Research Article

Different Types of Environmental Stressors Could Have Disruptive or Constructive Effects on Vestibular Compensation


Background and Aim: Stress could play either helpful or harmful roles in vestibular compensation, the process of recovery after vestibular system lesions. Herein, we examined the effect of two stressor types on vestibular compensation: chronic anxiety disorder induced by early maternal separation (MS), and caloric restriction by an intermittent fasting (IF) diet.
Methods: Male Wistar rats (n=56) received maternal separation (the MS group), intermittent fasting (IF group), unilateral vestibular deafferentation (UVD group), or a mixture of these interventions (UVD+IF, UVD+MS, and UVD+IF+MS). All the groups were compared with control animals. The animals’ balance, motor coordination, anxiety, locomotor activity, and serum cortisol levels were evaluated by rotarod, open field, and enzyme-linked immunosorbent assay methods, respectively. The data were compared with those of the healthy control (HC) group.
Results: The UVD animals did not show a significant change in the time on the rod, except for the IF+UVD group (p=0.04). There was no significant difference between the experimental groups on the open field indices, except for the MS+IF+UVD group which traveled a significantly less total distance (p=0.02). Serum cortisol levels were significantly higher than HCs for all the groups except for the sham saline and IF+UVD group (p<0.05).
Conclusion: IF seems to promote compensation after UVD, while MS may disrupt it. However, IF loses its beneficial outcomes if the animal has received another source of stress, i.e. MS.

[1] Saman Y, Bamiou DE, Gleeson M, Dutia MB. Interactions between stress and vestibular compensation - A review. Front Neurol. 2012;3:116. [DOI:10.3389/fneur.2012.00116]
[2] El Khouray A, Gruber SHM, Mørk A, Mathe AA. Adult life behavioral consequences of early maternal separation are alleviated by escitalopram treatment in a rat model of depression. Prog Neuropsychopharmacol Biol Psychiatry. 2006;30(3):535-40. [DOI:10.1016/j.pnpbp.2005.11.011]
[3] Issa AM, Rowe W, Gauthier S, Meaney MJ. Hypothalamicpituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. J Neurosci. 1990;10(10):3247-54. [DOI:10.1523/JNEUROSCI.10-10-03247.1990]
[4] Martin B, Mattson MP, Maudsley S. Caloric restriction and intermittent fasting-Two potential diets for successful brain aging. Ageing Res Rev. 2006;5(3):322-53. [DOI:10.1016/j.arr.2006.04.002]
[5] Bigelow RT, Semenov YR, du Lac S, Hoffman H, Agrawal Y. Vestibular vertigo and comorbid cognitive and psychiatric impairment: The 2008 National Health Interview Survey. J Neurol Neurosurg Psychiatry. 2016;87(4):367-72. [DOI:10.1136/jnnp-2015-310319]
[6] Staab JP, Ruckenstein MJ, Solomon D, Shepard NT. Serotonin reuptake inhibitors for dizziness with psychiatric symptoms. Arch Otolaryngol Head Neck Surg. 2002;128(5):554-60. [DOI:10.1001/archotol.128.5.554]
[7] Lepicard EM, Venault P, Perez-diaz F, Joubert C, Berthoz A, Chapouthier G. Balance control and posture differences in the anxious BALB/cByJ mice compared to the non-anxious C57BL/6J mice. Behav Brain Res. 2000;117(1-2):185-95. [DOI:10.1016/S0166-4328(00)00304-1]
[8] Zheng Y, Cheung I, Smith PF. Performance in anxiety and spatial memory tests following bilateral vestibular loss in the rat and effects of anxiolytic and anxiogenic drugs. Behav Brain Res. 2012;235(1):21-9. [DOI:10.1016/j.bbr.2012.07.025]
[9] Madala Halagappa VK, Guo Z, Pearson M, Matsuoka Y, Cutler RG, Laferla FM, et al. Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer’s disease. Neurobiol Dis. 2007;26(1):212-20. [DOI:10.1016/j.nbd.2006.12.019]
[10] Anson RM, Guo Z, de Cabo R, Lyun T, Rios M, Hagepanos A, et al. Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc Natl Acad Sci U S A. 2003;100(10):6216-20. [DOI:10.1073/pnas.1035720100]
[11] Levay EA, Govic A, Penman J, Paolini AG, Kent S. Effects of adult-onset calorie restriction on anxiety-like behavior in rats. Physiol Behav. 2007;92(5):889-96. [DOI:10.1016/j.physbeh.2007.06.018]
[12] Kretsch MJ, Green MW, Fong AK, Elliman NA, Johnson HL. Cognitive effects of a long-term weight reducing diet. Int J Obes Relat Metab Disord. 1997;21(1):14-21. [DOI:10.1038/sj.ijo.0800353]
[13] Fond G, Macgregor A, Leboyer M, Michalsen A. Fasting in mood disorders : neurobiology and effectiveness. A review of the literature. Psychiatry Res. 2013;209(3):253-8. [DOI:10.1016/j.psychres.2012.12.018]
[14] Jahng JW, Kim JG, Kim HJ, Kim B-T, Kang D-W, Lee J-H. Chronic food restriction in young rats results in depressionand anxiety-like behaviors with decreased expression of serotonin reuptake transporter. Brain Res. 2007;1150:100-7. [DOI:10.1016/j.brainres.2007.02.080]
[15] Lyford-Pike S, Vogelheim C, Chu E, Della Santina CC, Carey JP. Gentamicin is primarily localized in vestibular type I hair cells after intratympanic administration. J Assoc Res Otolaryngol. 2007;8(4):497-508. [DOI:10.1007/s10162-007-0093-8]
[16] Tian CJ, Kim SW, Kim YJ, Lim HJ, Park R, So H-S. Red ginseng protects against gentamicin-induced balance dysfunction and hearing loss in rats through antiapoptotic functions of ginsenoside. Food Chem Toxicol. 2013;60:369-76. [DOI:10.1016/j.fct.2013.07.069]
[17] Hirvonen TP, Minor LB, Hullar TE, Carey JP. Effects of intratympanic gentamicin on vestibular afferents and hair cells in the chinchilla. J Neurophysiol. 2005;93(2):643-55. [DOI:10.1152/jn.00160.2004]
[18] Struck MB, Andrutis KA, Ramirez HE, Battles AH. Effect of a short-term fast on ketamine-xylazine anesthesia in rats. J Am Assoc Lab Anim Sci. 2011;50(3):344-8.
[19] Tighilet B, Manrique C, Lacour M. Stress axis plasticity during vestibular compensation in the adult cat. Neuroscience. 2009;160(4):716-30. [DOI:10.1016/j.neuroscience.2009.02.070]
[20] Frame LT, Hart RW, Leakey JE. Caloric restriction as a mechanism mediating resistance to environmental disease. Environ Health Perspect. 1998;106 Suppl 1(Suppl 1):313-24. [DOI:10.1289/ehp.98106s1313]
[21] Larsen PJ, Jessop DS, Chowdrey HS, Lightman SL, Mikkelsen JD. Chronic administration of glucocorticoids directly upregulates prepro‐neuropeptide Y and Y1‐Receptor mRNA levels in the arcuate nucleus of the rat. J Neuroendocrinol. 1994;6(2):153-9. [DOI:10.1111/j.1365-2826.1994.tb00566.x]
[22] Selye H. Stress and the general adaptation syndrom. Br Med J. 1950;1(4667):1383-92. [DOI:10.1136/bmj.1.4667.1383]
[23] Gonzalez-Bono E, Rohleder N, Hellhammer DH, Salvador A, Kirschbaum C. Glucose but not protein or fat load amplifies the cortisol response to psychosocial stress. Horm Behav. 2002;41(3):328-33. [DOI:10.1006/hbeh.2002.1766]
[24] Kirschbaum C, Gonzalez-Bono E, Rohleder N, Gessner C, Pirke KM, Salvador A, et al. Effects of fasting and glucose load on free cortisol responses to stress and nicotine. J Clin Endocrinol Metab. 1997;82(4):1101-5. [DOI:10.1210/jcem.82.4.3882]
[25] Schmahl FW, Metzler B. The health risks of occupational stress in Islamic industrial workers during the Ramadan fasting period. Pol J Occup Med Environ Health. 1991;4(3):219-28.
IssueVol 31 No 1 (2022) QRcode
SectionResearch Article(s)
Anxiety fasting vestibular compensation

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
Sardari S, Asadi-Shekaari M, Khaksari M, Aghaei I, Delavari F, Vaziri Z. Different Types of Environmental Stressors Could Have Disruptive or Constructive Effects on Vestibular Compensation. Aud Vestib Res. 2021;31(1):45-52.