Combination of Vestibular Rehabilitation and Galvanic Vestibular Stimulation Improves Verbal and Visuospatial Memory: A Randomized Control Trial in Patients with Amnestic Mild Cognitive Impairment
-
Behnoush Kamali
,
Mansoureh Adel Ghahraman
,
Reza Hoseinabadi
,
Vajiheh Aghamollaii
,
Shohreh Jalaie
Abstract
Background and Aim: Considering the critical input of the vestibular system to the hippocampus as an area involved in cognition, and vestibular disorders reported in patients with amnestic Mild Cognitive Impairment (aMCI), we aimed to investigate the effects of Vestibular Rehabilitation (VR) with and without noisy Galvanic Vestibular Stimulation (nGVS) on cognitive function in patients with aMCI.
Methods: In a randomized controlled trial, twenty-two patients with aMCI were randomly assigned to two groups receiving: 1) VR for four weeks (VR group); 2) VR for four weeks with nGVS for three sessions (GVS+VR group). Outcome measures were Rey's Auditory-Verbal Learning Test (RAVLT), Corsi blocks, Visual Search (VS), and match to sample tests.
Results: Mean immediate and delayed recalls of RAVLT, all of the outcomes of Corsi blocks and VS tests, and the error rate of the match to sample tests improved significantly after intervention in VR and GVS+VR groups. Between-group differences were observed for learning and delayed recalls of RAVLT (p=0.001, d=0.444 and p<0.001, d=0.512 respectively), reaction times 1 and 2 in VS (p=0.007, d=0.325 and p=0.001, d=0.446 respectively), the total correct trial of Corsi blocks (p=0.026, d=0.235), and error rate of the match to sample (p=0.017, d=0.266) tests.
Conclusion: The synergistic effect of VR and GVS suggested that simultaneous use of both stimulations improves verbal and visuospatial memory in aMCI patients. Study protocol location: https://irct.ir/trial/47249 Trial registration number: IRCT20160131026279N3
[1] DeCarli C. Mild cognitive impairment: prevalence, prognosis, aetiology, and treatment. Lancet Neurol. 2003;2(1):15-21. [DOI:10.1016/S1474-4422(03)00262-X]
[2] Busse A, Hensel A, Gühne U, Angermeyer MC, Riedel-Heller SG. Mild cognitive impairment: long-term course of four clinical subtypes. Neurology. 2006;67(12):2176-85. [DOI:10.1212/01.wnl.0000249117.23318.e1]
[3] Nelson AP, O’Connor MG. Mild cognitive impairment: a neuropsychological perspective. CNS Spectr. 2008;13(1):56-64. [DOI:10.1017/S1092852900016163]
[4] Petersen RC. Mild Cognitive Impairment. Continuum (Minneap Minn). 2016;22(2 Dementia):404-18. [DOI:10.1212/CON.0000000000000313]
[5] Carter SF, Caine D, Burns A, Herholz K, Lambon Ralph MA. Staging of the cognitive decline in Alzheimer’s disease: insights from a detailed neuropsychological investigation of mild cognitive impairment and mild Alzheimer’s disease. Int J Geriatr Psychiatry. 2012;27(4):423-32. [DOI:10.1002/gps.2738]
[6] Hitier M, Besnard S, Smith PF. Vestibular pathways involved in cognition. Front Integr Neurosci. 2014;8:59. [DOI:10.3389/fnint.2014.00059]
[7] Burgess N, Maguire EA, O’Keefe J. The human hippocampus and spatial and episodic memory. Neuron. 2002;35(4):625-41. [DOI:10.1016/S0896-6273(02)00830-9]
[8] Alescio-Lautier B, Michel BF, Herrera C, Elahmadi A, Chambon C, Touzet C, et al. Visual and visuospatial short-term memory in mild cognitive impairment and Alzheimer disease: role of attention. Neuropsychologia. 2007;45(8):1948-60. [DOI:10.1016/j.neuropsychologia.2006.04.033]
[9] Rusconi ML, Suardi A, Zanetti M, Rozzini L. Spatial navigation in elderly healthy subjects, amnestic and non amnestic MCI patients. J Neurol Sci. 2015;359(1-2):430-7. [DOI:10.1016/j.jns.2015.10.010]
[10] Hanes DA, McCollum G. Cognitive-vestibular interactions: a review of patient difficulties and possible mechanisms. J Vestib Res. 2006;16(3):75-91. [DOI:10.3233/VES-2006-16301]
[11] Shinder ME, Taube JS. Differentiating ascending vestibular pathways to the cortex involved in spatial cognition. J Vestib Res. 2010;20(1):3-23. [DOI:10.3233/VES-2010-0344]
[12] Smith PF, Zheng Y. From ear to uncertainty: vestibular contributions to cognitive function. Front Integr Neurosci. 2013;7:84. [DOI:10.3389/fnint.2013.00084]
[13] Smith PF. The vestibular system and cognition. Curr Opin Neurol. 2017;30(1):84-9. [DOI:10.1097/WCO.0000000000000403]
[14] Smith PF, Brandt T, Strupp M, Darlington CL, Zheng Y. Balance before reason in rats and humans. Ann N Y Acad Sci. 2009;1164:127-33. [DOI:10.1111/j.1749-6632.2008.03726.x]
[15] Harun A, Oh ES, Bigelow RT, Studenski S, Agrawal Y. Vestibular Impairment in Dementia. Otol Neurotol. 2016;37(8):1137-42. [DOI:10.1097/MAO.0000000000001157]
[16] Shamsi N, Adel Ghahraman M, Hoseinabadi R, Aghamollaii V, Jalaie S. Vestibular evoked myogenic potentials: early predictors of Alzheimer’s disease? Aud Vestib Res. 2018;27(2):80-5.
[17] Wei EX, Oh ES, Harun A, Ehrenburg M, Xue QL, Simonsick E, et al. Increased Prevalence of Vestibular Loss in Mild Cognitive Impairment and Alzheimer’s Disease. Curr Alzheimer Res. 2019;16(12):1143-50. [DOI:10.2174/1567205016666190816114838]
[18] Cohen HS, Lincoln CM, Pavlik VN, Sangi-Haghpeykar H. Changes in Measures of Vestibular and Balance Function and Hippocampus Volume in Alzheimer’s Disease and Mild Cognitive Impairment. Otol Neurotol. 2022;43(6):e663-70. [DOI:10.1097/MAO.0000000000003540]
[19] Yargholi S, Adel Ghahraman M, Hoseinabadi R, Aghamollaii V, Jalaie S. Vestibulo-ocular reflex in patients with amnestic mild cognitive impairment and normal controls: a comparative study. Aud Vestib Res. 2018;27(2):93-100.
[20] Gurvich C, Maller JJ, Lithgow B, Haghgooie S, Kulkarni J. Vestibular insights into cognition and psychiatry. Brain Res. 2013;1537:244-59. [DOI:10.1016/j.brainres.2013.08.058]
[21] Previc FH. Vestibular loss as a contributor to Alzheimer’s disease. Med Hypotheses. 2013;80(4):360-7. [DOI:10.1016/j.mehy.2012.12.023]
[22] Eleftheriadou A, Skalidi N, Velegrakis GA. Vestibular rehabilitation strategies and factors that affect the outcome. Eur Arch Otorhinolaryngol. 2012;269(11):2309-16. [DOI:10.1007/s00405-012-2019-2]
[23] Sugaya N, Arai M, Goto F. Changes in cognitive function in patients with intractable dizziness following vestibular rehabilitation. Sci Rep. 2018;8(1):9984. [DOI:10.1038/s41598-018-28350-9]
[24] Lotfi Y, Rezazadeh N, Moossavi A, Haghgoo HA, Rostami R, Bakhshi E, et al. Preliminary evidence of improved cognitive performance following vestibular rehabilitation in children with combined ADHD (cADHD) and concurrent vestibular impairment. Auris Nasus Larynx. 2017;44(6):700-7. [DOI:10.1016/j.anl.2017.01.011]
[25] Utz KS, Dimova V, Oppenländer K, Kerkhoff G. Electrified minds: transcranial direct current stimulation (tDCS) and galvanic vestibular stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology--a review of current data and future implications. Neuropsychologia. 2010;48(10):2789-810. [DOI:10.1016/j.neuropsychologia.2010.06.002]
[26] Goldberg JM, Smith CE, Fernández C. Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol. 1984;51(6):1236-56. [DOI:10.1152/jn.1984.51.6.1236]
[27] Fitzpatrick RC, Day BL. Probing the human vestibular system with galvanic stimulation. J Appl Physiol (1985). 2004;96(6):2301-16. [DOI:10.1152/japplphysiol.00008.2004]
[28] Lobel E, Kleine JF, Bihan DL, Leroy-Willig A, Berthoz A. Functional MRI of galvanic vestibular stimulation. J Neurophysiol. 1998;80(5):2699-709. [DOI:10.1152/jn.1998.80.5.2699]
[29] Fink GR, Marshall JC, Weiss PH, Stephan T, Grefkes C, Shah NJ, et al. Performing allocentric visuospatial judgments with induced distortion of the egocentric reference frame: an fMRI study with clinical implications. Neuroimage. 2003;20(3):1505-17. [DOI:10.1016/j.neuroimage.2003.07.006]
[30] Stephan T, Deutschländer A, Nolte A, Schneider E, Wiesmann M, Brandt T, et al. Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage. 2005;26(3):721-32. [DOI:10.1016/j.neuroimage.2005.02.049]
[31] Wuehr M, Boerner JC, Pradhan C, Decker J, Jahn K, Brandt T, et al. Stochastic resonance in the human vestibular system - Noise-induced facilitation of vestibulospinal reflexes. Brain Stimul. 2018;11(2):261-3. [DOI:10.1016/j.brs.2017.10.016]
[32] Wilkinson D, Nicholls S, Pattenden C, Kilduff P, Milberg W. Galvanic vestibular stimulation speeds visual memory recall. Exp Brain Res. 2008;189(2):243-8. [DOI:10.1007/s00221-008-1463-0]
[33] Wilkinson D, Zubko O, Sakel M, Coulton S, Higgins T, Pullicino P. Galvanic vestibular stimulation in hemi-spatial neglect. Front Integr Neurosci. 2014;8:4. [DOI:10.3389/fnint.2014.00004]
[34] Adel Ghahraman M, Zahmatkesh M, Pourbakht A, Seifi B, Jalaie S, Adeli S, et al. Noisy galvanic vestibular stimulation enhances spatial memory in cognitive impairment-induced by intracerebroventricular-streptozotocin administration. Physiol Behav. 2016;157:217-24. [DOI:10.1016/j.physbeh.2016.02.021]
[35] Ali Ahmed RA, Fahmy EM, Awad AM, Hamdy MM, Abd Rahman Shaker HA. Efficacy of transmastoidal galvanic stimulation on recovery outcomes in patients with unilateral periphera vestibular disorders: a randomized controlled trial. Egypt J Neurol Psychiatr Neurosurg. 2020;56(1):1-9. [DOI:10.1186/s41983-020-00207-x]
[36] Barozzi S, Di Berardino F, Arisi E, Cesarani A. A comparison between oculomotor rehabilitation and vestibular electrical stimulation in unilateral peripheral vestibular deficit. Int Tinnitus J. 2006;12(1):45-9.
[37] Carmona S, Ferrero A, Pianetti G, Escolá N, Arteaga MV, Frankel L. Galvanic vestibular stimulation improves the results of vestibular rehabilitation. Ann N Y Acad Sci. 2011;1233:E1-7. [DOI:10.1111/j.1749-6632.2011.06269.x]
[38] Eder J, Kellerer S, Amberger T, Keywan A, Dlugaiczyk J, Wuehr M, et al. Combining vestibular rehabilitation with noisy galvanic vestibular stimulation for treatment of bilateral vestibulopathy. J Neurol. 2022;269(11):5731-7. [DOI:10.1007/s00415-022-11033-x]
[39] Jack CR Jr, Bennett DA, Blennow K, Carrillo MC, Dunn B, Haeberlein SB, et al; Contributors. NIA-AA Research Framework: Toward a biological definition of Alzheimer’s disease. Alzheimers Dement. 2018;14(4):535-62. [DOI:10.1016/j.jalz.2018.02.018]
[40] Hughes CP, Berg L, Danziger WL, Coben LA, Martin RL. A new clinical scale for the staging of dementia. Br J Psychiatry. 1982;140:566-72. [DOI:10.1192/bjp.140.6.566]
[41] Foroughan M, Jafari Z, Shirin Bayan P, Ghaem Magham Farahani Z, Rahgozar M. Validation of Mini- Mental State Examination (MMSE) in The Elderly Population of Tehran. Advances in Cognitive Science. 2008;10(2):29-37. Persian.
[42] Ansari NN, Naghdi S, Hasson S, Valizadeh L, Jalaie S. Validation of a Mini-Mental State Examination (MMSE) for the Persian population: a pilot study. Appl Neuropsychol. 2010;17(3):190-5. [DOI:10.1080/09084282.2010.499773]
[43] Rashedi V, Foroughan M, Chehrehnegar N. Psychometric Properties of the Persian Montreal Cognitive Assessment in Mild Cognitive Impairment and Alzheimer Disease. Dement Geriatr Cogn Dis Extra. 2021;11(1):51-7. [DOI:10.1159/000514673]
[44] Badrkhahan SZ, Sikaroodi H, Sharifi F, Kouti L, Noroozian M. Validity and reliability of the Persian version of the Montreal Cognitive Assessment (MoCA-P) scale among subjects with Parkinson’s disease. Appl Neuropsychol Adult. 2020;27(5):431-9. [DOI:10.1080/23279095.2019.1565762]
[45] Rezvanfard M, Ekhtiari H, Noroozian M, Rezvanifar A, Nilipour R, Karimi Javan G. The Rey Auditory Verbal Learning Test: alternate forms equivalency and reliability for the Iranian adult population (Persian version). Arch Iran Med. 2011;14(2):104-9.
[46] Corsi PM. Human memory and the medial temporal region of the brain: ProQuest Information & Learning; 1973.
[47] Kessels RP, van Zandvoort MJ, Postma A, Kappelle LJ, de Haan EH. The Corsi Block-Tapping Task: standardization and normative data. Appl Neuropsychol. 2000;7(4):252-8. [DOI:10.1207/S15324826AN0704_8]
[48] Mueller ST. A partial implementation of the bica cognitive decathlon using the psychology experiment building language (PEBL). Int J Mach Conscious. 2010;02(02):273-88. [DOI:10.1142/S1793843010000497]
[49] Treisman A. Preattentive processing in vision. Comput Gr Image Process. 1985;31(2):156-77. [DOI:10.1016/S0734-189X(85)80004-9]
[50] Dilda V, MacDougall HG, Curthoys IS, Moore ST. Effects of Galvanic vestibular stimulation on cognitive function. Exp Brain Res. 2012;216(2):275-85. [DOI:10.1007/s00221-011-2929-z]
[51] Oppenländer K, Utz KS, Reinhart S, Keller I, Kerkhoff G, Schaadt AK. Subliminal galvanic-vestibular stimulation recalibrates the distorted visual and tactile subjective vertical in right-sided stroke. Neuropsychologia. 2015;74:178-83. [DOI:10.1016/j.neuropsychologia.2015.03.004]
[52] Cawthorne T. The physiological basis for head exercises. J Char Soc Physiother. 1944;3:106-7.
[53] Cooksey F. Rehabilitation in vestibular injuries. SAGE Publications; 1946. [DOI:10.1177/003591574603900523]
[54] Curthoys IS, Halmagyi HG. Vestibular compensationrecovery after unilateral vestibular loss. In: Herdman SJ, Clendaniel R, editors. Vestibular Rehabilitation 4th ed. Philadelphia: FA Davis; 2014. p. 121-50.
[55] Dix MR. The physiological basis and practical value of head exercises in the treatment of vertigo. Practitioner. 1976;217(1302):919-24.
[56] Corna S, Nardone A, Prestinari A, Galante M, Grasso M, Schieppati M. Comparison of Cawthorne-Cooksey exercises and sinusoidal support surface translations to improve balance in patients with unilateral vestibular deficit. Arch Phys Med Rehabil. 2003;84(8):1173-84. [DOI:10.1016/S0003-9993(03)00130-8]85
[57] Nardone A, Godi M, Artuso A, Schieppati M. Balance rehabilitation by moving platform and exercises in patients with neuropathy or vestibular deficit. Arch Phys Med Rehabil. 2010;91(12):1869-77. [DOI:10.1016/j.apmr.2010.09.011]
[58] Tekin Dal B, Bumin G, Aksoy S, Günaydın RÖ. Comparison of Activity-Based Home Program and Cawthorne-Cooksey Exercises in Patients With Chronic Unilateral Peripheral Vestibular Disorders. Arch Phys Med Rehabil. 2021;102(7):1300-7. [DOI:10.1016/j.apmr.2020.12.022]
[59] Kim HY. Statistical notes for clinical researchers: Sample size calculation 3. Comparison of several means using one-way ANOVA. Restor Dent Endod. 2016;41(3):231-4. [DOI:10.5395/rde.2016.41.3.231]
[60] Kim HY. Statistical notes for clinical researchers: effect size. Restor Dent Endod. 2015;40(4):328-31. [DOI:10.5395/rde.2015.40.4.328]
[61] Roh M, Lee E. Effects of gaze stability exercises on cognitive function, dynamic postural ability, balance confidence, and subjective health status in old people with mild cognitive impairment. J Exerc Rehabil. 2019;15(2):270-4. [DOI:10.12965/jer.1938026.013]
[62] Putcha D, Brickhouse M, Wolk DA, Dickerson BC; Alzheimer’s Disease Neuroimaging Initiative. Fractionating the Rey Auditory Verbal Learning Test: Distinct roles of large-scale cortical networks in prodromal Alzheimer’s disease. Neuropsychologia. 2019;129:83-92. [DOI:10.1016/j.neuropsychologia.2019.03.015]
[63] van Asselen M, Kessels RP, Neggers SF, Kappelle LJ, Frijns CJ, Postma A. Brain areas involved in spatial working memory. Neuropsychologia. 2006;44(7):1185-94. [DOI:10.1016/j.neuropsychologia.2005.10.005]
[64] LoPresti ML, Schon K, Tricarico MD, Swisher JD, Celone KA, Stern CE. Working memory for social cues recruits orbitofrontal cortex and amygdala: a functional magnetic resonance imaging study of delayed matching to sample for emotional expressions. J Neurosci. 2008;28(14):3718-28. [DOI:10.1523/JNEUROSCI.0464-08.2008]
[65] Nobre AC, Coull JT, Walsh V, Frith CD. Brain activations during visual search: contributions of search efficiency versus feature binding. Neuroimage. 2003;18(1):91-103. [DOI:10.1006/nimg.2002.1329]
[66] Lopez C, Blanke O. The thalamocortical vestibular system in animals and humans. Brain Res Rev. 2011;67(1-2):119-46. [DOI:10.1016/j.brainresrev.2010.12.002]
[67] Nagamatsu LS, Chan A, Davis JC, Beattie BL, Graf P, Voss MW, et al. Physical activity improves verbal and spatial memory in older adults with probable mild cognitive impairment: a 6-month randomized controlled trial. J Aging Res. 2013;2013:861893. [DOI:10.1155/2013/861893]
[68] Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A. 2011;108(7):3017-22. [DOI:10.1073/pnas.1015950108]
[69] Stigger FS, Zago Marcolino MA, Portela KM, Plentz RDM. Effects of Exercise on Inflammatory, Oxidative, and Neurotrophic Biomarkers on Cognitively Impaired Individuals Diagnosed with Dementia or Mild Cognitive Impairment: A Systematic Review and Meta-Analysis. J Gerontol A Biol Sci Med Sci. 2019;74(5):616-24. [DOI:10.1093/gerona/gly173]
[70] Huang X, Zhao X, Li B, Cai Y, Zhang S, Yu F, Wan Q. Biomarkers for evaluating the effects of exercise interventions in patients with MCI or dementia: A systematic review and meta-analysis. Exp Gerontol. 2021;151:111424. [DOI:10.1016/j.exger.2021.111424]
[71] Jee YS, Ko IG, Sung YH, Lee JW, Kim YS, Kim SE, et al. Effects of treadmill exercise on memory and c-Fos expression in the hippocampus of the rats with intracerebroventricular injection of streptozotocin. Neurosci Lett. 2008;443(3):188-92. [DOI:10.1016/j.neulet.2008.07.078]
[72] Teixeira CVL, Ribeiro de Rezende TJ, Weiler M, Magalhães TNC, Carletti-Cassani AFMK, Silva TQAC, et al. Cognitive and structural cerebral changes in amnestic mild cognitive impairment due to Alzheimer’s disease after multicomponent training. Alzheimers Dement (N Y). 2018;4:473-480. [DOI:10.1016/j.trci.2018.02.003]
[73] Dawidowicz L, L Ash E, Korczyn AD, Andelman F, Levy S, Elkana O. Can the RAVLT predict deterioration from MCI to dementia? Data from long term follow up. Exp Aging Res. 2021;47(4):347-56. [DOI:10.1080/0361073X.2021.1898182]
[74] Mueller ST, Piper BJ. The Psychology Experiment Building Language (PEBL) and PEBL Test Battery. J Neurosci Methods. 2014;222:250-9. [DOI:10.1016/j.jneumeth.2013.10.024]
[75] Scarpina F, D’Agata F, Priano L, Mauro A. Difference Between Young and Old Adults’ Performance on the Psychology Experiment Building Language (PEBL) Test Battery: What Is the Role of Familiarity With Technology in Cognitive Performance? Assessment. 2021;28(6):1723-34. [DOI:10.1177/1073191120918010]
[76] Piper B, Mueller ST, Talebzadeh S, Ki MJ. Evaluation of the validity of the Psychology Experiment Building Language tests of vigilance, auditory memory, and decision making. Peer J. 2016;4:e1772. [DOI:10.7717/peerj.1772]
[2] Busse A, Hensel A, Gühne U, Angermeyer MC, Riedel-Heller SG. Mild cognitive impairment: long-term course of four clinical subtypes. Neurology. 2006;67(12):2176-85. [DOI:10.1212/01.wnl.0000249117.23318.e1]
[3] Nelson AP, O’Connor MG. Mild cognitive impairment: a neuropsychological perspective. CNS Spectr. 2008;13(1):56-64. [DOI:10.1017/S1092852900016163]
[4] Petersen RC. Mild Cognitive Impairment. Continuum (Minneap Minn). 2016;22(2 Dementia):404-18. [DOI:10.1212/CON.0000000000000313]
[5] Carter SF, Caine D, Burns A, Herholz K, Lambon Ralph MA. Staging of the cognitive decline in Alzheimer’s disease: insights from a detailed neuropsychological investigation of mild cognitive impairment and mild Alzheimer’s disease. Int J Geriatr Psychiatry. 2012;27(4):423-32. [DOI:10.1002/gps.2738]
[6] Hitier M, Besnard S, Smith PF. Vestibular pathways involved in cognition. Front Integr Neurosci. 2014;8:59. [DOI:10.3389/fnint.2014.00059]
[7] Burgess N, Maguire EA, O’Keefe J. The human hippocampus and spatial and episodic memory. Neuron. 2002;35(4):625-41. [DOI:10.1016/S0896-6273(02)00830-9]
[8] Alescio-Lautier B, Michel BF, Herrera C, Elahmadi A, Chambon C, Touzet C, et al. Visual and visuospatial short-term memory in mild cognitive impairment and Alzheimer disease: role of attention. Neuropsychologia. 2007;45(8):1948-60. [DOI:10.1016/j.neuropsychologia.2006.04.033]
[9] Rusconi ML, Suardi A, Zanetti M, Rozzini L. Spatial navigation in elderly healthy subjects, amnestic and non amnestic MCI patients. J Neurol Sci. 2015;359(1-2):430-7. [DOI:10.1016/j.jns.2015.10.010]
[10] Hanes DA, McCollum G. Cognitive-vestibular interactions: a review of patient difficulties and possible mechanisms. J Vestib Res. 2006;16(3):75-91. [DOI:10.3233/VES-2006-16301]
[11] Shinder ME, Taube JS. Differentiating ascending vestibular pathways to the cortex involved in spatial cognition. J Vestib Res. 2010;20(1):3-23. [DOI:10.3233/VES-2010-0344]
[12] Smith PF, Zheng Y. From ear to uncertainty: vestibular contributions to cognitive function. Front Integr Neurosci. 2013;7:84. [DOI:10.3389/fnint.2013.00084]
[13] Smith PF. The vestibular system and cognition. Curr Opin Neurol. 2017;30(1):84-9. [DOI:10.1097/WCO.0000000000000403]
[14] Smith PF, Brandt T, Strupp M, Darlington CL, Zheng Y. Balance before reason in rats and humans. Ann N Y Acad Sci. 2009;1164:127-33. [DOI:10.1111/j.1749-6632.2008.03726.x]
[15] Harun A, Oh ES, Bigelow RT, Studenski S, Agrawal Y. Vestibular Impairment in Dementia. Otol Neurotol. 2016;37(8):1137-42. [DOI:10.1097/MAO.0000000000001157]
[16] Shamsi N, Adel Ghahraman M, Hoseinabadi R, Aghamollaii V, Jalaie S. Vestibular evoked myogenic potentials: early predictors of Alzheimer’s disease? Aud Vestib Res. 2018;27(2):80-5.
[17] Wei EX, Oh ES, Harun A, Ehrenburg M, Xue QL, Simonsick E, et al. Increased Prevalence of Vestibular Loss in Mild Cognitive Impairment and Alzheimer’s Disease. Curr Alzheimer Res. 2019;16(12):1143-50. [DOI:10.2174/1567205016666190816114838]
[18] Cohen HS, Lincoln CM, Pavlik VN, Sangi-Haghpeykar H. Changes in Measures of Vestibular and Balance Function and Hippocampus Volume in Alzheimer’s Disease and Mild Cognitive Impairment. Otol Neurotol. 2022;43(6):e663-70. [DOI:10.1097/MAO.0000000000003540]
[19] Yargholi S, Adel Ghahraman M, Hoseinabadi R, Aghamollaii V, Jalaie S. Vestibulo-ocular reflex in patients with amnestic mild cognitive impairment and normal controls: a comparative study. Aud Vestib Res. 2018;27(2):93-100.
[20] Gurvich C, Maller JJ, Lithgow B, Haghgooie S, Kulkarni J. Vestibular insights into cognition and psychiatry. Brain Res. 2013;1537:244-59. [DOI:10.1016/j.brainres.2013.08.058]
[21] Previc FH. Vestibular loss as a contributor to Alzheimer’s disease. Med Hypotheses. 2013;80(4):360-7. [DOI:10.1016/j.mehy.2012.12.023]
[22] Eleftheriadou A, Skalidi N, Velegrakis GA. Vestibular rehabilitation strategies and factors that affect the outcome. Eur Arch Otorhinolaryngol. 2012;269(11):2309-16. [DOI:10.1007/s00405-012-2019-2]
[23] Sugaya N, Arai M, Goto F. Changes in cognitive function in patients with intractable dizziness following vestibular rehabilitation. Sci Rep. 2018;8(1):9984. [DOI:10.1038/s41598-018-28350-9]
[24] Lotfi Y, Rezazadeh N, Moossavi A, Haghgoo HA, Rostami R, Bakhshi E, et al. Preliminary evidence of improved cognitive performance following vestibular rehabilitation in children with combined ADHD (cADHD) and concurrent vestibular impairment. Auris Nasus Larynx. 2017;44(6):700-7. [DOI:10.1016/j.anl.2017.01.011]
[25] Utz KS, Dimova V, Oppenländer K, Kerkhoff G. Electrified minds: transcranial direct current stimulation (tDCS) and galvanic vestibular stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology--a review of current data and future implications. Neuropsychologia. 2010;48(10):2789-810. [DOI:10.1016/j.neuropsychologia.2010.06.002]
[26] Goldberg JM, Smith CE, Fernández C. Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol. 1984;51(6):1236-56. [DOI:10.1152/jn.1984.51.6.1236]
[27] Fitzpatrick RC, Day BL. Probing the human vestibular system with galvanic stimulation. J Appl Physiol (1985). 2004;96(6):2301-16. [DOI:10.1152/japplphysiol.00008.2004]
[28] Lobel E, Kleine JF, Bihan DL, Leroy-Willig A, Berthoz A. Functional MRI of galvanic vestibular stimulation. J Neurophysiol. 1998;80(5):2699-709. [DOI:10.1152/jn.1998.80.5.2699]
[29] Fink GR, Marshall JC, Weiss PH, Stephan T, Grefkes C, Shah NJ, et al. Performing allocentric visuospatial judgments with induced distortion of the egocentric reference frame: an fMRI study with clinical implications. Neuroimage. 2003;20(3):1505-17. [DOI:10.1016/j.neuroimage.2003.07.006]
[30] Stephan T, Deutschländer A, Nolte A, Schneider E, Wiesmann M, Brandt T, et al. Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage. 2005;26(3):721-32. [DOI:10.1016/j.neuroimage.2005.02.049]
[31] Wuehr M, Boerner JC, Pradhan C, Decker J, Jahn K, Brandt T, et al. Stochastic resonance in the human vestibular system - Noise-induced facilitation of vestibulospinal reflexes. Brain Stimul. 2018;11(2):261-3. [DOI:10.1016/j.brs.2017.10.016]
[32] Wilkinson D, Nicholls S, Pattenden C, Kilduff P, Milberg W. Galvanic vestibular stimulation speeds visual memory recall. Exp Brain Res. 2008;189(2):243-8. [DOI:10.1007/s00221-008-1463-0]
[33] Wilkinson D, Zubko O, Sakel M, Coulton S, Higgins T, Pullicino P. Galvanic vestibular stimulation in hemi-spatial neglect. Front Integr Neurosci. 2014;8:4. [DOI:10.3389/fnint.2014.00004]
[34] Adel Ghahraman M, Zahmatkesh M, Pourbakht A, Seifi B, Jalaie S, Adeli S, et al. Noisy galvanic vestibular stimulation enhances spatial memory in cognitive impairment-induced by intracerebroventricular-streptozotocin administration. Physiol Behav. 2016;157:217-24. [DOI:10.1016/j.physbeh.2016.02.021]
[35] Ali Ahmed RA, Fahmy EM, Awad AM, Hamdy MM, Abd Rahman Shaker HA. Efficacy of transmastoidal galvanic stimulation on recovery outcomes in patients with unilateral periphera vestibular disorders: a randomized controlled trial. Egypt J Neurol Psychiatr Neurosurg. 2020;56(1):1-9. [DOI:10.1186/s41983-020-00207-x]
[36] Barozzi S, Di Berardino F, Arisi E, Cesarani A. A comparison between oculomotor rehabilitation and vestibular electrical stimulation in unilateral peripheral vestibular deficit. Int Tinnitus J. 2006;12(1):45-9.
[37] Carmona S, Ferrero A, Pianetti G, Escolá N, Arteaga MV, Frankel L. Galvanic vestibular stimulation improves the results of vestibular rehabilitation. Ann N Y Acad Sci. 2011;1233:E1-7. [DOI:10.1111/j.1749-6632.2011.06269.x]
[38] Eder J, Kellerer S, Amberger T, Keywan A, Dlugaiczyk J, Wuehr M, et al. Combining vestibular rehabilitation with noisy galvanic vestibular stimulation for treatment of bilateral vestibulopathy. J Neurol. 2022;269(11):5731-7. [DOI:10.1007/s00415-022-11033-x]
[39] Jack CR Jr, Bennett DA, Blennow K, Carrillo MC, Dunn B, Haeberlein SB, et al; Contributors. NIA-AA Research Framework: Toward a biological definition of Alzheimer’s disease. Alzheimers Dement. 2018;14(4):535-62. [DOI:10.1016/j.jalz.2018.02.018]
[40] Hughes CP, Berg L, Danziger WL, Coben LA, Martin RL. A new clinical scale for the staging of dementia. Br J Psychiatry. 1982;140:566-72. [DOI:10.1192/bjp.140.6.566]
[41] Foroughan M, Jafari Z, Shirin Bayan P, Ghaem Magham Farahani Z, Rahgozar M. Validation of Mini- Mental State Examination (MMSE) in The Elderly Population of Tehran. Advances in Cognitive Science. 2008;10(2):29-37. Persian.
[42] Ansari NN, Naghdi S, Hasson S, Valizadeh L, Jalaie S. Validation of a Mini-Mental State Examination (MMSE) for the Persian population: a pilot study. Appl Neuropsychol. 2010;17(3):190-5. [DOI:10.1080/09084282.2010.499773]
[43] Rashedi V, Foroughan M, Chehrehnegar N. Psychometric Properties of the Persian Montreal Cognitive Assessment in Mild Cognitive Impairment and Alzheimer Disease. Dement Geriatr Cogn Dis Extra. 2021;11(1):51-7. [DOI:10.1159/000514673]
[44] Badrkhahan SZ, Sikaroodi H, Sharifi F, Kouti L, Noroozian M. Validity and reliability of the Persian version of the Montreal Cognitive Assessment (MoCA-P) scale among subjects with Parkinson’s disease. Appl Neuropsychol Adult. 2020;27(5):431-9. [DOI:10.1080/23279095.2019.1565762]
[45] Rezvanfard M, Ekhtiari H, Noroozian M, Rezvanifar A, Nilipour R, Karimi Javan G. The Rey Auditory Verbal Learning Test: alternate forms equivalency and reliability for the Iranian adult population (Persian version). Arch Iran Med. 2011;14(2):104-9.
[46] Corsi PM. Human memory and the medial temporal region of the brain: ProQuest Information & Learning; 1973.
[47] Kessels RP, van Zandvoort MJ, Postma A, Kappelle LJ, de Haan EH. The Corsi Block-Tapping Task: standardization and normative data. Appl Neuropsychol. 2000;7(4):252-8. [DOI:10.1207/S15324826AN0704_8]
[48] Mueller ST. A partial implementation of the bica cognitive decathlon using the psychology experiment building language (PEBL). Int J Mach Conscious. 2010;02(02):273-88. [DOI:10.1142/S1793843010000497]
[49] Treisman A. Preattentive processing in vision. Comput Gr Image Process. 1985;31(2):156-77. [DOI:10.1016/S0734-189X(85)80004-9]
[50] Dilda V, MacDougall HG, Curthoys IS, Moore ST. Effects of Galvanic vestibular stimulation on cognitive function. Exp Brain Res. 2012;216(2):275-85. [DOI:10.1007/s00221-011-2929-z]
[51] Oppenländer K, Utz KS, Reinhart S, Keller I, Kerkhoff G, Schaadt AK. Subliminal galvanic-vestibular stimulation recalibrates the distorted visual and tactile subjective vertical in right-sided stroke. Neuropsychologia. 2015;74:178-83. [DOI:10.1016/j.neuropsychologia.2015.03.004]
[52] Cawthorne T. The physiological basis for head exercises. J Char Soc Physiother. 1944;3:106-7.
[53] Cooksey F. Rehabilitation in vestibular injuries. SAGE Publications; 1946. [DOI:10.1177/003591574603900523]
[54] Curthoys IS, Halmagyi HG. Vestibular compensationrecovery after unilateral vestibular loss. In: Herdman SJ, Clendaniel R, editors. Vestibular Rehabilitation 4th ed. Philadelphia: FA Davis; 2014. p. 121-50.
[55] Dix MR. The physiological basis and practical value of head exercises in the treatment of vertigo. Practitioner. 1976;217(1302):919-24.
[56] Corna S, Nardone A, Prestinari A, Galante M, Grasso M, Schieppati M. Comparison of Cawthorne-Cooksey exercises and sinusoidal support surface translations to improve balance in patients with unilateral vestibular deficit. Arch Phys Med Rehabil. 2003;84(8):1173-84. [DOI:10.1016/S0003-9993(03)00130-8]85
[57] Nardone A, Godi M, Artuso A, Schieppati M. Balance rehabilitation by moving platform and exercises in patients with neuropathy or vestibular deficit. Arch Phys Med Rehabil. 2010;91(12):1869-77. [DOI:10.1016/j.apmr.2010.09.011]
[58] Tekin Dal B, Bumin G, Aksoy S, Günaydın RÖ. Comparison of Activity-Based Home Program and Cawthorne-Cooksey Exercises in Patients With Chronic Unilateral Peripheral Vestibular Disorders. Arch Phys Med Rehabil. 2021;102(7):1300-7. [DOI:10.1016/j.apmr.2020.12.022]
[59] Kim HY. Statistical notes for clinical researchers: Sample size calculation 3. Comparison of several means using one-way ANOVA. Restor Dent Endod. 2016;41(3):231-4. [DOI:10.5395/rde.2016.41.3.231]
[60] Kim HY. Statistical notes for clinical researchers: effect size. Restor Dent Endod. 2015;40(4):328-31. [DOI:10.5395/rde.2015.40.4.328]
[61] Roh M, Lee E. Effects of gaze stability exercises on cognitive function, dynamic postural ability, balance confidence, and subjective health status in old people with mild cognitive impairment. J Exerc Rehabil. 2019;15(2):270-4. [DOI:10.12965/jer.1938026.013]
[62] Putcha D, Brickhouse M, Wolk DA, Dickerson BC; Alzheimer’s Disease Neuroimaging Initiative. Fractionating the Rey Auditory Verbal Learning Test: Distinct roles of large-scale cortical networks in prodromal Alzheimer’s disease. Neuropsychologia. 2019;129:83-92. [DOI:10.1016/j.neuropsychologia.2019.03.015]
[63] van Asselen M, Kessels RP, Neggers SF, Kappelle LJ, Frijns CJ, Postma A. Brain areas involved in spatial working memory. Neuropsychologia. 2006;44(7):1185-94. [DOI:10.1016/j.neuropsychologia.2005.10.005]
[64] LoPresti ML, Schon K, Tricarico MD, Swisher JD, Celone KA, Stern CE. Working memory for social cues recruits orbitofrontal cortex and amygdala: a functional magnetic resonance imaging study of delayed matching to sample for emotional expressions. J Neurosci. 2008;28(14):3718-28. [DOI:10.1523/JNEUROSCI.0464-08.2008]
[65] Nobre AC, Coull JT, Walsh V, Frith CD. Brain activations during visual search: contributions of search efficiency versus feature binding. Neuroimage. 2003;18(1):91-103. [DOI:10.1006/nimg.2002.1329]
[66] Lopez C, Blanke O. The thalamocortical vestibular system in animals and humans. Brain Res Rev. 2011;67(1-2):119-46. [DOI:10.1016/j.brainresrev.2010.12.002]
[67] Nagamatsu LS, Chan A, Davis JC, Beattie BL, Graf P, Voss MW, et al. Physical activity improves verbal and spatial memory in older adults with probable mild cognitive impairment: a 6-month randomized controlled trial. J Aging Res. 2013;2013:861893. [DOI:10.1155/2013/861893]
[68] Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A. 2011;108(7):3017-22. [DOI:10.1073/pnas.1015950108]
[69] Stigger FS, Zago Marcolino MA, Portela KM, Plentz RDM. Effects of Exercise on Inflammatory, Oxidative, and Neurotrophic Biomarkers on Cognitively Impaired Individuals Diagnosed with Dementia or Mild Cognitive Impairment: A Systematic Review and Meta-Analysis. J Gerontol A Biol Sci Med Sci. 2019;74(5):616-24. [DOI:10.1093/gerona/gly173]
[70] Huang X, Zhao X, Li B, Cai Y, Zhang S, Yu F, Wan Q. Biomarkers for evaluating the effects of exercise interventions in patients with MCI or dementia: A systematic review and meta-analysis. Exp Gerontol. 2021;151:111424. [DOI:10.1016/j.exger.2021.111424]
[71] Jee YS, Ko IG, Sung YH, Lee JW, Kim YS, Kim SE, et al. Effects of treadmill exercise on memory and c-Fos expression in the hippocampus of the rats with intracerebroventricular injection of streptozotocin. Neurosci Lett. 2008;443(3):188-92. [DOI:10.1016/j.neulet.2008.07.078]
[72] Teixeira CVL, Ribeiro de Rezende TJ, Weiler M, Magalhães TNC, Carletti-Cassani AFMK, Silva TQAC, et al. Cognitive and structural cerebral changes in amnestic mild cognitive impairment due to Alzheimer’s disease after multicomponent training. Alzheimers Dement (N Y). 2018;4:473-480. [DOI:10.1016/j.trci.2018.02.003]
[73] Dawidowicz L, L Ash E, Korczyn AD, Andelman F, Levy S, Elkana O. Can the RAVLT predict deterioration from MCI to dementia? Data from long term follow up. Exp Aging Res. 2021;47(4):347-56. [DOI:10.1080/0361073X.2021.1898182]
[74] Mueller ST, Piper BJ. The Psychology Experiment Building Language (PEBL) and PEBL Test Battery. J Neurosci Methods. 2014;222:250-9. [DOI:10.1016/j.jneumeth.2013.10.024]
[75] Scarpina F, D’Agata F, Priano L, Mauro A. Difference Between Young and Old Adults’ Performance on the Psychology Experiment Building Language (PEBL) Test Battery: What Is the Role of Familiarity With Technology in Cognitive Performance? Assessment. 2021;28(6):1723-34. [DOI:10.1177/1073191120918010]
[76] Piper B, Mueller ST, Talebzadeh S, Ki MJ. Evaluation of the validity of the Psychology Experiment Building Language tests of vigilance, auditory memory, and decision making. Peer J. 2016;4:e1772. [DOI:10.7717/peerj.1772]
| Files | ||
| Issue | Vol 32 No 3 (2023) | |
| Section | Research Article(s) | |
| DOI | https://doi.org/10.18502/avr.v32i3.12933 | |
| Keywords | ||
| Mild cognitive impairment spatial memory verbal memory hippocampus galvanic vestibular stimulation vestibular rehabilitation | ||
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How to Cite
1.
Kamali B, Adel Ghahraman M, Hoseinabadi R, Aghamollaii V, Jalaie S. Combination of Vestibular Rehabilitation and Galvanic Vestibular Stimulation Improves Verbal and Visuospatial Memory: A Randomized Control Trial in Patients with Amnestic Mild Cognitive Impairment. Aud Vestib Res. 2023;32(3):174-185.
