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Cognitive deficits in patients with a chronic vestibular failure

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Abstract

Behavioral studies in rodents and humans have demonstrated deficits of spatial memory and orientation in bilateral vestibular failure (BVF). Our aim was to explore the functional consequences of chronic vestibular failure on different cognitive domains including spatial as well as non-spatial cognitive abilities. Sixteen patients with a unilateral vestibular failure (UVF), 18 patients with a BVF, and 17 healthy controls (HC) participated in the study. To assess the cognitive domains of short-term memory, executive function, processing speed and visuospatial abilities the following tests were used: Theory of Visual Attention (TVA), TAP Alertness and Visual Scanning, the Stroop Color-Word, and the Corsi Block Tapping Test. The cognitive scores were correlated with the degree of vestibular dysfunction and the duration of the disease, respectively. Groups did not differ significantly in age, sex, or handedness. BVF patients were significantly impaired in all of the examined cognitive domains but not in all tests of the particular domain, whereas UVF patients exhibited significant impairments in their visuospatial abilities and in one of the two processing speed tasks when compared independently with HC. The degree of vestibular dysfunction significantly correlated with some of the cognitive scores. Neither the side of the lesion nor the duration of disease influenced cognitive performance. The results demonstrate that vestibular failure can lead to cognitive impairments beyond the spatial navigation deficits described earlier. These cognitive impairments are more significant in BVF patients, suggesting that the input from one labyrinth which is distributed into bilateral vestibular circuits is sufficient to maintain most of the cognitive functions. These results raise the question whether BVF patients may profit from specific cognitive training in addition to physiotherapy.

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References

  1. Smith PF, Zheng Y (2013) From ear to uncertainty: vestibular contributions to cognitive function. Front Integr Neurosci 7:84

    Article  PubMed  PubMed Central  Google Scholar 

  2. Besnard S, Lopez C, Brandt T et al (2015) The vestibular system in cognitive and memory processes in mammalians. Front Integr Neurosci 9:55

    Article  PubMed  PubMed Central  Google Scholar 

  3. Baek JH, Zheng Y, Darlington CL, Smith PF (2010) Evidence that spatial memory deficits following bilateral vestibular deafferentation in rats are probably permanent. Neurobiol Learn Mem 94(3):402–413

    Article  PubMed  Google Scholar 

  4. Besnard S, Machado ML, Vignaux G et al (2012) Influence of vestibular input on spatial and nonspatial memory and on hippocampal NMDA receptors. Hippocampus 22(4):814–826

    Article  CAS  PubMed  Google Scholar 

  5. Brandt T, Schautzer F, Hamilton DA et al (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128:2732–2741

    Article  PubMed  Google Scholar 

  6. Yardley L, Burgneay J, Nazareth I, Luxon L (1998) Neuro-otological and psychiatric abnormalities in a community sample of people with dizziness: a blind, controlled investigation. J Neurol Neurosurg Psychiatry 65(5):679–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Black FO, Pesznecker S, Stallings V (2004) Permanent gentamicin vestibulotoxicity. Otol Neurotol 25(4):559–569

    Article  PubMed  Google Scholar 

  8. Bigelow RT, Agrawal Y (2015) Vestibular involvement in cognition: visuospatial ability, attention, executive function, and memory. J Vestib Res 25(2):73–89

    PubMed  Google Scholar 

  9. Risey J, Briner W (1990) Dyscalculia in patients with vertigo. J Vestib Res 1(1):31–37

    PubMed  Google Scholar 

  10. Redfern MS, Talkowski ME, Jennings JR, Furman JM (2004) Cognitive influences in postural control of patients with unilateral vestibular loss. Gait Posture 19(2):105–114

    Article  PubMed  Google Scholar 

  11. Péruch P, Lopez C, Redon-Zouiteni C et al (2011) Vestibular information is necessary for maintaining metric properties of representational space: evidence from mental imagery. Neuropsychologia 49(11):3136–3144

    Article  PubMed  Google Scholar 

  12. Hüfner K, Hamilton DA, Kalla R et al (2007) Spatial memory and hippocampal volume in humans with unilateral vestibular deafferentation. Hippocampus 17(6):471–485

    Article  PubMed  Google Scholar 

  13. Kremmyda O, Huefner K, Flanagin VL et al (2016) Beyond dizziness: virtual navigation, spatial anxiety and hippocampal volume in bilateral vestibulopathy. Front Hum Neurosci 10:139. doi:10.3389/fnhum.2016.00139 (eCollection)

    Article  PubMed  PubMed Central  Google Scholar 

  14. Dieterich M, Bense S, Lutz S et al (2003) Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 13(9):994–1007

    Article  CAS  PubMed  Google Scholar 

  15. Bense S, Bartenstein P, Lutz S et al (1004) Three determinants of vestibular hemispheric dominance during caloric stimulation. Ann N Y Acad Sci 1:440–445

    Google Scholar 

  16. Zingler VC, Cnyrim C, Jahn K et al (2007) Causative factors and epidemiology of bilateral vestibulopathy in 255 patients. Ann Neurol 61(6):524–532

    Article  PubMed  Google Scholar 

  17. Zingler VC, Weintz E, Jahn K et al (2008) Follow-up of vestibular function in bilateral vestibulopathy. J Neurol Neurosurg Psychiatry 79:284–288

    Article  CAS  PubMed  Google Scholar 

  18. Jongkees LB, Maas JP, Philipzoon AJ (1962) Clinical nystagmography: a detailed study of electro-nystagmography in 341 patients with vertigo. Pract Otorhinolaryngol 24:65–93

    CAS  Google Scholar 

  19. Honrubia V (1994) Quantitative vestibular function tests and the clinical examination. In: Herdman SJ (ed) Vestibular rehabilitation. Davis, Philadelphia, pp 113–164

    Google Scholar 

  20. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  21. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198

    Article  CAS  PubMed  Google Scholar 

  22. Tschan R, Wiltink J, Best C et al (2008) Validation of the German version of the Vertigo Symptom Scale (VSS) in patients with organic or somatoform dizziness and healthy controls. J Neurol 255(8):1168–1175

    Article  CAS  PubMed  Google Scholar 

  23. Finke K, Bublak P, Krummenacher J et al (2005) Usability of a theory of visual attention (TVA) for parameter-based measurement of attention I: evidence from normal subjects. Int Neuropsychol Soc 11(7):832–842

    Google Scholar 

  24. Jensen AR, Rohwer WD Jr (1966) The Stroop color-word test: a review. Acta Psychol (Amst) 25(1):36–93

    Article  CAS  Google Scholar 

  25. Kessels RPC, van Zandvoort MJE, Postma A et al (2000) The Corsi Block-Tapping Task: standardization and normative data. Appl Neuropsychol 7(4):252–258

    Article  CAS  PubMed  Google Scholar 

  26. Glasauer S, Amorim MA, Viaud-Delmon I, Berthoz A (2002) Differential effects of labyrinthine dysfunction on distance and direction during blindfolded walking of a triangular path. Exp Brain Res 145(4):489–497

    Article  CAS  PubMed  Google Scholar 

  27. Péruch P, Borel L, Magnan J, Lacour M (2005) Direction and distance deficits in path integration after unilateral vestibular loss depend on task complexity. Cogn Brain Res 25(3):862–872

    Article  Google Scholar 

  28. Guidetti G, Monzani D, Trebbi M, Rovatti V (2008) Impaired navigational skills in patients with psychological distress and chronic peripheral vestibular hypofunction without vertigo. Acta Otorhinolaryngol Ital 28(1):21–25

    CAS  PubMed  PubMed Central  Google Scholar 

  29. zu Eulenburg P, Caspers S, Roski C, Eickhoff SB (2012) Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage 60(1):162–169

    Article  CAS  PubMed  Google Scholar 

  30. Mast FW, Preuss N, Hartmann M, Grabherr L (2014) Spatial cognition, body representation and affective processes: the role of vestibular information beyond ocular reflexes and control of posture. Front Integr Neurosci 8:44. doi:10.3389/fnint.2014.00044 (ECollection)

    Article  PubMed  PubMed Central  Google Scholar 

  31. Krall SC, Rottschy C, Oberwelland E et al (2015) The role of the right temporoparietal junction in attention and social interaction as revealed by ALE meta-analysis. Brain Struct Funct 220(2):587–604

    Article  CAS  PubMed  Google Scholar 

  32. Schultz H, Sommer T, Peters J (2012) Direct evidence for domain-sensitive functional subregions in human entorhinal cortex. J Neurosci 32(14):4716–4723

    Article  CAS  PubMed  Google Scholar 

  33. Dieterich M, Bauermann T, Best C et al (2007) Evidence for cortical visual substitution of chronic bilateral vestibular failure (an fMRI study). Brain 130:2108–2116

    Article  PubMed  Google Scholar 

  34. Becker-Bense S, Dieterich M, Buchholz HG et al (2014) The differential effects of acute right- vs. left-sided vestibular failure on brain metabolism. Brain Struct Funct 219(4):1355–1367

    Article  CAS  PubMed  Google Scholar 

  35. zu Eulenburg P, Stoeter P, Dieterich M (2010) Voxel-based morphometry depicts central compensation after vestibular neuritis. Ann Neurol 68(2):241–249

    Article  PubMed  Google Scholar 

  36. Zwergal A, Schlichtiger J, Xiong G et al (2014) Sequential [18F]FDG µPET whole-brain imaging of central vestibular compensation: a model of deafferentation-induced brain plasticity. Brain Struct Funct 221(1):159–170

    Article  PubMed  Google Scholar 

  37. Talkowski ME, Redfern MS, Jennings JR, Furman JM (2005) Cognitive requirements for vestibular and ocular motor processing in healthy adults and patients with unilateral vestibular lesions. J Cogn Neurosci 17(9):1432–1441

    Article  CAS  PubMed  Google Scholar 

  38. Grabherr L, Cuffel C, Guyot JP, Mast FW (2011) Mental transformation abilities in patients with unilateral and bilateral vestibular loss. Exp Brain Res 209(2):205–214

    Article  PubMed  Google Scholar 

  39. Kirsch V, Keeser D, Hergenroeder T et al (2016) Structural and functional connectivity mapping of the vestibular circuitry from human brainstem to cortex. Brain Struct Funct 221(3):1291–1308

    Article  CAS  PubMed  Google Scholar 

  40. Bigelow RT, Semenov YR, Trevino C, Ferrucci L, Resnick SM, Simonsick EM, Q-L Xue, Agrawal Y (2015) Association between visuospatial ability and vestibular function in the baltimore longitudinal study of aging. J Am Geriatr Soc 63(9):1837–1844

    Article  PubMed  PubMed Central  Google Scholar 

  41. Hüfner K, Stephan T, Hamilton DA et al (2009) Gray-matter atrophy after chronic complete unilateral vestibular deafferentation. Ann N Y Acad Sci 1164:383–385

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Neurology, Ludwig-Maximilians University, Klinikum Grosshadern, Marchioninistrasse 15, 81377, Munich, Germany

    Pauline Popp, Melanie Wulff, Maxine Rühl & Marianne Dieterich

  2. Graduate School of Systemic Neurosciences, Ludwig-Maximilians University, Munich, Germany

    Pauline Popp, Melanie Wulff, Kathrin Finke & Marianne Dieterich

  3. Department of Psychology, Ludwig-Maximilians University, Munich, Germany

    Kathrin Finke

  4. German Center for Vertigo and Balance Disorders, Ludwig-Maximilians University, Munich, Germany

    Maxine Rühl, Thomas Brandt & Marianne Dieterich

  5. Clinical Neuroscience, Ludwig-Maximilians University, Munich, Germany

    Thomas Brandt

  6. SyNergy, Munich Cluster of Systems Neurology, Munich, Germany

    Marianne Dieterich

Authors
  1. Pauline Popp
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  2. Melanie Wulff
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  3. Kathrin Finke
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  4. Maxine Rühl
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  5. Thomas Brandt
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  6. Marianne Dieterich
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Correspondence to Marianne Dieterich.

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Conflicts of interest

PP had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis and reports no disclosures. MW, KF, MR, TB, and MD report no disclosures.

Ethical statement

The study was approved by the local ethics committee of the Ludwig-Maximilians University, Munich. All subjects gave their informed written consent to participate in the study.

Funding

This work was supported by funds from the German Research Foundation (GRK Grant Code 1091. to PP, MW, MD), the German Federal Ministry of Education and Research (BMBF Grant Code 01 EO 0901 to MD, TB), the Hertie–Foundation (TB), and the German Foundation for Neurology (MD, MR). The funding sources played no role in the design and performance of the study; collection, management, analysis, and interpretation of the data; or preparation, review, or approval of the manuscript.

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Popp, P., Wulff, M., Finke, K. et al. Cognitive deficits in patients with a chronic vestibular failure. J Neurol 264, 554–563 (2017). https://doi.org/10.1007/s00415-016-8386-7

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  • DOI: https://doi.org/10.1007/s00415-016-8386-7

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