A Review on the Measures of Auditory Cognition in Individuals with Vestibular Disorders
,
Abstract
Background and Aim: The vestibular system, which involves the peripheral vestibular apparatus and central vestibular pathways, is crucial for balance and posture. In addition to its primary functions, the vestibular system is closely linked with cognitive processes, as evidenced by its connections with the neocortex and limbic system. Vestibular dysfunction has been associated with cognitive impairments, particularly in areas of auditory cognition, where allocating cognitive resources for balance maintenance detracts from higher cognitive functions. This review examines the existing literature on the auditory-cognitive consequences of vestibular dysfunction.
Recent finding: This systematic review gives comprehensive information about the existing research on the impact of vestibular pathology on auditory cognitive abilities. Following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, 226 articles were initially identified, with six studies meeting the inclusion criteria after thorough screening. The review highlights the varied effects of vestibular dysfunction on auditory cognition, revealing significant impairments in auditory working memory and attention, particularly in conditions like bilateral vestibulopathy and vestibular migraine. However, inconsistencies in the literature regarding specific vestibular pathologies and their impact on auditory cognition underscore the need for further targeted research.
Conclusions: The findings suggest a complex interplay between vestibular function and auditory cognition, with implications for the diagnosis and management of cognitive deficits in individuals with vestibular disorders.
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2. Tamura R, Ono T, Fukuda M, Nakamura K. Recognition of egocentric and allocentric visual and auditory space by neurons in the hippocampus of monkeys. Neurosci Lett. 1990;109(3):293-8. [DOI:10.1016/0304-3940(90)90010-7]
3. Andersen RA. Encoding of intention and spatial location in the posterior parietal cortex. Cereb Cortex. 1995;5(5):457-69. [DOI:10.1093/cercor/5.5.457]
4. Chaudhary S, Saywell N, Taylor D. The Differentiation of Self-Motion From External Motion Is a Prerequisite for Postural Control: A Narrative Review of Visual-Vestibular Interaction. Front Hum Neurosci. 2022;16:697739. [DOI:10.3389/fnhum.2022.697739]
5. Berthoz A. How does the cerebral cortex process and utilize vestibular signals? In: Balow RW, Halmagyi GM, editors. Disorders of the vestibular system. New York: Oxford University Press; 1996. p. 113-25.
6. Fukushima K. Corticovestibular interactions: anatomy, electrophysiology, and functional considerations. Exp Brain Res. 1997;117(1):1-16. [DOI:10.1007/pl00005786]
7. Smith PF. Vestibular-hippocampal interactions. Hippocampus. 1997;7(5):465-71. [DOI:10.1002/(SICI)1098-1063(1997)7:5<465::AID-HIPO3>3.0.CO;2-G]
8. Wiener S, Berthoz A. Forebrain structures mediating the vestibular contribution during navigation. In: Berthoz A, editor. Multisensory Control of Movement [Internet]. Oxford University Press; 1993 [cited 2023 Dec 26]. p. 0. Available from: https://doi.org/10.1093/acprof:oso/9780198547853.003.0208
9. Surgent OJ, Dadalko OI, Pickett KA, Travers BG. Balance and the brain: A review of structural brain correlates of postural balance and balance training in humans. Gait Posture. 2019;71:245-52. [DOI:10.1016/j.gaitpost.2019.05.011]
10. Paus T. Functional anatomy of arousal and attention systems in the human brain. Prog Brain Res. 2000;126:65-77. [DOI:10.1016/S0079-6123(00)26007-X]
11. Bosmans J, Gommeren H, Gilles A, Mertens G, Van Ombergen A, Cras P, et al. Evidence of Vestibular and Balance Dysfunction in Patients With Mild Cognitive Impairment and Alzheimer's Disease. Ear Hear. 2024;45(1):53-61. [DOI:10.1097/AUD.0000000000001401]
12. 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]
13. Lee HW, Lim YH, Kim SH. Dizziness in patients with cognitive impairment. J Vestib Res. 2020;30(1):17-23. [DOI:10.3233/VES-190686]
14. 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]
15. 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]
16. 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]
17. Danneels M, Van Hecke R, Leyssens L, van de Berg R, Dhooge I, Cambier D, et al. The impact of vestibular function on cognitive-motor interference: a case-control study on dual-tasking in persons with bilateral vestibulopathy and normal hearing. Sci Rep. 2023;13(1):13772. [DOI:10.1038/s41598-023-40465-2]
18. Kim SY, Yoo DM, Min C, Choi HG. Increased Risk of Neurodegenerative Dementia after Benign Paroxysmal Positional Vertigo. Int J Environ Res Public Health. 2021;18(19):10553. [DOI:10.3390/ijerph181910553]
19. Lacroix E, Deggouj N, Edwards MG, Van Cutsem J, Van Puyvelde M, Pattyn N. The Cognitive-Vestibular Compensation Hypothesis: How Cognitive Impairments Might Be the Cost of Coping With Compensation. Front Hum Neurosci. 2021;15:732974. [DOI:10.3389/fnhum.2021.732974]
20. 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):554-63. [DOI:10.1007/s00415-016-8386-7]
21. Smith PF, Zheng Y, Horii A, Darlington CL. Does vestibular damage cause cognitive dysfunction in humans? J Vestib Res. 2005;15(1):1-9. [DOI:10.3233/VES-2005-15101]
22. Egeth H. Attention and Effort by Daniel Kahneman. Am J Psychol. 1975;88(2):339-40. [DOI:10.2307/1421603]
23. Chari DA, Madhani A, Sharon JD, Lewis RF. Evidence for cognitive impairment in patients with vestibular disorders. J Neurol. 2022;269(11):5831-42. [DOI:10.1007/s00415-022-11289-3]
24. Djian C, Champion K, Lai N, Drouet L, Amador Borrero B, Depond A, et al. Infliximab for the Treatment of Inflammatory Labyrinthitis: A Retrospective Cohort Study. J Clin Med. 2023;12(13):4350. [DOI:10.3390/jcm12134350]
25. Lopez-Escamez JA, Carey J, Chung WH, Goebel JA, Magnusson M, Mandalà M, et al. Diagnostic criteria for Menière's disease. J Vestib Res. 2015;25(1):1-7. [DOI:10.3233/VES-150549]
26. Michalik D. Vestibular schwannoma. InnovAiT. 2022;16(1):34-8. [DOI:10.1177/17557380221135038]
27. Ahn JH, Oh SH, Jang H, Lee JB, Chung JW. Impact of hearing loss on the performance of auditory processing measured by questionnaires in Korean adolescents. Sci Rep. 2020;10(1):10118. [DOI:10.1038/s41598-020-67033-2]
28. Wayne RV, Johnsrude IS. A review of causal mechanisms underlying the link between age-related hearing loss and cognitive decline. Ageing Res Rev. 2015;23(Pt B):154-66. [DOI:10.1016/j.arr.2015.06.002]
29. Tawfik S, Amin R, Ibrahim S, Abdel Rahman TT. Deficits in central auditory processing among migraine patients. Egypt J Otolaryngol. 2021;37:121. [DOI:10.1186/s43163-021-00170-1]
30. Lempert T, Olesen J, Furman J, Seemungal B, Carey J, Bisdorff A, et al. Vestibular migraine: Diagnostic criteria (Update)1: Literature update 2021. J Vestib Res. 2021;32(1):1-6. [DOI:10.3233/VES-201644]
31. von Brevern M, Bertholon P, Brandt T, Fife T, Imai T, Nuti D, et al. Benign paroxysmal positional vertigo: Diagnostic criteria. J Vestib Res. 2015;25(3-4):105-17. [DOI:10.3233/VES-150553]
32. Gates GA, Beiser A, Rees TS, D'Agostino RB, Wolf PA. Central auditory dysfunction may precede the onset of clinical dementia in people with probable Alzheimer's disease. J Am Geriatr Soc. 2002;50(3):482-8. [DOI:10.1046/j.1532-5415.2002.50114.x]
33. Gates GA, Anderson ML, Feeney MP, McCurry SM, Larson EB. Central auditory dysfunction in older persons with memory impairment or Alzheimer dementia. Arch Otolaryngol Head Neck Surg. 2008;134(7):771-7. [DOI:10.1001/archotol.134.7.771]
34. Gates GA, Gibbons LE, McCurry SM, Crane PK, Feeney MP, Larson EB. Executive dysfunction and presbycusis in older persons with and without memory loss and dementia. Cogn Behav Neurol. 2010;23(4):218-23. [DOI:10.1097/WNN.0b013e3181d748d7]
35. Gold M, Lightfoot LA, Hnath-Chisolm T. Hearing loss in a memory disorders clinic. A specially vulnerable population. Arch Neurol. 1996 Sep;53(9):922-8. [DOI:10.1001/archneur.1996.00550090134019]
36. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097. [DOI:10.1371/journal.pmed.1000097]
37. Ma X, Shen J, Sun J, Wang L, Wang W, He K, et al. P300 Event-Related Potential Predicts Cognitive Dysfunction in Patients with Vestibular Disorders. Biomedicines. 2023;11(9):2365. [DOI:10.3390/biomedicines11092365]
38. Kumar K, S K, Ebenezer A, Kalaiah MK, D D. Cortical auditory potentials and cognitive potentials in individuals with and without vestibular dysfunction. F1000Res. 2023;11:1013. [DOI:10.12688/f1000research.122677.2]
39. Ahmad M, Bola L, Boutabla A, King S, Lewis RF, Chari DA. Visuospatial Cognitive Dysfunction in Patients with Vestibular Loss. Otol Neurotol. 2022;43(10):e1140-e7. [DOI:10.1097/MAO.0000000000003696]
40. 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]
41. 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.
42. Guidetti G, Guidetti R, Manfredi M, Manfredi M. Vestibular pathology and spatial working memory. Acta Otorhinolaryngol Ital. 2020;40(1):72-8.
43. Ayar DA, Kumral E, Celebisoy N. Cognitive functions in acute unilateral vestibular loss. J Neurol. 2020;267(Suppl 1):153-9. [DOI:10.1007/s00415-020-09829-w]
44. Yavas E, Gonzalez S, Fanselow MS. Interactions between the hippocampus, prefrontal cortex, and amygdala support complex learning and memory. F1000Res. 2019;8:F1000 Faculty Rev-1292. [DOI:10.12688/f1000research.19317.1]
2. Tamura R, Ono T, Fukuda M, Nakamura K. Recognition of egocentric and allocentric visual and auditory space by neurons in the hippocampus of monkeys. Neurosci Lett. 1990;109(3):293-8. [DOI:10.1016/0304-3940(90)90010-7]
3. Andersen RA. Encoding of intention and spatial location in the posterior parietal cortex. Cereb Cortex. 1995;5(5):457-69. [DOI:10.1093/cercor/5.5.457]
4. Chaudhary S, Saywell N, Taylor D. The Differentiation of Self-Motion From External Motion Is a Prerequisite for Postural Control: A Narrative Review of Visual-Vestibular Interaction. Front Hum Neurosci. 2022;16:697739. [DOI:10.3389/fnhum.2022.697739]
5. Berthoz A. How does the cerebral cortex process and utilize vestibular signals? In: Balow RW, Halmagyi GM, editors. Disorders of the vestibular system. New York: Oxford University Press; 1996. p. 113-25.
6. Fukushima K. Corticovestibular interactions: anatomy, electrophysiology, and functional considerations. Exp Brain Res. 1997;117(1):1-16. [DOI:10.1007/pl00005786]
7. Smith PF. Vestibular-hippocampal interactions. Hippocampus. 1997;7(5):465-71. [DOI:10.1002/(SICI)1098-1063(1997)7:5<465::AID-HIPO3>3.0.CO;2-G]
8. Wiener S, Berthoz A. Forebrain structures mediating the vestibular contribution during navigation. In: Berthoz A, editor. Multisensory Control of Movement [Internet]. Oxford University Press; 1993 [cited 2023 Dec 26]. p. 0. Available from: https://doi.org/10.1093/acprof:oso/9780198547853.003.0208
9. Surgent OJ, Dadalko OI, Pickett KA, Travers BG. Balance and the brain: A review of structural brain correlates of postural balance and balance training in humans. Gait Posture. 2019;71:245-52. [DOI:10.1016/j.gaitpost.2019.05.011]
10. Paus T. Functional anatomy of arousal and attention systems in the human brain. Prog Brain Res. 2000;126:65-77. [DOI:10.1016/S0079-6123(00)26007-X]
11. Bosmans J, Gommeren H, Gilles A, Mertens G, Van Ombergen A, Cras P, et al. Evidence of Vestibular and Balance Dysfunction in Patients With Mild Cognitive Impairment and Alzheimer's Disease. Ear Hear. 2024;45(1):53-61. [DOI:10.1097/AUD.0000000000001401]
12. 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]
13. Lee HW, Lim YH, Kim SH. Dizziness in patients with cognitive impairment. J Vestib Res. 2020;30(1):17-23. [DOI:10.3233/VES-190686]
14. 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]
15. 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]
16. 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]
17. Danneels M, Van Hecke R, Leyssens L, van de Berg R, Dhooge I, Cambier D, et al. The impact of vestibular function on cognitive-motor interference: a case-control study on dual-tasking in persons with bilateral vestibulopathy and normal hearing. Sci Rep. 2023;13(1):13772. [DOI:10.1038/s41598-023-40465-2]
18. Kim SY, Yoo DM, Min C, Choi HG. Increased Risk of Neurodegenerative Dementia after Benign Paroxysmal Positional Vertigo. Int J Environ Res Public Health. 2021;18(19):10553. [DOI:10.3390/ijerph181910553]
19. Lacroix E, Deggouj N, Edwards MG, Van Cutsem J, Van Puyvelde M, Pattyn N. The Cognitive-Vestibular Compensation Hypothesis: How Cognitive Impairments Might Be the Cost of Coping With Compensation. Front Hum Neurosci. 2021;15:732974. [DOI:10.3389/fnhum.2021.732974]
20. 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):554-63. [DOI:10.1007/s00415-016-8386-7]
21. Smith PF, Zheng Y, Horii A, Darlington CL. Does vestibular damage cause cognitive dysfunction in humans? J Vestib Res. 2005;15(1):1-9. [DOI:10.3233/VES-2005-15101]
22. Egeth H. Attention and Effort by Daniel Kahneman. Am J Psychol. 1975;88(2):339-40. [DOI:10.2307/1421603]
23. Chari DA, Madhani A, Sharon JD, Lewis RF. Evidence for cognitive impairment in patients with vestibular disorders. J Neurol. 2022;269(11):5831-42. [DOI:10.1007/s00415-022-11289-3]
24. Djian C, Champion K, Lai N, Drouet L, Amador Borrero B, Depond A, et al. Infliximab for the Treatment of Inflammatory Labyrinthitis: A Retrospective Cohort Study. J Clin Med. 2023;12(13):4350. [DOI:10.3390/jcm12134350]
25. Lopez-Escamez JA, Carey J, Chung WH, Goebel JA, Magnusson M, Mandalà M, et al. Diagnostic criteria for Menière's disease. J Vestib Res. 2015;25(1):1-7. [DOI:10.3233/VES-150549]
26. Michalik D. Vestibular schwannoma. InnovAiT. 2022;16(1):34-8. [DOI:10.1177/17557380221135038]
27. Ahn JH, Oh SH, Jang H, Lee JB, Chung JW. Impact of hearing loss on the performance of auditory processing measured by questionnaires in Korean adolescents. Sci Rep. 2020;10(1):10118. [DOI:10.1038/s41598-020-67033-2]
28. Wayne RV, Johnsrude IS. A review of causal mechanisms underlying the link between age-related hearing loss and cognitive decline. Ageing Res Rev. 2015;23(Pt B):154-66. [DOI:10.1016/j.arr.2015.06.002]
29. Tawfik S, Amin R, Ibrahim S, Abdel Rahman TT. Deficits in central auditory processing among migraine patients. Egypt J Otolaryngol. 2021;37:121. [DOI:10.1186/s43163-021-00170-1]
30. Lempert T, Olesen J, Furman J, Seemungal B, Carey J, Bisdorff A, et al. Vestibular migraine: Diagnostic criteria (Update)1: Literature update 2021. J Vestib Res. 2021;32(1):1-6. [DOI:10.3233/VES-201644]
31. von Brevern M, Bertholon P, Brandt T, Fife T, Imai T, Nuti D, et al. Benign paroxysmal positional vertigo: Diagnostic criteria. J Vestib Res. 2015;25(3-4):105-17. [DOI:10.3233/VES-150553]
32. Gates GA, Beiser A, Rees TS, D'Agostino RB, Wolf PA. Central auditory dysfunction may precede the onset of clinical dementia in people with probable Alzheimer's disease. J Am Geriatr Soc. 2002;50(3):482-8. [DOI:10.1046/j.1532-5415.2002.50114.x]
33. Gates GA, Anderson ML, Feeney MP, McCurry SM, Larson EB. Central auditory dysfunction in older persons with memory impairment or Alzheimer dementia. Arch Otolaryngol Head Neck Surg. 2008;134(7):771-7. [DOI:10.1001/archotol.134.7.771]
34. Gates GA, Gibbons LE, McCurry SM, Crane PK, Feeney MP, Larson EB. Executive dysfunction and presbycusis in older persons with and without memory loss and dementia. Cogn Behav Neurol. 2010;23(4):218-23. [DOI:10.1097/WNN.0b013e3181d748d7]
35. Gold M, Lightfoot LA, Hnath-Chisolm T. Hearing loss in a memory disorders clinic. A specially vulnerable population. Arch Neurol. 1996 Sep;53(9):922-8. [DOI:10.1001/archneur.1996.00550090134019]
36. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097. [DOI:10.1371/journal.pmed.1000097]
37. Ma X, Shen J, Sun J, Wang L, Wang W, He K, et al. P300 Event-Related Potential Predicts Cognitive Dysfunction in Patients with Vestibular Disorders. Biomedicines. 2023;11(9):2365. [DOI:10.3390/biomedicines11092365]
38. Kumar K, S K, Ebenezer A, Kalaiah MK, D D. Cortical auditory potentials and cognitive potentials in individuals with and without vestibular dysfunction. F1000Res. 2023;11:1013. [DOI:10.12688/f1000research.122677.2]
39. Ahmad M, Bola L, Boutabla A, King S, Lewis RF, Chari DA. Visuospatial Cognitive Dysfunction in Patients with Vestibular Loss. Otol Neurotol. 2022;43(10):e1140-e7. [DOI:10.1097/MAO.0000000000003696]
40. 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]
41. 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.
42. Guidetti G, Guidetti R, Manfredi M, Manfredi M. Vestibular pathology and spatial working memory. Acta Otorhinolaryngol Ital. 2020;40(1):72-8.
43. Ayar DA, Kumral E, Celebisoy N. Cognitive functions in acute unilateral vestibular loss. J Neurol. 2020;267(Suppl 1):153-9. [DOI:10.1007/s00415-020-09829-w]
44. Yavas E, Gonzalez S, Fanselow MS. Interactions between the hippocampus, prefrontal cortex, and amygdala support complex learning and memory. F1000Res. 2019;8:F1000 Faculty Rev-1292. [DOI:10.12688/f1000research.19317.1]
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How to Cite
1.
Vinod V, Barman A. A Review on the Measures of Auditory Cognition in Individuals with Vestibular Disorders. Aud Vestib Res. 2025;.
