REVIEW ARTICLES
Vestibular Function in Mild Cognitive Impairment and Alzheimer's Disease: A Narrative Review
Hafif Bilişsel Bozuklukta ve Alzheimer Hastalığında Vestibüler Fonksiyon: Geleneksel Derleme
Received Date : 02 Feb 2024
Accepted Date : 21 May 2024
Available Online : 28 May 2024
Anı PARABAKAN POLATa, Berna Deniz KUNTMANa
aUniversity of Health Sciences Gülhane Faculty of Health Sciences, Department of Audiology, Ankara, Türkiye
Doi: 10.24179/kbbbbc.2024-101930 - Makale Dili: EN
Journal of Ear Nose Throat and Head Neck Surgery. 2024;32(3):139-46.
Copyright © 2020 by Turkey Association of Society of Ear Nose Throat and Head Neck Surgery. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
ABSTRACT
The vestibular system is responsible for gaze stabilization
and postural control. Recent studies have shown that vestibular function
is related to various cognitive processes, too. These studies have examined
the effect of the vestibular system on cognitive functions as a
whole. However, it is unclear how different parts of the vestibular system,
the semicircular canals and otolith organs, contribute to these processes.
Several studies investigating the relationship between vestibular
system and cognition have evaluated vestibular function in adults with
Alzheimer’s disease and mild cognitive impairment. In this review, the
current literature evaluating vestibular function in adults with cognitive
impairment will be investigated and we will discuss possible causal
links between the vestibular and cognitive functions. Electronic
databases such as PubMed, Cochrane Library, Science Direct, Google
Scholar were searched using the keywords of “cognition”, “cognitive
function”, “cognitive impairment”, “mild cognitive impairment”,
“Alzheimer’s disease”, “dementia”, “vestibular system”, “vestibular
function”, “vestibular function tests”, “Vestibular Evoked Myogenic
Potentials”, “ocular Vestibular Evoked Myogenic Potentials”, “cervical
Vestibular Evoked Myogenic Potentials”, “Video Head Impulse
Test”, “Videonystagmography”, “oculomotor tests” and various combinations
of these keywords between January 2023 and 2024. After the
titles and abstracts of the relevant articles were reviewed by the researchers,
the articles related to the research topic were listed and reviewed.
Although the findings obtained from the studies using different
vestibular tests in Alzheimer's disease and mild cognitive impairment
vary, the studies indicate the importance of the Vestibular Evoked Myogenic
Potentials test in the early diagnosis of Alzheimer's disease. Further
studies are needed in which vestibular functions are evaluated in
adults with cognitive impairment.
Keywords: Cognition; vestibular function test; Alzheimer’s disease; mild cognitive impairment
ÖZET
Vestibüler sistem bakış stabilizasyonu ve postüral kontrolün
sağlanmasından sorumludur. Son yıllarda yapılan araştırmalar, vestibüler
işlevin sadece denge ve postüral kontrolü sürdürmekle değil, aynı
zamanda çeşitli bilişsel süreçlerle de ilişkili olduğunu göstermiştir. Bu
çalışmalar, vestibüler sistemin bilişsel işlevler üzerindeki etkisini bir
bütün olarak ele almıştır. Ancak vestibüler sistemin semisirküler kanallar
ve otolit organlar gibi farklı bölümlerinin bu süreçlere nasıl katkıda
bulunduğu hâlâ açık değildir. Vestibüler sistem ile biliş arasındaki
ilişkiyi araştıran çalışmaların bir kısmında, Alzheimer hastalığı ve hafif
bilişsel bozukluğu olan erişkinlerde vestibüler fonksiyon değerlendirilmiştir.
Bu derlemede, bilişsel bozukluğu olan erişkinlerde vestibüler
işlevi değerlendiren güncel literatür incelenecek ve vestibüler ve bilişsel
işlevler arasındaki olası nedensel bağlantılar tartışılacaktır. Ocak
2023-2024 tarihleri arasında PubMed, Cochrane Library, Science Direct,
Google Scholar gibi elektronik veri tabanlarında “biliş”, “bilişsel
fonksiyon”, “bilişsel bozukluk”, “hafif bilişsel bozukluk”, “Alzheimer
hastalığı”, “demans”, “vestibüler sistem”, “vestibüler fonksiyon”, “vestibüler
fonksiyon testleri”, “Vestibüler Uyarılmış Miyojenik Potansiyeller”,
“oküler Vestibüler Uyarılmış Miyojenik Potansiyeller”,
“servikal Vestibüler Uyarılmış Miyojenik Potansiyeller”, “Video Head
İmpuls Test”, “Videonistagmografi”, “okülomotor testler” anahtar kelimeleri
ve bu anahtar kelimelerin çeşitli kombinasyonları kullanılarak
arama yapılmıştır. İlgili makalelerin başlıkları ve özetleri araştırmacılar
tarafından incelendikten sonra araştırma konusuyla ilgili makaleler
listelenerek incelenmiştir. Alzheimer hastalığı ve hafif bilişsel bozuklukta
farklı vestibüler testler kullanılarak yapılan çalışmalardan elde
edilen bulgular farklılık göstermekle birlikte, çalışmalar Alzheimer hastalığının
erken teşhisinde Vestibüler Uyarılmış Miyojenik Potansiyeller
testinin önemini ortaya koymaktadır.Bilişsel bozukluğu olan
erişkinlerde vestibüler fonksiyonların değerlendirildiği ileri çalışmalara
ihtiyaç vardır.
Anahtar Kelimeler: Biliş; vestibüler fonksiyon testleri; Alzheimer Hastalığı; hafif bilişsel bozukluk
KAYNAKLAR
- Smith PF. The vestibular system and cognition. Curr Opin Neurol. 2017;30(1):84-9. [Crossref] [PubMed]
- Previc FH. Vestibular loss as a contributor to Alzheimer's disease. Med Hypotheses. 2013;80(4):360-7. [Crossref] [PubMed]
- Baek JH, Zheng Y, Darlington CL, Smith PF. Evidence that spatial memory deficits following bilateral vestibular deafferentation in rats are probably permanent. Neurobiol Learn Mem. 2010;94(3):402-13. [Crossref] [PubMed]
- Bigelow RT, Agrawal Y. Vestibular involvement in cognition: Visuospatial ability, attention, executive function, and memory. J Vestib Res. 2015;25(2):73-89. [Crossref] [PubMed]
- Brandt T, Schautzer F, Hamilton DA, Brüning R, Markowitsch HJ, Kalla R, et al. Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain. 2005;128(Pt 11):2732-41. [Crossref] [PubMed]
- Hüfner K, Hamilton DA, Kalla R, Stephan T, Glasauer S, Ma J, et al. Spatial memory and hippocampal volume in humans with unilateral vestibular deafferentation. Hippocampus. 2007;17(6):471-85. [Crossref] [PubMed]
- Mujdeci B, Turkyilmaz D, Yagcioglu S, Aksoy S. The effects of concurrent cognitive tasks on postural sway in healthy subjects. Braz J Otorhinolaryngol. 2016;82(1):3-10. [Crossref] [PubMed] [PMC]
- Agrawal Y, Smith PF, Rosenberg PB. Vestibular impairment, cognitive decline and Alzheimer's disease: balancing the evidence. Aging Ment Health. 2020;24(5):705-8. [Crossref] [PubMed] [PMC]
- Bigelow RT, Semenov YR, Trevino C, Ferrucci L, Resnick SM, Simonsick EM, et al. Association between visuospatial ability and vestibular function in the Baltimore longitudinal study of aging. J Am Geriatr Soc. 2015;63(9):1837-44. [Crossref] [PubMed] [PMC]
- Birdane L, Incesulu A, Gurbuz MK, Ozbabalik D. Sacculocolic reflex in patients with dementia: is it possible to use it for early diagnosis? Neurol Sci. 2012;33(1):17-21. [Crossref] [PubMed]
- Harun A, Oh ES, Bigelow RT, Studenski S, Agrawal Y. Vestibular Impairment in Dementia. Otol Neurotol. 2016;37(8):1137-42. [Crossref] [PubMed] [PMC]
- Micarelli A, Viziano A, Della-Morte D, Augimeri I, Alessandrini M. Degree of functional impairment associated with vestibular hypofunction among older adults with cognitive decline. Otol Neurotol. 2018;39(5):e392-e400. [Crossref] [PubMed]
- Nakamagoe K, Fujimiya S, Koganezawa T, Kadono K, Shimizu K, Fujizuka N, et al. Vestibular function impairment in Alzheimer's disease. J Alzheimers Dis. 2015;47(1):185-96. [Crossref] [PubMed]
- Nakamagoe K, Kadono K, Koganezawa T, Takiguchi M, Terada M, Yamamoto F, et al. Vestibular impairment in frontotemporal dementia syndrome. Dement Geriatr Cogn Dis Extra. 2016;6(2):194-204. [Crossref] [PubMed] [PMC]
- Wei EX, Oh ES, Harun A, Ehrenburg M, Agrawal Y. Saccular impairment in Alzheimer's disease is associated with driving difficulty. Dement Geriatr Cogn Disord. 2017;44(5-6):294-302. [Crossref] [PubMed] [PMC]
- Wei EX, Oh ES, Harun A, Ehrenburg M, Agrawal Y. Vestibular loss predicts poorer spatial cognition in patients with Alzheimer's Disease. J Alzheimers Dis. 2018;61(3):995-1003. [Crossref] [PubMed]
- Çelebisoy N. Vestibüler sistem, navigasyon, kognisyon. Ardıç FN, editör. Vertigo. 2. Baskı. İzmir: US Akademi; 2019. p.31-5.
- Stackman RW, Clark AS, Taube JS. Hippocampal spatial representations require vestibular input. Hippocampus. 2002;12(3):291-303. [Crossref] [PubMed] [PMC]
- Frederickson CJ, Frederickson MH, Lewis C, Howell GA, Smylie C, Wright CG. Hippocampal EEG in normal mice and in mice with congenital vestibular defects. Behav Neural Biol. 1982;34(2):121-31. [Crossref] [PubMed]
- Arnolds DE, Lopes da Silva FH, Boeijinga P, Kamp A, Aitink W. Hippocampal EEG and motor activity in the cat: the role of eye movements and body acceleration. Behav Brain Res. 1984;12(2):121-35. [Crossref] [PubMed]
- Matthews BL, Campbell KA, Deadwyler SA. Rotational stimulation disrupts spatial learning in fornix-lesioned rats. Behav Neurosci. 1988;102(1):35-42. [Crossref] [PubMed]
- Horii A, Takeda N, Mochizuki T, Okakura-Mochizuki K, Yamamoto Y, Yamatodani A. Effects of vestibular stimulation on acetylcholine release from rat hippocampus: an in vivo microdialysis study. J Neurophysiol. 1994;72(2):605-11. [Crossref] [PubMed]
- Sharp PE, Blair HT, Etkin D, Tzanetos DB. Influences of vestibular and visual motion information on the spatial firing patterns of hippocampal place cells. J Neurosci. 1995;15(1 Pt 1):173-89. [Crossref] [PubMed] [PMC]
- Gavrilov VV, Wiener SI, Berthoz A. Enhanced hippocampal theta EEG during whole body rotations in awake restrained rats. Neurosci Lett. 1995;197(3):239-41. [Crossref] [PubMed]
- Moffat SD, Elkins W, Resnick SM. Age differences in the neural systems supporting human allocentric spatial navigation. Neurobiol Aging. 2006;27(7):965-72. [Crossref] [PubMed]
- Moser E, Moser MB. Mapping your every move. Cerebrum. 2014;2014:4. [PubMed] [PMC]
- Moser MB, Rowland DC, Moser EI. Place cells, grid cells, and memory. Cold Spring Harb Perspect Biol. 2015;7(2):a021808. [Crossref] [PubMed] [PMC]
- O'Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971;34(1):171-5. [Crossref] [PubMed]
- Woollett K, Maguire EA. Exploring anterograde associative memory in London taxi drivers. Neuroreport. 2012;23(15):885-8. [Crossref] [PubMed] [PMC]
- Jacob PY, Poucet B, Liberge M, Save E, Sargolini F. Vestibular control of entorhinal cortex activity in spatial navigation. Front Integr Neurosci. 2014;8:38. [Crossref] [PubMed] [PMC]
- Lisman J, Buzsáki G, Eichenbaum H, Nadel L, Ranganath C, Redish AD. Viewpoints: how the hippocampus contributes to memory, navigation and cognition. Nat Neurosci. 2017;20(11):1434-47. Erratum in: Nat Neurosci. 2017. [Crossref] [PubMed] [PMC]
- İzci Y, Erbaş YC. Hipokampus: yapısı ve fonksiyonları [Hippocampus: its structure and functions]. Türk Nöroşir Derg. 2015;25(3):287-95. [Link]
- Filimon F. Are All Spatial Reference Frames Egocentric? Reinterpreting evidence for allocentric, object-centered, or world-centered reference frames. Front Hum Neurosci. 2015;9:648. [Crossref] [PubMed] [PMC]
- Brandt T, Zwergal A, Glasauer S. 3-D spatial memory and navigation: functions and disorders. Curr Opin Neurol. 2017;30(1):90-7. [Crossref] [PubMed]
- Colombo D, Serino S, Tuena C, Pedroli E, Dakanalis A, Cipresso P, et al. Egocentric and allocentric spatial reference frames in aging: A systematic review. Neurosci Biobehav Rev. 2017;80:605-21. [Crossref] [PubMed]
- Tolman EC. Cognitive maps in rats and men. Psychol Rev. 1948;55(4):189-208. [Crossref] [PubMed]
- O'Keefe J, Conway DH. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp Brain Res. 1978;31(4):573-90. [Crossref] [PubMed]
- Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. Microstructure of a spatial map in the entorhinal cortex. Nature. 2005;436(7052):801-6. [Crossref] [PubMed]
- Burgess N. Spatial cognition and the brain. Ann N Y Acad Sci. 2008;1124:77-97. [Crossref] [PubMed]
- Moser EI, Kropff E, Moser MB. Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci. 2008;31:69-89. [Crossref] [PubMed]
- Moser EI, Roudi Y, Witter MP, Kentros C, Bonhoeffer T, Moser MB. Grid cells and cortical representation. Nat Rev Neurosci. 2014;15(7):466-81. [Crossref] [PubMed]
- 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. [Crossref] [PubMed] [PMC]
- Baydan M, Caliskan H, Balam-Yavuz B, Aksoy S, Böke B. The Interaction Between Mild Cognitive Impairment with Vestibulo-ocular Reflex, Dynamic Visual Acuity and Postural Balance in Older Adults. Exp Gerontol. 2020;130:110785. [Crossref] [PubMed]
- Previc FH, Krueger WW, Ross RA, Roman MA, Siegel G. The relationship between vestibular function and topographical memory in older adults. Front Integr Neurosci. 2014;8:46. [Crossref] [PubMed] [PMC]
- Curthoys IS, MacDougall HG, Vidal PP, de Waele C. Sustained and transient vestibular systems: a physiological basis for interpreting vestibular function. Front Neurol. 2017;8:117. [Crossref] [PubMed] [PMC]
- Smith PF. The growing evidence for the importance of the otoliths in spatial memory. Front Neural Circuits. 2019;13:66. [Crossref] [PubMed] [PMC]
- Kammermeier S, Singh A, Noachtar S, Krotofil I, Bötzel K. Intermediate latency evoked potentials of cortical multimodal vestibular areas: acoustic stimulation. Clin Neurophysiol. 2015;126(3):614-25. [Crossref] [PubMed]
- Erbek S. Vestibüler uyarılmış kas potansiyelleri (VEMP). Ardıç FN, editör. Vertigo. 2. Baskı. İzmir: US Akademi; 2019. p.179-90.
- Cullen KE. The vestibular system: multimodal integration and encoding of self-motion for motor control. Trends Neurosci. 2012;35(3):185-96. [Crossref] [PubMed] [PMC]
- Smith PF. Vestibular dysfunction and Alzheimer's disease. Med Hypotheses. 2013;81(6):1169-70. [Crossref] [PubMed]
- Smith PF, Zheng Y. From ear to uncertainty: vestibular contributions to cognitive function. Front Integr Neurosci. 2013;7:84. [Crossref] [PubMed] [PMC]
- Welgampola MS, Colebatch JG. Vestibulocollic reflexes: normal values and the effect of age. Clin Neurophysiol. 2001;112(11):1971-9. [Crossref] [PubMed]
- Ross MD, Peacor D, Johnsson LG, Allard LF. Observations on normal and degenerating human otoconia. Ann Otol Rhinol Laryngol. 1976;85(3 pt 1):310-26. [Crossref] [PubMed]
- Yılmaz N, Söylemez E, İla K, Söylemez T, Ertuğrul S. Yaşlanmanın okülomotor fonksiyonlara etkisi [The effect of aging on oculomotor functions]. KBB ve BBC Dergisi. 2020;28(1):16-21. [Crossref]
- Lee DY, Fletcher E, Carmichael OT, Singh B, Mungas D, Reed B, et al. Sub-regional hippocampal injury is associated with fornix degeneration in Alzheimer's disease. Front Aging Neurosci. 2012;4:1. [Crossref] [PubMed] [PMC]
- Papathanasiou ES, Murofushi T, Akin FW, Colebatch JG. International guidelines for the clinical application of cervical vestibular evoked myogenic potentials: an expert consensus report. Clin Neurophysiol. 2014;125(4):658-66. [Crossref] [PubMed]
- Rosengren SM, Welgampola MS, Colebatch JG. Vestibular evoked myogenic potentials: past, present and future. Clin Neurophysiol. 2010;121(5):636-51. [Crossref] [PubMed]
- McCaslin DL. Eye movement examination. In: McCaslin DL, ed. Electronystagmography and Videonystagmography (ENG/VNG). 2nd ed. San Diego, CA: Plural Publishing; 2019. p.87-122.