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Unilateral vestibular deafferentation impairs embodied spatial cognition

Journal of Neurology volume 266, pages 149–159 (2019)Cite this article

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.

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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’).

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Affiliations

  1. Laboratoire de Neurosciences Sensorielles et Cognitives-UMR 7260, Aix Marseille Univ, CNRS, FR3C - Case B, 3 Place Victor Hugo, 13331, Marseille Cedex 03, France

    Diane Deroualle, Liliane Borel, Brandon Tanguy & Christophe Lopez

  2. Department of Otorhinolaryngology, Head and Neck Surgery, Hôpital La Conception, APHM, Marseille, France

    Laurence Bernard-Demanze, Marion Montava & Jean-Pierre Lavieille

  3. Department of Otorhinolaryngology, Head and Neck Surgery, Ramsay Générale de Santé, Hôpital Privé Clairval, Marseille, France

    Arnaud Devèze

Authors
  1. Diane Deroualle
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  2. Liliane Borel
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  3. Brandon Tanguy
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  4. Laurence Bernard-Demanze
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  5. Arnaud Devèze
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  6. Marion Montava
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  7. Jean-Pierre Lavieille
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  8. Christophe Lopez
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Correspondence to Christophe Lopez.

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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.

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Deroualle, D., Borel, L., Tanguy, B. et al. Unilateral vestibular deafferentation impairs embodied spatial cognition. J Neurol 266, 149–159 (2019). https://doi.org/10.1007/s00415-019-09433-7

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  • DOI: https://doi.org/10.1007/s00415-019-09433-7

Keywords

  • Perspective taking
  • Vestibular system
  • Unilateral vestibular loss
  • Mental imagery
  • 3D object mental rotation