Skip to main content
Top
Published in: Journal of Neurology 3/2017

01-03-2017 | Original Communication

Cognitive deficits in patients with a chronic vestibular failure

Authors: Pauline Popp, Melanie Wulff, Kathrin Finke, Maxine Rühl, Thomas Brandt, Marianne Dieterich

Published in: Journal of Neurology | Issue 3/2017

Login to get access

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.
Literature
3.
go back to reference 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):402–413CrossRefPubMed 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):402–413CrossRefPubMed
4.
go back to reference 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):814–826CrossRefPubMed 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):814–826CrossRefPubMed
5.
go back to reference Brandt T, Schautzer F, Hamilton DA et al (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128:2732–2741CrossRefPubMed Brandt T, Schautzer F, Hamilton DA et al (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128:2732–2741CrossRefPubMed
6.
go back to reference 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):679–684CrossRefPubMedPubMedCentral 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):679–684CrossRefPubMedPubMedCentral
7.
go back to reference Black FO, Pesznecker S, Stallings V (2004) Permanent gentamicin vestibulotoxicity. Otol Neurotol 25(4):559–569CrossRefPubMed Black FO, Pesznecker S, Stallings V (2004) Permanent gentamicin vestibulotoxicity. Otol Neurotol 25(4):559–569CrossRefPubMed
8.
go back to reference Bigelow RT, Agrawal Y (2015) Vestibular involvement in cognition: visuospatial ability, attention, executive function, and memory. J Vestib Res 25(2):73–89PubMed Bigelow RT, Agrawal Y (2015) Vestibular involvement in cognition: visuospatial ability, attention, executive function, and memory. J Vestib Res 25(2):73–89PubMed
9.
go back to reference Risey J, Briner W (1990) Dyscalculia in patients with vertigo. J Vestib Res 1(1):31–37PubMed Risey J, Briner W (1990) Dyscalculia in patients with vertigo. J Vestib Res 1(1):31–37PubMed
10.
go back to reference Redfern MS, Talkowski ME, Jennings JR, Furman JM (2004) Cognitive influences in postural control of patients with unilateral vestibular loss. Gait Posture 19(2):105–114CrossRefPubMed Redfern MS, Talkowski ME, Jennings JR, Furman JM (2004) Cognitive influences in postural control of patients with unilateral vestibular loss. Gait Posture 19(2):105–114CrossRefPubMed
11.
go back to reference 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):3136–3144CrossRefPubMed 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):3136–3144CrossRefPubMed
12.
go back to reference Hüfner K, Hamilton DA, Kalla R et al (2007) Spatial memory and hippocampal volume in humans with unilateral vestibular deafferentation. Hippocampus 17(6):471–485CrossRefPubMed Hüfner K, Hamilton DA, Kalla R et al (2007) Spatial memory and hippocampal volume in humans with unilateral vestibular deafferentation. Hippocampus 17(6):471–485CrossRefPubMed
14.
go back to reference Dieterich M, Bense S, Lutz S et al (2003) Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 13(9):994–1007CrossRefPubMed Dieterich M, Bense S, Lutz S et al (2003) Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 13(9):994–1007CrossRefPubMed
15.
go back to reference 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 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
16.
go back to reference Zingler VC, Cnyrim C, Jahn K et al (2007) Causative factors and epidemiology of bilateral vestibulopathy in 255 patients. Ann Neurol 61(6):524–532CrossRefPubMed Zingler VC, Cnyrim C, Jahn K et al (2007) Causative factors and epidemiology of bilateral vestibulopathy in 255 patients. Ann Neurol 61(6):524–532CrossRefPubMed
17.
go back to reference Zingler VC, Weintz E, Jahn K et al (2008) Follow-up of vestibular function in bilateral vestibulopathy. J Neurol Neurosurg Psychiatry 79:284–288CrossRefPubMed Zingler VC, Weintz E, Jahn K et al (2008) Follow-up of vestibular function in bilateral vestibulopathy. J Neurol Neurosurg Psychiatry 79:284–288CrossRefPubMed
18.
go back to reference 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 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
19.
go back to reference Honrubia V (1994) Quantitative vestibular function tests and the clinical examination. In: Herdman SJ (ed) Vestibular rehabilitation. Davis, Philadelphia, pp 113–164 Honrubia V (1994) Quantitative vestibular function tests and the clinical examination. In: Herdman SJ (ed) Vestibular rehabilitation. Davis, Philadelphia, pp 113–164
20.
go back to reference Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMed Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMed
21.
go back to reference 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):189–198CrossRefPubMed 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):189–198CrossRefPubMed
22.
go back to reference 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):1168–1175CrossRefPubMed 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):1168–1175CrossRefPubMed
23.
go back to reference 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 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
24.
go back to reference Jensen AR, Rohwer WD Jr (1966) The Stroop color-word test: a review. Acta Psychol (Amst) 25(1):36–93CrossRef Jensen AR, Rohwer WD Jr (1966) The Stroop color-word test: a review. Acta Psychol (Amst) 25(1):36–93CrossRef
25.
go back to reference Kessels RPC, van Zandvoort MJE, Postma A et al (2000) The Corsi Block-Tapping Task: standardization and normative data. Appl Neuropsychol 7(4):252–258CrossRefPubMed Kessels RPC, van Zandvoort MJE, Postma A et al (2000) The Corsi Block-Tapping Task: standardization and normative data. Appl Neuropsychol 7(4):252–258CrossRefPubMed
26.
go back to reference 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):489–497CrossRefPubMed 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):489–497CrossRefPubMed
27.
go back to reference 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):862–872CrossRef 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):862–872CrossRef
28.
go back to reference 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):21–25PubMedPubMedCentral 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):21–25PubMedPubMedCentral
29.
go back to reference zu Eulenburg P, Caspers S, Roski C, Eickhoff SB (2012) Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage 60(1):162–169CrossRefPubMed zu Eulenburg P, Caspers S, Roski C, Eickhoff SB (2012) Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage 60(1):162–169CrossRefPubMed
31.
go back to reference 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):587–604CrossRefPubMed 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):587–604CrossRefPubMed
32.
go back to reference Schultz H, Sommer T, Peters J (2012) Direct evidence for domain-sensitive functional subregions in human entorhinal cortex. J Neurosci 32(14):4716–4723CrossRefPubMed Schultz H, Sommer T, Peters J (2012) Direct evidence for domain-sensitive functional subregions in human entorhinal cortex. J Neurosci 32(14):4716–4723CrossRefPubMed
33.
go back to reference Dieterich M, Bauermann T, Best C et al (2007) Evidence for cortical visual substitution of chronic bilateral vestibular failure (an fMRI study). Brain 130:2108–2116CrossRefPubMed Dieterich M, Bauermann T, Best C et al (2007) Evidence for cortical visual substitution of chronic bilateral vestibular failure (an fMRI study). Brain 130:2108–2116CrossRefPubMed
34.
go back to reference 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):1355–1367CrossRefPubMed 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):1355–1367CrossRefPubMed
35.
go back to reference zu Eulenburg P, Stoeter P, Dieterich M (2010) Voxel-based morphometry depicts central compensation after vestibular neuritis. Ann Neurol 68(2):241–249CrossRefPubMed zu Eulenburg P, Stoeter P, Dieterich M (2010) Voxel-based morphometry depicts central compensation after vestibular neuritis. Ann Neurol 68(2):241–249CrossRefPubMed
36.
go back to reference 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):159–170CrossRefPubMed 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):159–170CrossRefPubMed
37.
go back to reference 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):1432–1441CrossRefPubMed 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):1432–1441CrossRefPubMed
38.
go back to reference 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):205–214CrossRefPubMed 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):205–214CrossRefPubMed
39.
go back to reference 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):1291–1308CrossRefPubMed 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):1291–1308CrossRefPubMed
40.
go back to reference 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):1837–1844CrossRefPubMedPubMedCentral 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):1837–1844CrossRefPubMedPubMedCentral
41.
go back to reference Hüfner K, Stephan T, Hamilton DA et al (2009) Gray-matter atrophy after chronic complete unilateral vestibular deafferentation. Ann N Y Acad Sci 1164:383–385CrossRefPubMed Hüfner K, Stephan T, Hamilton DA et al (2009) Gray-matter atrophy after chronic complete unilateral vestibular deafferentation. Ann N Y Acad Sci 1164:383–385CrossRefPubMed
Metadata
Title
Cognitive deficits in patients with a chronic vestibular failure
Authors
Pauline Popp
Melanie Wulff
Kathrin Finke
Maxine Rühl
Thomas Brandt
Marianne Dieterich
Publication date
01-03-2017
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 3/2017
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-016-8386-7

Other articles of this Issue 3/2017

Journal of Neurology 3/2017 Go to the issue

Pioneers in Neurology

Edwin Bickerstaff (1920–2008)