Skip to main content
SpringerLink
Log in

Navigation strategies in patients with vestibular loss tested in a virtual reality T-maze

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

During navigation, humans mainly rely on egocentric and allocentric spatial strategies, two different frames of reference working together to build a coherent representation of the environment. Spatial memory deficits during navigation have been repeatedly reported in patients with vestibular disorders. However, little is known about how vestibular disorders can change the use of spatial navigation strategies. Here, we used a new reverse T-maze paradigm in virtual reality to explore whether vestibular loss specifically modifies the use of egocentric or allocentric spatial strategies in patients with unilateral (n = 23) and bilateral (n = 23) vestibular loss compared to healthy volunteers (n = 23) matched for age, sex and education level. Results showed that the odds of selecting and using a specific strategy in the T-maze were significantly reduced in both unilateral and bilateral vestibular loss. An exploratory analysis suggests that only right vestibular loss decreased the odds of adopting a spatial strategy, indicating an asymmetry of vestibular functions. When considering patients who used strategies to navigate, we observed that a bilateral vestibular loss reduced the odds to use an allocentric strategy, whereas a unilateral vestibular loss decreased the odds to use an egocentric strategy. Age was significantly associated with an overall lower chance to adopt a navigation strategy and, more specifically, with a decrease in the odds of using an allocentric strategy. We did not observe any sex difference in the ability to select and use a specific navigation strategy. Findings are discussed in light of previous studies on visuo-spatial abilities and studies of vestibulo-hippocampal interactions in peripheral vestibular disorders. We discuss the potential impact of the history of the disease (chronic stage in patients with a bilateral vestibulopathy vs. subacute stage in patients with a unilateral vestibular loss), of hearing impairment and non-specific attentional deficits in patients with vestibular disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Andersen NE, Dahmani L, Konishi K, Bohbot VD (2012) Eye tracking, strategies, and sex differences in virtual navigation. Neurobiol Learn Mem 97(1):81–89. https://doi.org/10.1016/j.nlm.2011.09.007

    Article  PubMed  Google Scholar 

  2. Angelaki DE, Cullen KE (2008) Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31(1):125–150. https://doi.org/10.1146/annurev.neuro.31.060407.125555

    Article  CAS  PubMed  Google Scholar 

  3. Anson E, Ehrenburg MR, Simonsick EM, Agrawal Y (2021) Association between vestibular function and rotational spatial orientation perception in older adults. J Vestib Res 31(6):469–478. https://doi.org/10.3233/VES-201582

    Article  CAS  PubMed  Google Scholar 

  4. Astur RS, Purton AJ, Zaniewski MJ, Cimadevilla J, Markus EJ (2016) Human sex differences in solving a virtual navigation problem. Behav Brain Res 308:236–243. https://doi.org/10.1016/j.bbr.2016.04.037

    Article  PubMed  Google Scholar 

  5. Ayar DA, Kumral E, Celebisoy N (2020) Cognitive functions in acute unilateral vestibular loss. J Neurol 267(S1):153–159. https://doi.org/10.1007/s00415-020-09829-w

    Article  PubMed  PubMed Central  Google Scholar 

  6. Baddeley A. D, Emslie H, Nimmo-Smith I. (2006). Doors and people: a test of visual and verbal recall and recognition. Harcourt Assessment.

  7. 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. https://doi.org/10.1016/j.nlm.2010.08.007

    Article  PubMed  Google Scholar 

  8. Bates SL, Wolbers T (2014) How cognitive aging affects multisensory integration of navigational cues. Neurobiol Aging 35(12):2761–2769. https://doi.org/10.1016/j.neurobiolaging.2014.04.003

    Article  PubMed  Google Scholar 

  9. Belrose JC, Noppens RR (2019) Anesthesiology and cognitive impairment: a narrative review of current clinical literature. BMC Anesthesiol 19(1):241. https://doi.org/10.1186/s12871-019-0903-7

    Article  PubMed  PubMed Central  Google Scholar 

  10. Besnard S, Machado ML, Vignaux G, Boulouard M, Coquerel A, Bouet V, Freret T, Denise P, Lelong-Boulouard V (2012) Influence of vestibular input on spatial and nonspatial memory and on hippocampal NMDA receptors. Hippocampus 22(4):814–826. https://doi.org/10.1002/hipo.20942

    Article  CAS  PubMed  Google Scholar 

  11. Bessot N, Denise P, Toupet M, Van Nechel C, Chavoix C (2012) Interference between walking and a cognitive task is increased in patients with bilateral vestibular loss. Gait Posture 36(2):319–321. https://doi.org/10.1016/j.gaitpost.2012.02.021

    Article  PubMed  Google Scholar 

  12. Bigelow RT, Semenov YR, du Lac S, Hoffman HJ, Agrawal Y (2016) Vestibular vertigo and comorbid cognitive and psychiatric impairment: the 2008 National Health Interview Survey. J Neurol Neurosurg Psychiatry 87(4):367–372. https://doi.org/10.1136/jnnp-2015-310319

    Article  PubMed  Google Scholar 

  13. Bohbot VD, McKenzie S, Konishi K, Fouquet C, Kurdi V, Schachar R, Boivin M, Robaey P (2012) Virtual navigation strategies from childhood to senescence: evidence for changes across the life span. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2012.00028

    Article  PubMed  PubMed Central  Google Scholar 

  14. Borel L, Lopez C, Péruch P, Lacour M (2008) Vestibular syndrome: a change in internal spatial representation. Neurophysiol Clin 38(6):375–389. https://doi.org/10.1016/j.neucli.2008.09.002

    Article  CAS  PubMed  Google Scholar 

  15. Bottini G, Karnath HO, Vallar G, Sterzi R, Frith CD, Frackowiak RS, Paulesu E (2001) Cerebral representations for egocentric space: functional-anatomical evidence from caloric vestibular stimulation and neck vibration. Brain 124:1182–1196

    Article  CAS  Google Scholar 

  16. Brandt T, Schautzer F, Hamilton DA, Brüning R, Markowitsch HJ, Kalla R, Darlington C, Smith P, Strupp M (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128(11):2732–2741. https://doi.org/10.1093/brain/awh617

    Article  PubMed  Google Scholar 

  17. Brandt T, Zwergal A, Glasauer S (2017) 3-D spatial memory and navigation: functions and disorders. Curr Opin Neurol 30(1):90–97. https://doi.org/10.1097/WCO.0000000000000415

    Article  PubMed  Google Scholar 

  18. Burgess N (2006) Spatial memory: how egocentric and allocentric combine. Trends Cogn Sci 10(12):551–557. https://doi.org/10.1016/j.tics.2006.10.005

    Article  PubMed  Google Scholar 

  19. Chen Y, Monaco S, Byrne P, Yan X, Henriques DYP, Crawford JD (2014) Allocentric versus egocentric representation of remembered reach targets in human cortex. J Neurosci 34(37):12515–12526. https://doi.org/10.1523/JNEUROSCI.1445-14.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58(3):306–324. https://doi.org/10.1016/j.neuron.2008.04.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Cutfield NJ, Scott G, Waldman AD, Sharp DJ, Bronstein AM (2014) Visual and proprioceptive interaction in patients with bilateral vestibular loss. NeuroImage Clinical 4:274–282. https://doi.org/10.1016/j.nicl.2013.12.013

    Article  PubMed  PubMed Central  Google Scholar 

  22. Deroualle D, Borel L, Tanguy B, Bernard-Demanze L, Devèze A, Montava M, Lavieille J-P, Lopez C (2019) Unilateral vestibular deafferentation impairs embodied spatial cognition. J Neurol 266(S1):149–159. https://doi.org/10.1007/s00415-019-09433-7

    Article  PubMed  Google Scholar 

  23. Deroualle D, Toupet M, van Nechel C, Duquesne U, Hautefort C, Lopez C (2017) Anchoring the self to the body in bilateral vestibular failure. PLoS ONE 12(1):e0170488. https://doi.org/10.1371/journal.pone.0170488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Devèze A, Montava M, Lopez C, Lacour M, Magnan J, Borel L (2015) Vestibular compensation following vestibular neurotomy. Eur Ann Otorhinolaryngol Head Neck Dis 132(4):197–203. https://doi.org/10.1016/j.anorl.2015.04.003

    Article  PubMed  Google Scholar 

  25. Dieterich M, Bense S, Lutz S, Drzezga A, Stephan T, Bartenstein P, Brandt T (2003) Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 13(9):994–1007. https://doi.org/10.1093/cercor/13.9.994

    Article  CAS  PubMed  Google Scholar 

  26. Dieterich M, Brandt T (2018) Global orientation in space and the lateralization of brain functions. Curr Opin Neurol 31(1):96–104. https://doi.org/10.1097/WCO.0000000000000516

    Article  PubMed  Google Scholar 

  27. Dieterich M, Kirsch V, Brandt T (2017) Right-sided dominance of the bilateral vestibular system in the upper brainstem and thalamus. J Neurol 264(Suppl 1):55–62. https://doi.org/10.1007/s00415-017-8453-8

    Article  PubMed  Google Scholar 

  28. Dobbels B, Mertens G, Gilles A, Claes A, Moyaert J, van de Berg R, Van de Heyning P, Vanderveken O, Van Rompaey V (2019) Cognitive function in acquired bilateral vestibulopathy: a cross-sectional study on cognition, hearing, and vestibular loss. Front Neurosci 13:340. https://doi.org/10.3389/fnins.2019.00340

    Article  PubMed  PubMed Central  Google Scholar 

  29. Dobbels B, Mertens G, Gilles A, Moyaert J, van de Berg R, Fransen E, Van de Heyning P, Van Rompaey V (2020) The virtual morris water task in 64 patients with bilateral vestibulopathy and the impact of hearing status. Front Neurol 11:710. https://doi.org/10.3389/fneur.2020.00710

    Article  PubMed  PubMed Central  Google Scholar 

  30. Fink GR, Marshall JC, Weiss PH, Stephan T, Grefkes C, Shah NJ, Zilles K, Dieterich M (2003) Performing allocentric visuospatial judgments with induced distortion of the egocentric reference frame: an fMRI study with clinical implications. Neuroimage 20:1505–1517

    Article  Google Scholar 

  31. 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 145:489–497. https://doi.org/10.1007/s00221-002-1146-1

    Article  CAS  PubMed  Google Scholar 

  32. Glasauer S, Amorim MA, Vitte E, Berthoz A (1994) Goal-directed linear locomotion in normal and labyrinthine-defective subjects. Exp Brain Res 98(2):323–335. https://doi.org/10.1007/BF00228420

    Article  CAS  PubMed  Google Scholar 

  33. Gliddon CM, Darlington CL, Smith PF (2004) Rapid vestibular compensation in guinea pig even with prolonged anesthesia. Neurosci Lett 371:138–141

    Article  CAS  Google Scholar 

  34. Göttlich M, Jandl NM, Sprenger A, Wojak JF, Münte TF, Krämer UM, Helmchen C (2016) Hippocampal gray matter volume in bilateral vestibular failure. Hum Brain Mapp 37(5):1998–2006. https://doi.org/10.1002/hbm.23152

    Article  PubMed  PubMed Central  Google Scholar 

  35. Gramann K, Onton J, Riccobon D, Mueller HJ, Bardins S, Makeig S (2010) Human brain dynamics accompanying use of egocentric and allocentric reference frames during navigation. J Cogn Neurosci 22(12):2836–2849. https://doi.org/10.1162/jocn.2009.21369

    Article  PubMed  PubMed Central  Google Scholar 

  36. Grön G, Wunderlich AP, Spitzer M, Tomczak R, Riepe MW (2000) Brain activation during human navigation: gender-different neural networks as substrate of performance. Nat Neurosci 3(4):404–408. https://doi.org/10.1038/73980

    Article  PubMed  Google Scholar 

  37. Guderian S, Dzieciol AM, Gadian DG, Jentschke S, Doeller CF, Burgess N, Mishkin M, Vargha-Khadem F (2015) Hippocampal volume reduction in humans predicts impaired allocentric spatial memory in virtual-reality navigation. J Neurosci 35(42):14123–14131. https://doi.org/10.1523/JNEUROSCI.0801-15.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Halmagyi GM, Weber KP, Curthoys IS (2010) Vestibular function after acute vestibular neuritis. Restor Neurol Neurosci 28(1):37–46. https://doi.org/10.3233/RNN-2010-0533

    Article  CAS  PubMed  Google Scholar 

  39. Hamann K-F, Weiss U, Ruile A (2009) Effects of acute vestibular lesions on visual orientation and spatial memory, shown for the visual straight ahead. Ann NY Acad Sci 1164(1):305–308. https://doi.org/10.1111/j.1749-6632.2009.03867.x

    Article  PubMed  Google Scholar 

  40. Harun A, Oh ES, Bigelow RT, Studenski S, Agrawal Y (2016) Vestibular Impairment in Dementia. Otol Neurotol 37(8):1137–1142. https://doi.org/10.1097/MAO.0000000000001157 (Official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology)

    Article  PubMed  PubMed Central  Google Scholar 

  41. Helmchen C, Ye Z, Sprenger A, Münte TF (2014) Changes in resting-state fMRI in vestibular neuritis. Brain Struct Funct 219(6):1889–1900. https://doi.org/10.1007/s00429-013-0608-5

    Article  PubMed  Google Scholar 

  42. Huffman DJ, Ekstrom AD (2019) A modality-independent network underlies the retrieval of large-scale spatial environments in the human brain. Neuron 104(3):611-622.e7. https://doi.org/10.1016/j.neuron.2019.08.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Hüfner K, Hamilton DA, Kalla R, Stephan T, Glasauer S, Ma J, Brüning R, Markowitsch HJ, Labudda K, Schichor C, Strupp M, Brandt T (2007) Spatial memory and hippocampal volume in humans with unilateral vestibular deafferentation. Hippocampus 17(6):471–485. https://doi.org/10.1002/hipo.20283

    Article  PubMed  Google Scholar 

  44. Hüfner K, Stephan T, Hamilton DA, Kalla R, Glasauer S, Strupp M, Brandt T (2009) Gray-matter atrophy after chronic complete unilateral vestibular deafferentation. Ann N Y Acad Sci 1164(1):383–385. https://doi.org/10.1111/j.1749-6632.2008.03719.x

    Article  PubMed  Google Scholar 

  45. Iglói K, Doeller CF, Paradis A-L, Benchenane K, Berthoz A, Burgess N, Rondi-Reig L (2015) Interaction between hippocampus and cerebellum Crus I in sequence-based but not place-based navigation. Cereb Cortex 25(11):4146–4154. https://doi.org/10.1093/cercor/bhu132 ((New York, N.Y.:1991))

    Article  PubMed  Google Scholar 

  46. Ionta S, Heydrich L, Lenggenhager B, Mouthon M, Fornari E, Chapuis D, Gassert R, Blanke O (2011) Multisensory mechanisms in temporo-parietal cortex support self-location and first-person perspective. Neuron 70:363–374. https://doi.org/10.1016/j.neuron.2011.03.009 (doi.org/S0896-6273(11)00200-5 [pii])

    Article  CAS  PubMed  Google Scholar 

  47. Irving S, Schöberl F, Pradhan C, Brendel M, Bartenstein P, Dieterich M, Brandt T, Zwergal A (2018) A novel real-space navigation paradigm reveals age- and gender-dependent changes of navigational strategies and hippocampal activation. J Neurol 265(S1):113–126. https://doi.org/10.1007/s00415-018-8987-4

    Article  PubMed  Google Scholar 

  48. Jacob A, Tward DJ, Resnick S, Smith PF, Lopez C, Rebello E, Wei EX, Tilak Ratnanather J, Agrawal Y (2020) Vestibular function and cortical and sub-cortical alterations in an aging population. Heliyon 6(8):e04728. https://doi.org/10.1016/j.heliyon.2020.e04728

    Article  PubMed  PubMed Central  Google Scholar 

  49. Jacob P-Y, Poucet B, Liberge M, Save E, Sargolini F (2014) Vestibular control of entorhinal cortex activity in spatial navigation. Front Integr Neurosci. https://doi.org/10.3389/fnint.2014.00038

    Article  PubMed  PubMed Central  Google Scholar 

  50. Jacobs J, Weidemann CT, Miller JF, Solway A, Burke JF, Wei X-X, Suthana N, Sperling MR, Sharan AD, Fried I, Kahana MJ (2013) Direct recordings of grid-like neuronal activity in human spatial navigation. Nat Neurosci 16(9):1188–1190. https://doi.org/10.1038/nn.3466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Jandl NM, Sprenger A, Wojak JF, Göttlich M, Münte TF, Krämer UM, Helmchen C (2015) Dissociable cerebellar activity during spatial navigation and visual memory in bilateral vestibular failure. Neuroscience 305:257–267. https://doi.org/10.1016/j.neuroscience.2015.07.089

    Article  CAS  PubMed  Google Scholar 

  52. Kamil RJ, Jacob A, Ratnanather JT, Resnick SM, Agrawal Y (2018) Vestibular function and hippocampal volume in the baltimore longitudinal study of aging (BLSA). Otol Neurotol 39(6):765–771. https://doi.org/10.1097/MAO.0000000000001838

    Article  PubMed  PubMed Central  Google Scholar 

  53. Karnath HO, Dieterich M (2006) Spatial neglect-a vestibular disorder? Brain 129:293–305

    Article  Google Scholar 

  54. Kremmyda O, Hüfner K, Flanagin VL, Hamilton DA, Linn J, Strupp M, Jahn K, Brandt T (2016) Beyond dizziness: virtual navigation, spatial anxiety and hippocampal volume in bilateral vestibulopathy. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2016.00139

    Article  PubMed  PubMed Central  Google Scholar 

  55. LaViola JJ (2000) A discussion of cybersickness in virtual environments. ACM SIGCHI Bulletin 32(1):47–56. https://doi.org/10.1145/333329.333344

    Article  Google Scholar 

  56. Lester AW, Moffat SD, Wiener JM, Barnes CA, Wolbers T (2017) The aging navigational system. Neuron 95(5):1019–1035. https://doi.org/10.1016/j.neuron.2017.06.037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Levy LJ, Astur RS, Frick KM (2005) Men and women differ in object memory but not performance of a virtual radial maze. Behav Neurosci 119(4):853–862. https://doi.org/10.1037/0735-7044.119.4.853

    Article  PubMed  Google Scholar 

  58. Li AWY, King J (2019) Spatial memory and navigation in ageing: a systematic review of MRI and fMRI studies in healthy participants. Neurosci Biobehav Rev 103:33–49. https://doi.org/10.1016/j.neubiorev.2019.05.005

    Article  PubMed  Google Scholar 

  59. Lindner A, Wiesen D, Karnath H-O (2021) Lying in a 3T MRI scanner induces neglect-like spatial attention bias. Elife 10:e71076. https://doi.org/10.7554/eLife.71076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Lopez C, Lacour M, Ahmadi AE, Magnan J, Borel L (2007) Changes of visual vertical perception: a long-term sign of unilateral and bilateral vestibular loss. Neuropsychologia 45:2025–2037

    Article  Google Scholar 

  61. Lopez C, Lacour M, Magnan J, Borel L (2006) Visual field dependence–independence before and after unilateral vestibular loss. NeuroReport 17(8):797–803. https://doi.org/10.1097/01.wnr.0000221843.58373.c8

    Article  PubMed  Google Scholar 

  62. Machado ML, Kroichvili N, Freret T, Philoxène B, Lelong-Boulouard V, Denise P, Besnard S (2012) Spatial and non-spatial performance in mutant mice devoid of otoliths. Neurosci Lett 522(1):57–61. https://doi.org/10.1016/j.neulet.2012.06.016

    Article  CAS  PubMed  Google Scholar 

  63. Machado ML, Lefèvre N, Philoxene B, Le Gall A, Madeleine S, Fleury P, Smith PF, Besnard S (2019) New software dedicated to virtual mazes for human cognitive investigations. J Neurosci Methods 327:108388. https://doi.org/10.1016/j.jneumeth.2019.108388

    Article  CAS  PubMed  Google Scholar 

  64. Machado M-L, Lelong-Boulouard V, Philoxene B, Davis A, Denise P, Besnard S (2014) Vestibular loss promotes procedural response during a spatial task in rats: procedural memory preference in vestibular-lesioned rat. Hippocampus 24(5):591–597. https://doi.org/10.1002/hipo.22251

    Article  PubMed  Google Scholar 

  65. Maguire EA (1998) Knowing where and getting there: a human navigation network. Science 280(5365):921–924. https://doi.org/10.1126/science.280.5365.921

    Article  CAS  PubMed  Google Scholar 

  66. Mashour GA, Palanca BJ, Basner M, Li D, Wang W, Blain-Moraes S, Lin N, Maier K, Muench M, Tarnal V, Vanini G, Ochroch EA, Hogg R, Schwartz M, Maybrier H, Hardie R, Janke E, Golmirzaie G, Picton P, Kelz MB (2021) Recovery of consciousness and cognition after general anesthesia in humans. Elife 10:e59525. https://doi.org/10.7554/eLife.59525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. McGarvie LA, MacDougall HG, Curthoys IS, Halmagyi GM (2020) Spontaneous recovery of the vestibulo-ocular reflex after vestibular neuritis; long-term monitoring with the video head impulse test in a single patient. Front Neurol 11:732. https://doi.org/10.3389/fneur.2020.00732

    Article  PubMed  PubMed Central  Google Scholar 

  68. McIntyre CK, Marriott LK, Gold PE (2003) Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats. Neurobiol Learn Mem 79(2):177–183. https://doi.org/10.1016/S1074-7427(02)00014-X

    Article  CAS  PubMed  Google Scholar 

  69. Mueller SC, Jackson CPT, Skelton RW (2008) Sex differences in a virtual water maze: an eye tracking and pupillometry study. Behav Brain Res 193(2):209–215. https://doi.org/10.1016/j.bbr.2008.05.017

    Article  PubMed  Google Scholar 

  70. Nakul E, Dabard C, Toupet M, Hautefort C, van Nechel C, Lenggenhager B, Lopez C (2020) Interoception and embodiment in patients with bilateral vestibulopathy. J Neurol 267(Suppl 1):109–117. https://doi.org/10.1007/s00415-020-10221-x

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  72. Pavlidou A, Ferrè ER, Lopez C (2018) Vestibular stimulation makes people more egocentric. Cortex. https://doi.org/10.1016/j.cortex.2017.12.005

    Article  PubMed  Google Scholar 

  73. Peirce J, Gray JR, Simpson S, MacAskill M, Höchenberger R, Sogo H, Kastman E, Lindeløv JK (2019) PsychoPy2: experiments in behavior made easy. Behav Res Methods 51(1):195–203. https://doi.org/10.3758/s13428-018-01193-y

    Article  PubMed  PubMed Central  Google Scholar 

  74. Péruch P, Borel L, Gaunet F, Thinus-Blanc G, Magnan J, Lacour M (1999) Spatial performance of unilateral vestibular defective patients in nonvisual versus visual navigation. J Vestib Res 9(1):37–47

    Article  Google Scholar 

  75. Péruch P, Borel L, Magnan J, Lacour M (2005) Direction and distance deficits in path integration after unilateral vestibular loss depend on task complexity. Brain Res Cogn Brain Res 25:862–872. https://doi.org/10.1016/j.cogbrainres.2005.09.012 (doi.org/S0926-6410(05)00287-9 [pii])

    Article  PubMed  Google Scholar 

  76. Popp P, Wulff M, Finke K, Rühl M, Brandt T, Dieterich M (2017) Cognitive deficits in patients with a chronic vestibular failure. J Neurol 264(3):554–563. https://doi.org/10.1007/s00415-016-8386-7

    Article  PubMed  Google Scholar 

  77. 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. https://doi.org/10.1016/S0966-6362(03)00032-8

    Article  PubMed  Google Scholar 

  78. Rodgers MK, Sindone JA, Moffat SD (2012) Effects of age on navigation strategy. Neurobiol Aging 33(1):202.e15-202.e22. https://doi.org/10.1016/j.neurobiolaging.2010.07.021

    Article  Google Scholar 

  79. Russell NA, Horii A, Smith PF, Darlington CL, Bilkey DK (2003) Bilateral peripheral vestibular lesions produce long-term changes in spatial learning in the rat. J Vestib Res 13(1):9–16

    Article  Google Scholar 

  80. Saj A, Bachelard-Serra M, Lavieille J, Honoré J, Borel L (2021) Signs of spatial neglect in unilateral peripheral vestibulopathy. Eur J Neurol 28(5):1779–1783. https://doi.org/10.1111/ene.14701

    Article  PubMed  Google Scholar 

  81. Saj A, Cojan Y, Musel B, Honoré J, Borel L, Vuilleumier P (2014) Functional neuro-anatomy of egocentric versus allocentric space representation. Neurophysiol Clin 44(1):33–40. https://doi.org/10.1016/j.neucli.2013.10.135

    Article  CAS  PubMed  Google Scholar 

  82. Saj A, Honoré J, Bernard-Demanze L, Devèze A, Magnan J, Borel L (2013) Where is straight ahead to a patient with unilateral vestibular loss? Cortex 49(5):1219–1228. https://doi.org/10.1016/j.cortex.2012.05.019

    Article  PubMed  Google Scholar 

  83. Salatino A, Iacono C, Gammeri R, Chiadò ST, Lambert J, Sulcova D, Mouraux A, George MS, Roberts DR, Berti A, Ricci R (2021) Zero gravity induced by parabolic flight enhances automatic capture and weakens voluntary maintenance of visuospatial attention. Npj Microgravity 7(1):29. https://doi.org/10.1038/s41526-021-00159-3

    Article  PubMed  PubMed Central  Google Scholar 

  84. Sandstrom NJ, Kaufman J, A. Huettel S (1998) Males and females use different distal cues in a virtual environment navigation task. Cogn Brain Res 6(4):351–360. https://doi.org/10.1016/S0926-6410(98)00002-0

    Article  CAS  Google Scholar 

  85. Schmitzer-Torbert N (2007) Place and response learning in human virtual navigation: behavioral measures and gender differences. Behav Neurosci 121(2):277–290. https://doi.org/10.1037/0735-7044.121.2.277

    Article  PubMed  Google Scholar 

  86. Schöberl F, Pradhan C, Grosch M, Brendel M, Jostes F, Obermaier K, Sowa C, Jahn K, Bartenstein P, Brandt T, Dieterich M, Zwergal A (2021) Bilateral vestibulopathy causes selective deficits in recombining novel routes in real space. Sci Rep 11(1):2695. https://doi.org/10.1038/s41598-021-82427-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Schöberl F, Zwergal A, Brandt T (2020) Testing navigation in real space: contributions to understanding the physiology and pathology of human navigation control. Front Neural Circuits 14:6. https://doi.org/10.3389/fncir.2020.00006

    Article  PubMed  PubMed Central  Google Scholar 

  88. 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

    Article  PubMed  PubMed Central  Google Scholar 

  89. Semenov YR, Bigelow RT, Xue QL, du Lac S, Agrawal Y (2016) Association between vestibular and cognitive function in US. Adults: data from the national health and nutrition examination survey. J Gerontol A Biol Sci Med Sci 71(2):243–250. https://doi.org/10.1093/gerona/glv069

    Article  PubMed  Google Scholar 

  90. Seo YJ, Kim J, Kim SH (2016) The change of hippocampal volume and its relevance with inner ear function in Meniere’s disease patients. Auris Nasus Larynx 43(6):620–625. https://doi.org/10.1016/j.anl.2016.01.006

    Article  PubMed  Google Scholar 

  91. Sherrill KR, Erdem UM, Ross RS, Brown TI, Hasselmo ME, Stern CE (2013) Hippocampus and retrosplenial cortex combine path integration signals for successful navigation. J Neurosci 33(49):19304–19313. https://doi.org/10.1523/JNEUROSCI.1825-13.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Smith PF (2017) The vestibular system and cognition. Curr Opin Neurol 30(1):84–89. https://doi.org/10.1097/WCO.0000000000000403

    Article  PubMed  Google Scholar 

  93. Smith PF (2022) Hearing loss versus vestibular loss as contributors to cognitive dysfunction. J Neurol 269(1):87–99. https://doi.org/10.1007/s00415-020-10343-2

    Article  PubMed  Google Scholar 

  94. Strupp M, Kim J-S, Murofushi T, Straumann D, Jen JC, Rosengren SM, Della Santina CC, Kingma H (2017) Bilateral vestibulopathy: diagnostic criteria consensus document of the classification committee of the bárány society. J Vestib Res 27(4):177–189. https://doi.org/10.3233/VES-170619

    Article  PubMed  PubMed Central  Google Scholar 

  95. Taube JS, Valerio S, Yoder RM (2013) Is navigation in virtual reality with fmri really navigation? J Cogn Neurosci 25(7):1008–1019. https://doi.org/10.1162/jocn_a_00386

    Article  PubMed  Google Scholar 

  96. Ulrich S, Grill E, Flanagin VL (2019) Who gets lost and why: a representative cross-sectional survey on sociodemographic and vestibular determinants of wayfinding strategies. PLoS ONE 14(1):e0204781. https://doi.org/10.1371/journal.pone.0204781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Van Ombergen A, Wuyts FL, Jeurissen B, Sijbers J, Vanhevel F, Jillings S, Parizel PM, Sunaert S, Van de Heyning PH, Dousset V, Laureys S, Demertzi A (2017) Intrinsic functional connectivity reduces after first-time exposure to short-term gravitational alterations induced by parabolic flight. Sci Rep 7(1):3061. https://doi.org/10.1038/s41598-017-03170-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Vibert D, Häusler R (2000) Long-term evolution of subjective visual vertical after vestibular neurectomy and labyrinthectomy. Acta Otolaryngol 120(5):620–622. https://doi.org/10.1080/000164800750000432

    Article  CAS  PubMed  Google Scholar 

  99. Weniger G, Ruhleder M, Lange C, Wolf S, Irle E (2011) Egocentric and allocentric memory as assessed by virtual reality in individuals with amnestic mild cognitive impairment. Neuropsychologia 49(3):518–527. https://doi.org/10.1016/j.neuropsychologia.2010.12.031

    Article  PubMed  Google Scholar 

  100. Xie Y, Bigelow RT, Frankenthaler SF, Studenski SA, Moffat SD, Agrawal Y (2017) Vestibular loss in older adults is associated with impaired spatial navigation: data from the triangle completion task. Front Neurol 8:173. https://doi.org/10.3389/fneur.2017.00173

    Article  PubMed  PubMed Central  Google Scholar 

  101. Yoder RM, Taube JS (2014) The vestibular contribution to the head direction signal and navigation. Front Integr Neurosci. https://doi.org/10.3389/fnint.2014.00032

    Article  PubMed  PubMed Central  Google Scholar 

  102. Zu Eulenburg P, Stoeter P, Dieterich M (2010) Voxel-based morphometry depicts central compensation after vestibular neuritis. Ann Neurol 68(2):241–249. https://doi.org/10.1002/ana.22063

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank InMind-VR for providing the VRMaze software.

Author information

Authors and Affiliations

  1. Aix Marseille University, CNRS, LNC, FR3C, Marseille, France

    Roberto Gammeri, Jacques Léonard, Estelle Nakul & Christophe Lopez

  2. Department of Psychology, University of Turin, Torino, Italy

    Roberto Gammeri

  3. IRON, Institut de Recherche en Oto-Neurologie, Paris, France

    Michel Toupet, Charlotte Hautefort & Christian van Nechel

  4. Centre d’Explorations Fonctionnelles Oto-Neurologiques, Paris, France

    Michel Toupet

  5. Service ORL, Hôpital Lariboisière, Paris, France

    Charlotte Hautefort

  6. Unité Troubles de L’Équilibre Et Vertiges, CHU Brugmann, Bruxelles, Belgium

    Christian van Nechel

  7. Unité de Neuro-Ophtalmologie, CHU Erasme, Bruxelles, Belgium

    Christian van Nechel

  8. Clinique Des Vertiges, Bruxelles, Belgium

    Christian van Nechel

  9. Université de Normandie, INSERM U1075 COMETE, Caen, France

    Stéphane Besnard & Marie-Laure Machado

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

    Marion Montava & Jean-Pierre Lavieille

Authors
  1. Roberto Gammeri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jacques Léonard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michel Toupet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charlotte Hautefort
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christian van Nechel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stéphane Besnard
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marie-Laure Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Estelle Nakul
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Marion Montava
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jean-Pierre Lavieille
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Christophe Lopez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christophe Lopez.

Ethics declarations

Conflicts of interest

S. Besnard and M.L. Machado have or had financial relationships with InMind-VR and have been involved in the development of the VRMaze software.

Ethical approval

Participants were informed about the study and gave their written informed consent. Procedures were approved by the local Ethics Committee (CPP Sud-Méditerranée II) and followed the Declaration of Helsinki.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 162 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gammeri, R., Léonard, J., Toupet, M. et al. Navigation strategies in patients with vestibular loss tested in a virtual reality T-maze. J Neurol 269, 4333–4348 (2022). https://doi.org/10.1007/s00415-022-11069-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-022-11069-z

Keywords

Search

Navigation