Experimental Brain Research

, Volume 209, Issue 2, pp 205–214 | Cite as

Mental transformation abilities in patients with unilateral and bilateral vestibular loss

  • Luzia Grabherr
  • Cyril Cuffel
  • Jean-Philippe Guyot
  • Fred W. Mast
Research Article

Abstract

Vestibular information helps to establish a reliable gravitational frame of reference and contributes to the adequate perception of the location of one’s own body in space. This information is likely to be required in spatial cognitive tasks. Indeed, previous studies suggest that the processing of vestibular information is involved in mental transformation tasks in healthy participants. In this study, we investigate whether patients with bilateral or unilateral vestibular loss show impaired ability to mentally transform images of bodies and body parts compared to a healthy, age-matched control group. An egocentric and an object-based mental transformation task were used. Moreover, spatial perception was assessed using a computerized version of the subjective visual vertical and the rod and frame test. Participants with bilateral vestibular loss showed impaired performance in mental transformation, especially in egocentric mental transformation, compared to participants with unilateral vestibular lesions and the control group. Performance of participants with unilateral vestibular lesions and the control group are comparable, and no differences were found between right- and left-sided labyrinthectomized patients. A control task showed no differences between the three groups. The findings from this study substantiate that central vestibular processes are involved in imagined spatial body transformations; but interestingly, only participants with bilateral vestibular loss are affected, whereas unilateral vestibular loss does not lead to a decline in spatial imagery.

Keywords

Vestibular Spatial cognition Mental rotation Subjective visual vertical Rod and frame test 

Notes

Acknowledgments

We thank the participants for volunteering to participate, Nikola Sanz and Aurélie Manuel for assistance with data collection, Michael Vögeli for his support in programming and Claudia Blum for designing the stimuli. We would also like to thank two anonymous reviewers for helpful comments on an earlier version of the manuscript. This study was funded by a grant from the Swiss National Science Foundation (Sinergia project “Balancing Self and Body”).

Supplementary material

221_2011_2535_MOESM1_ESM.pdf (54 kb)
Supplementary material 1 (PDF 53.9 kb)
221_2011_2535_MOESM2_ESM.pdf (68 kb)
Supplementary material 2 (PDF 68.4 kb)

References

  1. Amorim MA, Isableu B, Jarraya M (2006) Embodied spatial transformations: “body analogy” for the mental rotation of objects. J Exp Psychol Gen 135:327–347CrossRefPubMedGoogle Scholar
  2. Andre JM, Martinet N, Paysant J, Beis JM, Le Chapelain L (2001) Temporary phantom limbs evoked by vestibular caloric stimulation in amputees. Neuropsychiatry Neuropsychol Behav Neurol 14:190–196PubMedGoogle Scholar
  3. Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M (2001) Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol 85:886–899PubMedGoogle Scholar
  4. Bisiach E, Rusconi ML, Vallar G (1991) Remission of somatoparaphrenic delusion through vestibular stimulation. Neuropsychologia 29:1029–1031CrossRefPubMedGoogle Scholar
  5. Blanke O, Mohr C, Michel CM, Pascual-Leone A, Brugger P, Seeck M, Landis T, Thut G (2005) Linking out-of-body experience and self processing to mental own-body imagery at the temporoparietal junction. J Neurosci 25:550–557CrossRefPubMedGoogle Scholar
  6. Bohmer A, Mast F (1999a) Assessing otolith function by the subjective visual vertical. Ann N Y Acad Sci 871:221–231CrossRefPubMedGoogle Scholar
  7. Bohmer A, Mast F (1999b) Chronic unilateral loss of otolith function revealed by the subjective visual vertical during off center yaw rotation. J Vestib Res 9:413–422PubMedGoogle Scholar
  8. Borel L, Lopez C, Peruch P, Lacour M (2008) Vestibular syndrome: a change in internal spatial representation. Neurophysiol Clin 38:375–389CrossRefPubMedGoogle Scholar
  9. Brandt T, Dieterich M (1999) The vestibular cortex. Its locations, functions, and disorders. Ann N Y Acad Sci 871:293–312CrossRefPubMedGoogle Scholar
  10. Brandt T, Schautzer F, Hamilton DA, Bruning R, Markowitsch HJ, Kalla R, Darlington C, Smith P, Strupp M (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128:2732–2741CrossRefPubMedGoogle Scholar
  11. Chen-Huang C, McCrea RA (1999) Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation. J Neurophysiol 81:2538–2557PubMedGoogle Scholar
  12. Clement G, Fraysse MJ, Deguine O (2009) Mental representation of space in vestibular patients with otolithic or rotatory vertigo. Neuroreport 20:457–461CrossRefPubMedGoogle Scholar
  13. Creem-Regehr SH, Neil JA, Yeh HJ (2007) Neural correlates of two imagined egocentric transformations. Neuroimage 35:916–927CrossRefPubMedGoogle Scholar
  14. de Waele C, Baudonniere PM, Lepecq JC, Tran Ba Huy P, Vidal PP (2001) Vestibular projections in the human cortex. Exp Brain Res 141:541–551CrossRefPubMedGoogle Scholar
  15. Dieterich M, Brandt T (2008) Functional brain imaging of peripheral and central vestibular disorders. Brain 131:2538–2552CrossRefPubMedGoogle Scholar
  16. 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 13:994–1007CrossRefPubMedGoogle Scholar
  17. Emri M, Kisely M, Lengyel Z, Balkay L, Marian T, Miko L, Berenyi E, Sziklai I, Tron L, Toth A (2003) Cortical projection of peripheral vestibular signaling. J Neurophysiol 89:2639–2646CrossRefPubMedGoogle Scholar
  18. Grabherr L, Mast FW (2010) Effects of microgravity on cognition: The case of mental imagery. J Vestib Res 20:53–60PubMedGoogle Scholar
  19. Grabherr L, Karmali F, Bach S, Indermaur K, Metzler S, Mast FW (2007) Mental own-body and body-part transformations in microgravity. J Vestib Res 17:279–287PubMedGoogle Scholar
  20. Guerraz M, Yardley L, Bertholon P, Pollak L, Rudge P, Gresty MA, Bronstein AM (2001) Visual vertigo: symptom assessment, spatial orientation and postural control. Brain 124:1646–1656CrossRefPubMedGoogle Scholar
  21. Halmagyi GM, Curthoys IS, Cremer PD, Henderson CJ, Todd MJ, Staples MJ, D’Cruz DM (1990) The human horizontal vestibulo-ocular reflex in response to high-acceleration stimulation before and after unilateral vestibular neurectomy. Exp Brain Res 81:479–490CrossRefPubMedGoogle Scholar
  22. Hanes DA, McCollum G (2006) Cognitive-vestibular interactions: a review of patient difficulties and possible mechanisms. J Vestib Res 16:75–91PubMedGoogle Scholar
  23. Hufner K, Hamilton DA, Kalla R, Stephan T, Glasauer S, Ma J, Bruning R, Markowitsch HJ, Labudda K, Schichor C, Strupp M, Brandt T (2007) Spatial memory and hippocampal volume in humans with unilateral vestibular deafferentation. Hippocampus 17:471–485CrossRefPubMedGoogle Scholar
  24. Inagaki H, Meguro K, Shimada M, Ishizaki J, Okuzumi H, Yamadori A (2002) Discrepancy between mental rotation and perspective-taking abilities in normal aging assessed by Piaget’s three-mountain task. J Clin Exp Neuropsychol 24:18–25CrossRefPubMedGoogle Scholar
  25. Isaac A, Marks DF, Russell DG (1986) An instrument for assessing imagery of movement: the vividness of movement imagery questionnaire (VMIQ). J Mental Imag 10:23–30Google Scholar
  26. Isableu B, Gueguen M, Fourré B, Giraudet G, Amorim MA (2008) Assessment of visual field dependence: comparison between the mechanical 3D rod-and-frame test developed by Oltman in 1968 with a 2D computer-based version. J Vestib Res 18:239–247PubMedGoogle Scholar
  27. Le Chapelain L, Beis JM, Paysant J, Andre JM (2001) Vestibular caloric stimulation evokes phantom limb illusions in patients with paraplegia. Spinal Cord 39:85–87CrossRefPubMedGoogle Scholar
  28. Lenggenhager B, Lopez C, Blanke O (2008) Influence of galvanic vestibular stimulation on egocentric and object-based mental transformations. Exp Brain Res 184:211–221CrossRefPubMedGoogle Scholar
  29. Leone G, Lipshits M, Gurfinkel V, Berthoz A (1995) Is there an effect of weightlessness on mental rotation of three-dimensional objects? Brain Res Cogn Brain Res 2:255–267CrossRefPubMedGoogle Scholar
  30. Lobel E, Kleine JF, Leroy-Willig A, Van de Moortele PF, Le Bihan D, Grusser OJ, Berthoz A (1999) Cortical areas activated by bilateral galvanic vestibular stimulation. Ann N Y Acad Sci 871:313–323CrossRefPubMedGoogle Scholar
  31. Lopez C, Lacour M, Magnan J, Borel L (2006) Visual field dependence-independence before and after unilateral vestibular loss. Neuroreport 17:797–803CrossRefPubMedGoogle Scholar
  32. 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 45:2025–2037CrossRefPubMedGoogle Scholar
  33. Mamoto Y, Yamamoto K, Imai T, Tamura M, Kubo T (2002) Three-dimensional analysis of human locomotion in normal subjects and patients with vestibular deficiency. Acta Otolaryngol 122:495–500CrossRefPubMedGoogle Scholar
  34. Mast FW, Ganis G, Christie S, Kosslyn SM (2003) Four types of visual mental imagery processing in upright and tilted observers. Brain Res Cogn Brain Res 17:238–247CrossRefPubMedGoogle Scholar
  35. McCrea RA, Luan H (2003) Signal processing of semicircular canal and otolith signals in the vestibular nuclei during passive and active head movements. Ann N Y Acad Sci 1004:169–182CrossRefPubMedGoogle Scholar
  36. Parsons LM (1987a) Imagined spatial transformation of one’s body. J Exp Psychol Gen 116:172–191CrossRefPubMedGoogle Scholar
  37. Parsons LM (1987b) Imagined spatial transformations of one’s hands and feet. Cogn Psychol 19:178–241CrossRefPubMedGoogle Scholar
  38. Parsons LM(2003) Superior parietal cortices and varieties of mental rotation. Trends Cogn Sci 7:515–517CrossRefPubMedGoogle Scholar
  39. Peruch 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 25:862–872CrossRefPubMedGoogle Scholar
  40. Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118PubMedGoogle Scholar
  41. Ratcliff G (1979) Spatial thought, mental rotation and the right cerebral hemisphere. Neuropsychologia 17:49–54CrossRefPubMedGoogle Scholar
  42. Rodionov V, Zislin J, Elidan J (2004) Imagination of body rotation can induce eye movements. Acta Otolaryngol 124:684–689CrossRefPubMedGoogle Scholar
  43. Saimpont A, Pozzo T, Papaxanthis C (2009) Aging affects the mental rotation of left and right hands. PLoS One 4:e6714CrossRefPubMedGoogle Scholar
  44. Schautzer F, Hamilton D, Kalla R, Strupp M, Brandt T (2003) Spatial memory deficits in patients with chronic bilateral vestibular failure. Ann N Y Acad Sci 1004:316–324CrossRefPubMedGoogle Scholar
  45. Shepard RN, Metzler J (1971) Mental rotation of three-dimensional objects. Science 171:701–703CrossRefPubMedGoogle Scholar
  46. Smith PF, Zheng Y, Horii A, Darlington CL (2005) Does vestibular damage cause cognitive dysfunction in humans? J Vestib Res 15:1–9PubMedGoogle Scholar
  47. Tomasino B, Rumiati RI (2004) Effects of strategies on mental rotation and hemispheric lateralization: neuropsychological evidence. J Cogn Neurosci 16:878–888CrossRefPubMedGoogle Scholar
  48. Vibert D, Hausler R (2000) Long-term evolution of subjective visual vertical after vestibular neurectomy and labyrinthectomy. Acta Otolaryngol 120:620–622CrossRefPubMedGoogle Scholar
  49. Vitte E, Derosier C, Caritu Y, Berthoz A, Hasboun D, Soulie D (1996) Activation of the hippocampal formation by vestibular stimulation: a functional magnetic resonance imaging study. Exp Brain Res 112:523–526CrossRefPubMedGoogle Scholar
  50. Zacks J, Rypma B, Gabrieli JD, Tversky B, Glover GH (1999) Imagined transformations of bodies: an fMRI investigation. Neuropsychologia 37:1029–1040CrossRefPubMedGoogle Scholar
  51. Zacks JM, Mires J, Tversky B, Hazeltine E (2000) Mental spatial transformations of objects and perspective. Spatial Cognit Comput 2:315–332CrossRefGoogle Scholar
  52. Zacks JM, Ollinger JM, Sheridan MA, Tversky B (2002) A parametric study of mental spatial transformations of bodies. Neuroimage 16:857–872CrossRefPubMedGoogle Scholar
  53. Zacks JM, Gilliam F, Ojemann JG (2003) Selective disturbance of mental rotation by cortical stimulation. Neuropsychologia 41:1659–1667CrossRefPubMedGoogle Scholar
  54. Zheng Y, Darlington CL, Smith PF (2004) Bilateral labyrinthectomy causes long-term deficit in object recognition in rat. Neuroreport 15:1913–1916CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Luzia Grabherr
    • 1
  • Cyril Cuffel
    • 2
  • Jean-Philippe Guyot
    • 2
  • Fred W. Mast
    • 1
  1. 1.Department of PsychologyUniversity of BernBernSwitzerland
  2. 2.Department of Otorhinolaryngology, Head and Neck SurgeryUniversity Hospital of GenevaGenevaSwitzerland

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