Review Article

Vestibular contribution to memory processing

Abstract

Background and Aim: The vestibular system contributes in the stabilization of the head and body, orientation, and gazing through the processing of sensory inputs. A wealth of evidence supports the involvement of vestibular information in higher functions, too.
Methods: In this paper, we reviewed the previous studies on the effect of the vestibular system on memory as one of the cognitive functions.
Results: Clinical and laboratory findings indicate the association of vestibular inputs (besides postural control and oculomotor) with a variety of higher functions, especially memory function. Because part of the memory function is determined by other cognitive processes i.e. attention capacity, emotional disturbances, and executive functions, the study of the effect of vestibular inputs on these functions provides a more accurate view of how the vestibular inputs affect memory performance.
Conclusion: Although our current knowledge on vestibular-memory interaction is increasing, the exact involvement of vestibular signals in memory representations is still unclear and needs further studies to determine the theoretical basis of vestibular involvement in memory processing

1. Smith PF, Darlington CL, Zheng Y. Move it or lose it--is stimulation of the vestibular system necessary for normal spatial memory? Hippocampus. 2010;20(1):36-43. doi: 10.1002/hipo.2058
2. Highstein SM. Anatomy and physiology of the central and peripheral vestibular system: overview. In: Highstein SM, Fay RR, Popper AN, editors. Springer handbook of auditory research. New York: Springer; 2004. p. 1-10.
3. Eliot L. What's going on in there? How the brain and mind develop in the first five years of life. 1st ed. New York: Bantam; 1999.
4. Holstein GR, Friedrich VL Jr, Martinelli GP, Ogorodnikov D, Yakushin SB, Cohen B. Fos expression in neurons of the rat vestibulo-autonomic pathway activated by sinusoidal galvanic vestibular stimulation. Front Neurol. 2012;3:4. doi: 10.3389/fneur.2012.00004
5. Khan S, Chang R. Anatomy of the vestibular system: A review. NeuroRehabilitation. 2013;32(3):437-43. doi: 10.3233/NRE-130866
6. Smith PF. The vestibular system and cognition. Current opinion in neurology. 2017;30(1):84-9. doi: 10.1097/WCO.0000000000000403
7. Angelaki DE, Cullen KE. Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci. 2008;31:125-50. doi: 10.1146/annurev.neuro.31.060407.125555
8. Grabherr L, Macauda G, Lenggenhager B. The moving history of vestibular stimulation as a therapeutic intervention. Multisens Res. 2015;28(5-6):653-87.
9. Bigelow RT, Agrawal Y. Vestibular involvement in cognition: Visuospatial ability, attention, executive function, and memory. J Vestib Res. 2015;25(2):73-89. doi: 10.3233/VES-150544
10. 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
11. Hitier M, Besnard S, Smith PF. Vestibular pathways involved in cognition. Front Integr Neurosci. 2014;8:59. doi: 10.3389/fnint.2014.00059
12. 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
13. Mazzola L, Lopez C, Faillenot I, Chouchou F, Mauguière F, Isnard J. Vestibular responses to direct stimulation of the human insular cortex. Ann Neurol. 2014;76(4):609-19. doi: 10.1002/ana.24252
14. 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
15. 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. doi: 10.1002/hipo.20283
16. Lopez C. A neuroscientific account of how vestibular disorders impair bodily self-consciousness. Front Integr Neurosci. 2013;7:91. doi: 10.3389/fnint.2013.00091
17. Besnard S, Lopez C, Brandt T, Denise P, Smith PF. Editorial: the vestibular system in cognitive and memory processes in mammalians. Front Integr Neurosci. 2015;9:55. doi: 10.3389/fnint.2015.00055
18. Hanes DA, McCollum G. Cognitive-vestibular interactions: a review of patient difficulties and possible mechanisms. J Vestib Res. 2006;16(3):75-91.
19. 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. doi: 10.1093/brain/awh617
20. Glikmann-Johnston Y, Saling MM, Reutens DC, Stout JC. Hippocampal 5-HT1A receptor and spatial learning and memory. Front Pharmacol. 2015;6:289. doi: 10.3389/fphar.2015.00289
21. Squire LR. Memory and brain systems: 1969-2009. J Neurosci. 2009;29(41):12711-6. doi: 10.1523/JNEUROSCI.3575-09.2009
22. Moser EI, Kropff E, Moser MB. Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci. 2008;31:69-89. doi: 10.1146/annurev.neuro.31.061307.090723
23. Smith PF, Geddes LH, Baek JH, Darlington CL, Zheng Y. Modulation of memory by vestibular lesions and galvanic vestibular stimulation. Front Neurol. 2010;1:141. doi: 10.3389/fneur.2010.00141
24. Wilkinson D, Morris R, Milberg W, Sakel M. Caloric vestibular stimulation in aphasic syndrome. Front Integr Neurosci. 2013;7:99. doi: 10.3389/fnint.2013.00099
25. Popp P, Wulff M, Finke K, Rühl M, Brandt T, Dieterich M. Cognitive deficits in patients with a chronic vestibular failure. J Neurol. 2017;264(3):554-563. doi: 10.1007/s00415-016-8386-7
26. 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
27. Grimm RJ, Hemenway WG, Lebray PR, Black FO. The perilymph fistula syndrome defined in mild head trauma. Acta Otolaryngol Suppl. 1989;464:1-40.
28. Ghaheri F, Adel Ghahraman M, Jarollahi F, Jalaie S. [Visuo-spatial memory enhancement by galvanic vestibular stimulation: A preliminary report]. Audiol. 2014;23(1):50-61. Persian.
29. Schautzer F, Hamilton D, Kalla R, Strupp M, Brandt T. Spatial memory deficits in patients with chronic bilateral vestibular failure. Ann N Y Acad Sci. 2003;1004:316-24.
30. Kremmyda O, Hüfner K, Flanagin VL, Hamilton DA, Linn J, Strupp M, et al. Beyond dizziness: virtual navigation, spatial anxiety and hippocampal volume in bilateral vestibulopathy. Front Hum Neurosci. 2016;10:139. doi: 10.3389/fnhum.2016.00139
31. Guidetti G, Monzani D, Trebbi M, Rovatti V. Impaired navigation skills in patients with psychological distress and chronic peripheral vestibular hypofunction without vertigo. Acta Otorhinolaryngol Ital. 2008;28(1):21-5.
32. 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. doi: 10.1111/jgs.13609
33. Wiener-Vacher SR, Hamilton DA, Wiener SI. Vestibular activity and cognitive development in children: perspectives. Front Integr Neurosci. 2013;7:92. doi: 10.3389/fnint.2013.00092
34. Russell NA, Horii A, Smith PF, Darlington CL, Bilkey DK. Long-term effects of permanent vestibular lesions on hippocampal spatial firing. J Neurosci. 2003;23(16):6490-8.
35. Russell NA, Horii A, Smith PF, Darlington CL, Bilkey DK. Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat. J Neurophysiol. 2006;96(1):4-14. doi: 10.1152/jn.00953.2005
36. Tai SK, Ma J, Ossenkopp KP, Leung LS. Activation of immobility-related hippocampal theta by cholinergic septohippocampal neurons during vestibular stimulation. Hippocampus. 2012;22(4):914-25. doi: 10.1002/hipo.20955
37. Neo P, Carter D, Zheng Y, Smith P, Darlington C, McNaughton N. Septal elicitation of hippocampal theta rhythm did not repair cognitive and emotional deficits resulting from vestibular lesions. Hippocampus. 2012;22(5):1176-87. doi: 10.1002/hipo.20963
38. Zheng Y, Mason-Parker SE, Logan B, Darlington CL, Smith PF, Abraham WC. Hippocampal synaptic transmission and LTP in vivo are intact following bilateral vestibular deafferentation in the rat. Hippocampus. 2010;20(4):461-8. doi: 10.1002/hipo.20645
39. Cutfield NJ, Scott G, Waldman AD, Sharp DJ, Bronstein AM. Visual and proprioceptive interaction in patients with bilateral vestibular loss. Neuroimage Clin. 2014;4:274-82. doi: 10.1016/j.nicl.2013.12.013
40. Besnard S, Machado ML, Vignaux G, Boulouard M, Coquerel A, Bouet V, et al. Influence of vestibular input on spatial and nonspatial memory and on hippocampal NMDA receptors. Hippocampus. 2012;22(4):814-26. doi: 10.1002/hipo.20942
41. Zheng Y, Balabhadrapatruni S, Baek JH, Chung P, Gliddon C, Zhang M, et al. The effects of bilateral vestibular loss on hippocampal volume, neuronal number, and cell proliferation in rats. Front Neurol. 2012;3:20. doi: 10.3389/fneur.2012.00020
42. Seo YJ, Kim J, Kim SH. The change of hippocampal volume and its relevance with inner ear function in Meniere's disease patients. Auris Nasus Larynx. 2016;43(6):620-5. doi: 10.1016/j.anl.2016.01.006
43. Göttlich M, Jandl NM, Sprenger A, Wojak JF, Münte TF, Krämer UM, et al. Hippocampal gray matter volume in bilateral vestibular failure. Hum Brain Mapp. 2016;37(5):1998-2006. doi: 10.1002/hbm.23152
44. Balabhadrapatruni S, Zheng Y, Napper R, Smith PF. Basal dendritic length is reduced in the rat hippocampus following bilateral vestibular deafferentation. Neurobiol Learn Mem. 2016;131:56-60. doi: 10.1016/j.nlm.2016.03.009
45. 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
46. Aitken P, Zheng Y, Smith PF. Ethovision™ analysis of open field behaviour in rats following bilateral vestibular loss. J Vestib Res. 2017;27(2-3):89-101. doi: 10.3233/VES-170612
47. zu Eulenburg P, Stoeter P, Dieterich M. Voxel-based morphometry depicts central compensation after vestibular neuritis. Ann Neurol. 2010;68(2):241-9. doi: 10.1002/ana.22063
48. Brandt T, Zwergal A, Glasauer S. 3-D spatial memory and navigation: functions and disorders. Curr Opin Neurol. 2017;30(1):90-97. doi: 10.1097/WCO.0000000000000415
49. Helmchen C, Ye Z, Sprenger A, Münte TF. Changes in resting-state fMRI in vestibular neuritis. Brain Struct Funct. 2014;219(6):1889-900. doi: 10.1007/s00429-013-0608-5
50. Hüfner K, Binetti C, Hamilton DA, Stephan T, Flanagin VL, Linn J, et al. Structural and functional plasticity of the hippocampal formation in professional dancers and slackliners. Hippocampus. 2011;21(8):855-65. doi: 10.1002/hipo.20801
51. Stackman RW, Clark AS, Taube JS. Hippocampal spatial representations require vestibular input. Hippocampus. 2002;12(3):291-303. doi: 10.1002/hipo.1112
52. Buzsáki G. Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus. 2005;15(7):827-40. doi: 10.1002/hipo.20113
53. Yoder RM, Taube JS. Head direction cell activity in mice: robust directional signal depends on intact otolith organs. J Neurosci. 2009;29(4):1061-76. doi: 10.1523/JNEUROSCI.1679-08.2009
54. 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. doi: 10.3389/fnint.2014.00038
55. Grabherr L, Mast FW. Effects of microgravity on cognition: The case of mental imagery. J Vestib Res. 2010;20(1-2):53-60. doi: 10.3233/VES-2010-0364
56. Oman C. Spatial orientation and navigation in microgravity. In: Mast FW, Jäncke L, editors. Spatial processing in navigation, imagery and perception. New York: Springer; 2007. p. 209-48.
57. Fitzpatrick RC, Day BL. Probing the human vestibular system with galvanic stimulation. J Appl Physiol. 2004;96(6):2301-16. doi: 10.1152/japplphysiol.00008.2004
58. Palla A, Lenggenhager B. Ways to investigate vestibular contributions to cognitive processes. Front Integr Neurosci. 2014;8:40. doi: 10.3389/fnint.2014.00040
59. Lopez C, Blanke O, Mast FW. The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience. 2012;212:159-79. doi: 10.1016/j.neuroscience.2012.03.028
60. 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
61. 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
62. Cheng YY, Kuo CH, Hsieh WL, Lee SD, Lee WJ, Chen LK, et al. Anxiety, depression and quality of life (QoL) in patients with chronic dizziness. Arch Gerontol Geriatr. 2012;54(1):131-5. doi: 10.1016/j.archger.2011.04.007
63. 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
64. 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
65. Lee JW, Lee GE, An JH, Yoon SW, Heo M, Kim HY. Effects of galvanic vestibular stimulation on visual memory recall and EEG. J Phys Ther Sci. 2014;26(9):1333-6. doi: 10.1589/jpts.26.1333
66. 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
67. Bächtold D, Baumann T, Sándor PS, Kritos M, Regard M, Brugger P. Spatial- and verbal-memory improvement by cold-water caloric stimulation in healthy subjects. Exp Brain Res. 2001;136(1):128-32.
68. Miller SM, Ngo TT. Studies of caloric vestibular stimulation: implications for the cognitive neuro¬sciences, the clinical neurosciences and neurophi¬losophy. Acta Neuropsychiatr. 2007;19(3):183-203. doi: 10.1111/j.1601-5215.2007.00208.x
69. Gopinath A, Archana R, Sailesh KS, Mukkadan JK. Effect of caloric vestibular stimulation on memory. Int J Pharm Bio Sci. 2015;6(3):(B)453-59.
70. Deroualle D, Lopez C. Toward a vestibular contribution to social cognition. Front Integr Neurosci. 2014;8:16. doi: 10.3389/fnint.2014.00016
71. Blanke O, Mohr C, Michel CM, Pascual-Leone A, Brugger P, Seeck M, et al. Linking out-of-body experience and self processing to mental own-body imagery at the temporoparietal junction. J Neurosci. 2005;25(3):550-7. doi: 10.1523/JNEUROSCI.2612-04.2005
72. Smith PF. Dyscalculia and vestibular function. Med Hypotheses. 2012;79(4):493-6. doi: 10.1016/j.mehy.2012.06.032
73. Redfern MS, Müller ML, Jennings JR, Furman JM. Attentional dynamics in postural control during perturbations in young and older adults. J Gerontol A Biol Sci Med Sci. 2002;57(8):B298-303.
74. Yardley L, Papo D, Bronstein A, Gresty M, Gardner M, Lavie N, et al. Attentional demands of continuously monitoring orientation using vestibular information. Neuropsychologia. 2002;40(4):373-83. doi: 10.1016/S0028-3932(01)00113-0
75. Smith PF. Is hippocampal neurogenesis modulated by the sensation of self-motion encoded by the vestibular system? Neurosci Biobehav Rev. 2017;83:489-495. doi: 10.1016/j.neubiorev.2017.09.013
76. Rogge AK, Röder B, Zech A, Nagel V, Hollander K, Braumann KM, et al. Balance training improves memory and spatial cognition in healthy adults. Sci Rep. 2017;7(1):5661. doi: 10.1038/s41598-017-06071-9
77. Hindin SB, Zelinski EM. Extended practice and aerobic exercise interventions benefit untrained cognitive outcomes in older adults: a meta-analysis. J Am Geriatr Soc. 2012;60(1):136-41. doi: 10.1111/j.1532-5415.2011.03761.x
78. Rovio S, Kåreholt I, Helkala EL, Viitanen M, Winblad B, Tuomilehto J, et al. Leisure-time physical activity at midlife and the risk of dementia and Alzheimer's disease. Lancet Neurol. 2005;4(11):705-11. doi: 10.1016/S1474-4422(05)70198-8
79. Delp MD, Armstrong RB, Godfrey DA, Laughlin MH, Ross CD, Wilkerson MK. Exercise increases blood flow to locomotor, vestibular, cardiorespiratory and visual regions of the brain in miniature swine. J Physiol. 2001;533(Pt 3):849-59.
80. Gauchard GC, Gangloff P, Jeandel C, Perrin PP. Physical activity improves gaze and posture control in the elderly. Neurosci Res. 2003;45(4):409-17. doi: 10.1016/S0168-0102(03)00008-7
81. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory. Proceedings of the National Academy of Sciences. 2011;108(7):3017-22. doi: 10.1073/pnas.1015950108
82. Lahmann C, Henningsen P, Brandt T, Strupp M, Jahn K, Dieterich M, et al. Psychiatric comorbidity and psychosocial impairment among patients with vertigo and dizziness. J Neurol Neurosurg Psychiatry. 2015;86(3):302-8. doi: 10.1136/jnnp-2014-307601
83. Balaban CD, Thayer JF. Neurological bases for balance-anxiety links. Journal of anxiety disorders. 2001;15(1-2):53-79. doi: 10.1016/S0887-6185(00)00042-6
84. Eagger S, Luxon LM, Davies RA, Coelho A, Ron MA. Psychiatric morbidity in patients with peripheral vestibular disorder: a clinical and neuro-otological study. J Neurol Neurosurg Psychiatry. 1992;55(5):383-7.
85. Hariri AR, Goldberg TE, Mattay VS, Kolachana BS, Callicott JH, Egan MF, et al. Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J Neurosci. 2003;23(17):6690-4.
86. Herrero AI, Sandi C, Venero C. Individual differences in anxiety trait are related to spatial learning abilities and hippocampal expression of mineralocorticoid receptors. Neurobiol Learn Mem. 2006;86(2):150-9. doi: 10.1016/j.nlm.2006.02.001
87. Mathews A, May J, Mogg K, Eysenck M. Attentional bias in anxiety: selective search or defective filtering? J Abnorm Psychol. 1990;99(2):166-73. doi: 10.1037/0021-843X.99.2.166
88. Millan MJ, Agid Y, Brüne M, Bullmore ET, Carter CS, Clayton NS, et al. Cognitive dysfunction in psychiatric disorders: characteristics, causes and the quest for improved therapy. Nat Rev Drug Discov. 2012;11(2):141-68. doi: 10.1038/nrd3628
89. Preuss N, Hasler G, Mast FW. Caloric vestibular stimulation modulates affective control and mood. Brain Stimul. 2014;7(1):133-40. doi: 10.1016/j.brs.2013.09.003
90. Büttner-Ennever JA. A review of otolith pathways to brainstem and cerebellum. Ann N Y Acad Sci. 1999;871:51-64.
91. Baier B, Karnath HO, Dieterich M, Birklein F, Heinze C. Keeping memory clear and stable--the contribution of human basal ganglia and prefrontal cortex to working memory. J Neurosci. 2010;30(29):9788-92. doi: 10.1523/JNEUROSCI.1513-10.2010
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IssueVol 28 No 2 (2019) QRcode
SectionReview Article(s)
DOI https://doi.org/10.18502/avr.v28i2.860
Keywords
Vestibular system; vestibular cortex; cognitive function; memory

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Moossavi A, Jafari M. Vestibular contribution to memory processing. Aud Vestib Res. 2019;28(2):62-74.