tashiro S, Shinozaki M, Mukaino M, Renault-Mihara F, Toyama Y, Liu M, Nakamura M, Okano H. BDNF induced by treadmill training contributes to the suppression of spasticity and allodynia after spinal cord injury via upregulation of KCC2. Neurorehabil Neural Repair. 2015;29:677–89. https://doi.org/10.1177/1545968314562110.CrossRefPubMed

100.

Tighilet B, Bordiga P, Cassel R, Chabbert C. Peripheral vestibular plasticity vs central compensation: evidence and questions. J Neurol. 2019;266:27–32. https://doi.org/10.1007/s00415-019-09388-9.CrossRefPubMed

101.

Tighilet B, Brezun JM, Sylvie DD, G., Gaubert, C., Lacour, M., . New neurons in the vestibular nuclei complex after unilateral vestibular neurectomy in the adult cat: Reactive neurogenesis in adult vestibular lesioned cats. Eur J Neurosci. 2007;25:47–58. https://doi.org/10.1111/j.1460-9568.2006.05267.x.CrossRefPubMed

102.

Tighilet B, Chabbert C. Adult neurogenesis promotes balance recovery after vestibular loss. Prog Neurobiol. 2019;174:28–35. https://doi.org/10.1016/j.pneurobio.2019.01.001.CrossRefPubMed

103.

Tighilet, B., Dutheil, S., Siponen, M.I., Noreña, A.J., 2016. Reactive neurogenesis and down-regulation of the potassium-chloride cotransporter KCC2 in the cochlear nuclei after cochlear deafferentation. Front. Pharmacol. 7. https://doi.org/10.3389/fphar.2016.00281

104.

Tighilet B, Leonard J, Bernard-Demanze L, Lacour M. 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. 2015;769:342–9. https://doi.org/10.1016/j.ejphar.2015.11.041.CrossRefPubMed

105.

Tighilet B, Leonard J, Lacour M. Betahistine dihydrochloride treatment facilitates vestibular compensation in the cat. J Vestib Res. 1995;5:53–66.CrossRef

106.

Tighilet B, Manrique C, Lacour M. Stress axis plasticity during vestibular compensation in the adult cat. Neuroscience. 2009;160:716–30. https://doi.org/10.1016/j.neuroscience.2009.02.070.CrossRefPubMed

107.

Tighilet B, Péricat D, Frelat A, Cazals Y, Rastoldo G, Boyer F, Dumas O, Chabbert C. Adjustment of the dynamic weight distribution as a sensitive parameter for diagnosis of postural alteration in a rodent model of vestibular deficit. PLoS ONE. 2017;12: e0187472. https://doi.org/10.1371/journal.pone.0187472.CrossRefPubMedPubMedCentral

108.

Tighilet B, Trottier S, Mourre C, Lacour M. Changes in the histaminergic system during vestibular compensation in the cat: histamine and vestibular compensation. J Physiol. 2006;573:723–39. https://doi.org/10.1113/jphysiol.2006.107805.CrossRefPubMedPubMedCentral

109.

Uffer DS, Hegemann SCA. About the pathophysiology of acute unilateral vestibular deficit – vestibular neuritis (VN) or peripheral vestibulopathy (PVP)? VES. 2016;26:311–7. https://doi.org/10.3233/VES-160581.CrossRef

110.

Vidal, P.P., Wang, D.H., Graf, W., de Waele, C., 1993. Chapter 22 Vestibular control of skeletal geometry in the guinea pig: a problem of good trim?, in: Progress in Brain Research. Elsevier, pp. 229–243. https://doi.org/10.1016/S0079-6123(08)62282-7

111.

Walker MF. Treatment of vestibular neuritis. Curr Treat Options Neurol. 2009;11:41–5. https://doi.org/10.1007/s11940-009-0006-8.CrossRefPubMed

112.

Widera D, Mikenberg I, Elvers M, Kaltschmidt C, Kaltschmidt B. Tumor necrosis factor α triggers proliferation of adult neural stem cells via IKK/NF-κB signaling. BMC Neurosci. 2006;7:64. https://doi.org/10.1186/1471-2202-7-64.CrossRefPubMedPubMedCentral

113.

Yamamoto T. The Effect of Stress Application on Vestibular Compensation. Acta Otolaryngol. 2000;120:504–7. https://doi.org/10.1080/000164800750046009.CrossRefPubMed

114.

Yin Y, Sun W, Li Z, Zhang B, Cui H, Deng L, Xie P, Xiang J, Zou J. Effects of combining methylprednisolone with rolipram on functional recovery in adult rats following spinal cord injury. Neurochem Int. 2013;62:903–12. https://doi.org/10.1016/j.neuint.2013.03.005.CrossRefPubMed

115.

Yoo MH, Yang CJ, Kim SA, Park MJ, Ahn JH, Chung JW, Park HJ. Efficacy of steroid therapy based on symptomatic and functional improvement in patients with vestibular neuritis: a prospective randomized controlled trial. Eur Arch Otorhinolaryngol. 2017;274:2443–51. https://doi.org/10.1007/s00405-017-4556-1.CrossRefPubMed

116.

Young LR, Bernard-Demanze L, Dumitrescu M, Magnan J, Borel L, Lacour M. Postural performance of vestibular loss patients under increased postural threat. J Vestib Res. 2012;22:129–38. https://doi.org/10.3233/VES-2012-0449.CrossRefPubMed

Title: 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
Authors: Nada El Mahmoudi
Guillaume Rastoldo
Emna Marouane
David Péricat
Isabelle Watabe
Alain Tonetto
Charlotte Hautefort
Christian Chabbert
Francesca Sargolini
Brahim Tighilet
Publication date: 01-12-2021
Publisher: BioMed Central
Keyword: Vestibulopathy
Published in: Journal of Neuroinflammation / Issue 1/2021
Electronic ISSN: 1742-2094
DOI: https://doi.org/10.1186/s12974-021-02222-y

Keynote webinar | Spotlight on medication adherence

Springer Medicine

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

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2021

Microglia RAGE exacerbates the progression of neurodegeneration within the SOD1G93A murine model of amyotrophic lateral sclerosis in a sex-dependent manner

Sex differences and similarities in the neuroimmune response to central administration of poly I:C

Prostaglandin EP2 receptor antagonist ameliorates neuroinflammation in a two-hit mouse model of Alzheimer’s disease

Correction to: Small extracellular vesicles encapsulating CCL2 from activated astrocytes induce microglial activation and neuronal apoptosis after traumatic spinal cord injury

Tonicity-responsive enhancer-binding protein promotes diabetic neuroinflammation and cognitive impairment via upregulation of lipocalin-2

Inflammatory, synaptic, motor, and behavioral alterations induced by gestational sepsis on the offspring at different stages of life