Advertisement

Experimental Brain Research

, Volume 237, Issue 2, pp 401–410 | Cite as

Differential effects of vestibular processing on orienting exogenous and endogenous covert visual attention

  • Mariia Kaliuzhna
  • Andrea Serino
  • Steve Berger
  • Olaf BlankeEmail author
Research Article
  • 80 Downloads

Abstract

Recent research highlights the overwhelming role of vestibular information for higher order cognition. Central to body perception, vestibular cues provide information about self-location in space, self-motion versus object motion, and modulate the perception of space. Surprisingly, however, little research has dealt with how vestibular information combines with other senses to orient one’s attention in space. Here we used passive whole body rotations as exogenous (Experiment 1) or endogenous (Experiment 2) attentional cues and studied their effects on orienting visual attention in a classical Posner paradigm. We show that—when employed as an exogenous stimulus—rotation impacts attention orienting only immediately after vestibular stimulation onset. However, when acting as an endogenous stimulus, vestibular stimulation provides a robust benefit to target detection throughout the rotation profile. Our data also demonstrate that vestibular stimulation boosts attentional processing more generally, independent of rotation direction, associated with a general improvement in performance. These data provide evidence for distinct effects of vestibular processing on endogenous and exogenous attention as well as alertness that differ with respect to the temporal dynamics of the motion profile. These data reveal that attentional spatial processing and spatial body perception as manipulated through vestibular stimulation share important brain mechanisms.

Keywords

Vestibular Cognition Exogenous attention Endogenous attention 

Notes

Acknowledgements

This work has been supported by EU FP7 project VERE WP1, Grant agreement number 257695, the Swiss National Science Foundation and the Bertarelli foundation.

References

  1. Barr DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68(3):255–278Google Scholar
  2. Bates D, Maechler M (2010) lme4: linear mixed-effects models using S4 classes. R Package version 0.999375-999335Google Scholar
  3. Berger A, Henik A, Rafal R (2005) Competition between endogenous and exogenous orienting of visual attention. J Exp Psychol Gen 134(2):207Google Scholar
  4. Bottini G, Karnath H-O, 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(6):1182–1196Google Scholar
  5. Brown SB, Van Steenbergen H, Kedar T, Nieuwenhuis S (2014) Effects of arousal on cognitive control: empirical tests of the conflict-modulated Hebbian-learning hypothesis. Front Hum Neurosci 8:23Google Scholar
  6. Cappa S, Sterzi R, Vallar G, Bisiach E (1987) Remission of hemineglect and anosognosia during vestibular stimulation. Neuropsychologia 25(5):775–782Google Scholar
  7. Carmona JE, Holland AK, Stratton HJ, Harrison DW (2008) Sympathetic arousal to a vestibular stressor in high and low hostile men. Brain Cogn 66(2):150–155Google Scholar
  8. De Jong R, Liang C-C, Lauber E (1994) Conditional and unconditional automaticity: a dual-process model of effects of spatial stimulus-response correspondence. J Exp Psychol Hum Percept Perform 20(4):731Google Scholar
  9. Ferrè ER, Longo MR, Fiori F, Haggard P (2013) Vestibular modulation of spatial perception. Front Hum Neurosci 7:660Google Scholar
  10. Fiebelkorn IC, Foxe JJ, Butler JS, Mercier MR, Snyder AC, Molholm S (2011) Ready, set, reset: stimulus-locked periodicity in behavioral performance demonstrates the consequences of cross-sensory phase reset. J Neurosci 31(27):9971–9981Google Scholar
  11. 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(3):1505–1517Google Scholar
  12. Gale S, Prsa M, Schurger A, Gay A, Paillard A, Herbelin B, Guyot JP, Lopez C, Blanke O (2016) Oscillatory neural responses evoked by natural vestibular stimuli in humans. J Neurophysiol 115(3):1228–1242Google Scholar
  13. Garg M, Lata H, Walia L, Goyal O (2013) Effect of aerobic exercise on auditory and visual reaction times: a prospective study. Indian J Physiol Pharmacol 57(2):138–145Google Scholar
  14. Goldberg JM, Fernández C (2000) The vestibular system. Wiley Online Library, New YorkGoogle Scholar
  15. Gray R, Mohebbi R, Tan HZ (2009) The spatial resolution of crossmodal attention: Implications for the design of multimodal interfaces. ACM Trans Appl Percept (TAP) 6(1):4Google Scholar
  16. Green JJ, Woldorff MG (2012) Arrow-elicited cueing effects at short intervals: Rapid attentional orienting or cue-target stimulus conflict? Cognition 122(1):96–101Google Scholar
  17. Halligan P, Marshall J, Wade D (1989) Visuospatial neglect: underlying factors and test sensitivity. Lancet 334(8668):908–911Google Scholar
  18. Hartmann M, Farkas R, Mast FW (2012a) Self-motion perception influences number processing: evidence from a parity task. Cogn Process 13(1):189–192.  https://doi.org/10.1007/s10339-012-0484-6 Google Scholar
  19. Hartmann M, Grabherr L, Mast FW (2012b) Moving along the mental number line: interactions between whole-body motion and numerical cognition. J Exp Psychol Hum Percept Perform 38(6):1416Google Scholar
  20. Kaliuzhna M, Ferrè ER, Herbelin B, Blanke O, Haggard P (2016) Multisensory effects on somatosensation: a trimodal visuo-vestibular-tactile interaction. Sci Rep 6:26301Google Scholar
  21. Karnath H-O, Dieterich M (2006) Spatial neglect—a vestibular disorder? Brain 129(2):293–305Google Scholar
  22. Karnath H-O, Fetter M, Dichgans J (1996) Ocular exploration of space as a function of neck proprioceptive and vestibular input—observations in normal subjects and patients with spatial neglect after parietal lesions. Exp Brain Res 109(2):333–342Google Scholar
  23. Klein RM (2000) Inhibition of return. Trends Cogn Sci 4(4):138–147Google Scholar
  24. Kliegl R, Wei P, Dambacher M, Yan M, Zhou X (2011) Experimental effects and individual differences in linear mixed models: estimating the relationship between spatial, object, and attraction effects in visual attention. Front Psychol 1:238Google Scholar
  25. Lewald J, Karnath H-O (2000) Vestibular influence on human auditory space perception. J Neurophysiol 84(2):1107–1111Google Scholar
  26. Lewald J, Karnath HO (2001) Sound lateralization during passive whole-body rotation. Eur J Neurosci 13(12):2268–2272Google Scholar
  27. Max C, Widmann A, Kotz SA, Schröger E, Wetzel N (2015) Distraction by emotional sounds: disentangling arousal benefits and orienting costs. Emotion 15(4):428Google Scholar
  28. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113Google Scholar
  29. Posner MI (1980) Orienting of attention. Q J Exp Psychol 32(1):3–25Google Scholar
  30. Posner MI, Snyder CR, Davidson BJ (1980) Attention and the detection of signals. J Exp Psychol Gen 109(2):160Google Scholar
  31. Poulton EC (1950) Perceptual anticipation and reaction time. Q J Exp Psychol 2(3):99–112.  https://doi.org/10.1080/17470215008416582 Google Scholar
  32. Prime DJ, McDonald JJ, Green J, Ward LM (2008) When cross-modal spatial attention fails. Can J Exp Psychol/Rev Can Psychol Exp 62(3):192Google Scholar
  33. Proctor RW, Reeve TG (1990) Research on stimulus-response compatibility: toward a comprehensive account. In: Advances in psychology, vol 65. Elsevier, New York, pp 483–494Google Scholar
  34. Prsa M, Gale S, Blanke O (2012) Self-motion leads to mandatory cue fusion across sensory modalities. J Neurophysiol 108(8):2282–2291Google Scholar
  35. Raymond JE, Shapiro KL, Arnell KM (1992) Temporary suppression of visual processing in an RSVP task: an attentional blink? J Exp Psychol Hum Percept Perform 18(3):849Google Scholar
  36. Rorden C, Karnath H-O, Driver J (2001) Do neck-proprioceptive and caloric-vestibular stimulation influence covert visual attention in normals, as they influence visual neglect? Neuropsychologia 39(4):364–375Google Scholar
  37. Santangelo V, Van der Lubbe RH, Belardinelli MO, Postma A (2006) Spatial attention triggered by unimodal, crossmodal, and bimodal exogenous cues: a comparison of reflexive orienting mechanisms. Exp Brain Res 173(1):40–48Google Scholar
  38. Santangelo V, Van der Lubbe RH, Belardinelli MO, Postma A (2008) Multisensory integration affects ERP components elicited by exogenous cues. Exp Brain Res 185(2):269–277Google Scholar
  39. Shuren J, Hartley T, Heilman KM (1998) The effects of rotation on spatial attention. Cogn Behav Neurol 11(2):72–75Google Scholar
  40. Sloan RP, Bagiella E, Shapiro PA, Kuhl JP, Chernikhova D, Berg J, Myers MM (2001) Hostility, gender, and cardiac autonomic control. Psychosom Med 63(3):434–440Google Scholar
  41. Spence C (2010) Crossmodal spatial attention. Ann N Y Acad Sci 1191(1):182–200Google Scholar
  42. Vallar G, Sterzi R, Bottini G, Cappa S, Rusconi ML (1990) Temporary remission of left hemianesthesia after vestibular stimulation. A sensory neglect phenomenon. Cortex 26(1):123–131Google Scholar
  43. van Elk M, Blanke O (2012) Balancing bistable perception during self-motion. Exp Brain Res 222(3):219–228Google Scholar
  44. Watanabe K (2001) Modulation of spatial attention with unidirectional field motion: an implication for the shift of the OKN beating field. Vis Res 41(6):801–814Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Center for Neuroprosthetics, Brain Mind Institute, Faculty of Life Sciences, School of Life ScienceEcole Polytechnique Fédérale de LausanneLausanneSwitzerland
  2. 2.Laboratory of Cognitive Neuroscience, Brain Mind Institute, School of Life ScienceEcole Polytechnique Fédérale de LausanneLausanneSwitzerland
  3. 3.Department of PsychologyUniversity of BolognaBolognaItaly
  4. 4.Department of NeurologyUniversity HospitalGenevaSwitzerland

Personalised recommendations