Abstract
A growing number of studies indicate that cognitive complaints are common in patients with peripheral vestibular disorders. A better understanding of how vestibular disorders influence cognition in these patients requires a clear delineation of the cognitive domains affected by vestibular disorders. Here, we compared the consequences of left and right vestibular neurectomy on third-person perspective taking—a visuo-spatial task requiring mainly own-body mental imagery, and on 3D objects mental rotation imagery—requiring object-based mental imagery, but no perspective taking. Patients tested 1 week after a unilateral vestibular neurectomy and a group of age- and gender-matched healthy participants played a virtual ball-tossing game from their own first-person perspective (1PP) and from the perspective of a distant avatar (third-person perspective, 3PP). Results showed larger response times in the patients with respect to their controls for the 3PP taking task, but not for the 1PP task and the 3D objects mental imagery. In addition, we found that only patients with left vestibular neurectomy presented altered 3PP taking abilities when compared to their controls. This study suggests that unilateral vestibular loss affects mainly own-body mental transformation and that only left vestibular loss seems to impair this cognitive process. Our study also brings further evidence that vestibular signals contribute to the sensorimotor bases of social cognition and strengthens the connections between the so far distinct fields of social neuroscience and human vestibular physiology.
Similar content being viewed by others
References
Smith PF (2017) The vestibular system and cognition. Curr Opin Neurol 30:84–89. https://doi.org/10.1097/WCO.0000000000000403
Bigelow RT, Agrawal Y (2015) Vestibular involvement in cognition: visuospatial ability, attention, executive function, and memory. J Vestib Res Equilib Orientat 25:73–89. https://doi.org/10.3233/VES-150544
Bigelow RT, Semenov YR, du Lac S et al (2016) Vestibular vertigo and comorbid cognitive and psychiatric impairment: the 2008 National Health Interview Survey. J Neurol Neurosurg Psychiatry 87:367–372. https://doi.org/10.1136/jnnp-2015-310319
Popp P, Wulff M, Finke K et al (2017) Cognitive deficits in patients with a chronic vestibular failure. J Neurol 264:554–563. https://doi.org/10.1007/s00415-016-8386-7
Péruch P, Borel L, Gaunet F et al (1999) Spatial performance of unilateral vestibular defective patients in nonvisual versus visual navigation. J Vestib Res 9:37–47
Brandt T, Schautzer F, Hamilton DA et al (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128:2732–2741
Allum JHJ, Langewitz W, Sleptsova M et al (2017) Mental body transformation deficits in patients with chronic balance disorders. J Vestib Res Equilib Orientat 27:113–125. https://doi.org/10.3233/VES-170613
Grabherr L, Cuffel C, Guyot JP, Mast FW (2011) Mental transformation abilities in patients with unilateral and bilateral vestibular loss. Exp Brain Res 209:205–214. https://doi.org/10.1007/s00221-011-2535-0
Péruch P, Lopez C, Redon C et al (2011) Vestibular information is necessary for maintaining metric properties of representational space: evidence from mental imagery. Neuropsychologia 49:3136–3144
Candidi M, Micarelli A, Viziano A et al (2013) Impaired mental rotation in benign paroxysmal positional vertigo and acute vestibular neuritis. Front Hum Neurosci 7:783. https://doi.org/10.3389/fnhum.2013.00783
Dieterich M, Bense S, Lutz S et al (2003) Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 13:994–1007
Dieterich M, Kirsch V, Brandt T (2017) Right-sided dominance of the bilateral vestibular system in the upper brainstem and thalamus. J Neurol 264:55–62. https://doi.org/10.1007/s00415-017-8453-8
Saj A, Honoré J, Bernard-Demanze L et al (2013) Where is straight ahead to a patient with unilateral vestibular loss? Cortex 49:1219–1228. https://doi.org/10.1016/j.cortex.2012.05.019
Hüfner K, Hamilton DA, Kalla R et al (2007) Spatial memory and hippocampal volume in humans with unilateral vestibular deafferentation. Hippocampus 17:471–485. https://doi.org/10.1002/hipo.20283
Kessler K, Thomson LA (2010) The embodied nature of spatial perspective taking: embodied transformation versus sensorimotor interference. Cognition 114:72–88. https://doi.org/10.1016/j.cognition.2009.08.015
Deroualle D, Borel L, Devèze A, Lopez C (2015) Changing perspective: the role of vestibular signals. Neuropsychologia 79(Part B):175–185. https://doi.org/10.1016/j.neuropsychologia.2015.08.022
David N, Bewernick BH, Cohen MX et al (2006) Neural representations of self versus other: visual-spatial perspective taking and agency in a virtual ball-tossing game. J Cogn Neurosci 18:898–910
Becker-Bense S, Dieterich M, Buchholz H-G et al (2014) The differential effects of acute right- vs. left-sided vestibular failure on brain metabolism. Brain Struct Funct 219:1355–1367. https://doi.org/10.1007/s00429-013-0573-z
Pavlidou A, Ferrè ER, Lopez C (2018) Vestibular stimulation makes people more egocentric. Cortex J Devoted Study Nerv Syst Behav 101:302–305. https://doi.org/10.1016/j.cortex.2017.12.005
Lopez C, Elzière M (2018) Out-of-body experience in vestibular disorders—a prospective study of 210 patients with dizziness. Cortex J Devoted Study Nerv Syst Behav 104:193–206. https://doi.org/10.1016/j.cortex.2017.05.026
Macauda G, Moisa M, Mast FW et al (2019) Shared neural mechanisms between imagined and perceived egocentric motion—a combined GVS and fMRI study. Cortex J Devoted Study Nerv Syst Behav 119:20–32. https://doi.org/10.1016/j.cortex.2019.04.004
Koos WT, Day JD, Matula C, Levy DI (1998) Neurotopographic considerations in the microsurgical treatment of small acoustic neurinomas. J Neurosurg 88:506–512. https://doi.org/10.3171/jns.1998.88.3.0506
Deroualle D, Lopez C (2014) Toward a vestibular contribution to social cognition. Front Integr Neurosci 8:16. https://doi.org/10.3389/fnint.2014.00016
Lenggenhager B, Lopez C, Blanke O (2008) Influence of galvanic vestibular stimulation on egocentric and object-based mental transformations. Exp Brain Res 184:211–221
Lopez C, Nakul E, Preuss N et al (2018) Distorted own-body representations in patients with dizziness and during caloric vestibular stimulation. J Neurol 265:86–94. https://doi.org/10.1007/s00415-018-8906-8
Toupet M, Van Nechel C, Bozorg Grayeli A (2014) Influence of body laterality on recovery from subjective visual vertical tilt after vestibular neuritis. Audiol Neurootol 19:248–255. https://doi.org/10.1159/000360266
Bigelow RT, Semenov YR, Trevino C et al (2015) Association between visuospatial ability and vestibular function in the Baltimore longitudinal study of aging. J Am Geriatr Soc 63:1837–1844. https://doi.org/10.1111/jgs.13609
Falconer CJ, Mast FW (2012) Balancing the mind: vestibular induced facilitation of egocentric mental transformations. Exp Psychol 59:332–339. https://doi.org/10.1027/1618-3169/a000161
Secora K, Emmorey K (2019) Social abilities and visual-spatial perspective-taking skill: deaf signers and hearing nonsigners. J Deaf Stud Deaf Educ. https://doi.org/10.1093/deafed/enz006
Stackman RW, Clark AS, Taube JS (2002) Hippocampal spatial representations require vestibular input. Hippocampus 12:291–303. https://doi.org/10.1002/hipo.1112
Acknowledgements
The research leading to these results has received funding from the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme (FP7/2007-2013) under REA Grant agreement number 333607 (‘BODILYSELF, vestibular and multisensory investigations of bodilyself-consciousness’).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
C. Lopez serves as an associate editor of Frontiers in Integrative Neuroscience and guest editor of Frontiers in Neurology.
Ethical standard
Ethical approvals have been obtained from the local ethics committees (Comité de Protection des Personnes Sud-Mediterranée II, 2011-A01221-40) and participants provided informed consent in accordance with the Declaration of Helsinki.
Additional information
This manuscript is part of a supplement sponsored by the German Federal Ministry of Education and Research within the funding initiative for integrated research and treatment centers.
Rights and permissions
About this article
Cite this article
Deroualle, D., Borel, L., Tanguy, B. et al. Unilateral vestibular deafferentation impairs embodied spatial cognition. J Neurol 266 (Suppl 1), 149–159 (2019). https://doi.org/10.1007/s00415-019-09433-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00415-019-09433-7