Skip to main content

Perceived timing of vestibular stimulation relative to touch, light and sound

Abstract

Different senses have different processing times. Here we measured the perceived timing of galvanic vestibular stimulation (GVS) relative to tactile, visual and auditory stimuli. Simple reaction times for perceived head movement (438 ± 49 ms) were significantly longer than to touches (245 ± 14 ms), lights (220 ± 13 ms), or sounds (197 ± 13 ms). Temporal order and simultaneity judgments both indicated that GVS had to occur about 160 ms before other stimuli to be perceived as simultaneous with them. This lead was significantly less than the relative timing predicted by reaction time differences compatible with an incomplete tendency to compensate for differences in processing times.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Allan LG (1975) The relationship between judgments of successiveness and judgments of order. Percept Psychophys 18:29–36

    Google Scholar 

  • Alvarez-Buylla R, de Arellano JR (1952) Local responses in Pacinian corpuscles. Am J Physiol 172:237–244

    Google Scholar 

  • Angelaki DE, Cullen KE (2008) Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31:125–150

    PubMed  Article  CAS  Google Scholar 

  • Aw ST, Todd MJ, Halmagyi GM (2006) Latency and initiation of the human vestibuloocular reflex to pulsed galvanic stimulation. J Neurophysiol 96:925–930

    PubMed  Article  Google Scholar 

  • Bekesy GV (1963) Interaction of paired sensory stimuli and conduction in peripheral nerves. J Appl Physiol 18:1276–1284

    Google Scholar 

  • Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M (2001) Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol 85:886–899

    PubMed  CAS  Google Scholar 

  • Bergenheim M, Johansson H, Granlund B, Pederson J (1996) Experimental evidence for a synchronization of sensory information to conscious experience. In: Hameroff SR, Kaszniak AW, Scott AC (eds) Toward a science of consciousness: the first Tucson discussions and debates. MIT Press, Cambridge, pp 303–310

    Google Scholar 

  • Biguer B, Donaldson IML, Hein A, Jeannerod M (1988) Neck muscle vibration modifies the representation of visual motion and direction in man. Brain 111:1405–1424

    PubMed  Article  Google Scholar 

  • Brandt T, Dieterich M (1999) The vestibular cortex: its locations, functions, and disorders. Ann N Y Acad Sci 871:293–312

    PubMed  Article  CAS  Google Scholar 

  • Brantberg K, Magnusson M (1990) Galvanically induced asymmetric optokinetic after-nystagmus. Acta Otolaryngol 110:189–195

    PubMed  Article  CAS  Google Scholar 

  • Bucher SF, Dieterich M, Wiesmann M, Weiss A, Zink R, Yousry TA, Brandt T (1998) Cerebral functional magnetic resonance imaging of vestibular, auditory, and nociceptive areas during galvanic stimulation. Ann Neurol 44:120–125

    PubMed  Article  CAS  Google Scholar 

  • Buys E (1909) Beitrag zum Studium des galvanischen Nystagmus mit hilfe der Nystagmographie. Mschr Ohrenheilk 43:801–803

    Google Scholar 

  • Capelli A, Israel I (2007) One-second interval production task during postrotatory sensation. J Vestib Res 17:239–249

    PubMed  CAS  Google Scholar 

  • Capelli A, Deborne R, Israël I (2007) Temporal intervals production during passive self-motion in darkness. Curr Psychol Lett 22

  • Corey DP, Hudspeth AJ (1979) Ionic basis of the receptor potential in a vertebrate hair cell. Nature 281:675–677

    PubMed  Article  CAS  Google Scholar 

  • Craig JC, Baihua XU (1990) Temporal order and tactile patterns. Percept Psychophys 47:22–34

    PubMed  CAS  Google Scholar 

  • Day BL, Severac Cauquil A, Bartolomei L, Pastor MA, Lyon IN (1997) Human body-segment tilts induced by galvanic stimulation: a vestibularly driven balance protection mechanism. J Physiol 500:661–672

    PubMed  CAS  Google Scholar 

  • de Waele C, Baudonniere PM, Lepecq JC, Tran Ba Huy P, Vidal PP (2001) Vestibular projections in the human cortex. Exp Brain Res 141:541–551

    PubMed  Article  Google Scholar 

  • Diederich A (1995) Intersensory facilitation of reaction time: evaluation of counter and diffusion coactivation models. J Math Psychol 39:197–215

    Article  Google Scholar 

  • Engel GR, Dougherty WG (1971) Visual–auditory distance constancy. Nature 234:308

    PubMed  Article  CAS  Google Scholar 

  • Exner S (1868) Über die zu einer Gesichtswahrnehmung nöthige Zeit. Wiener Sitzungsberichte der Mathematisch-Naturwissenschaftlichen Classe der Kaiserlichen Akademie der Wissenschaften 58:601–632

  • Fernandez C, Goldberg JM (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophysiol 34:661–675

    PubMed  CAS  Google Scholar 

  • Figliozzi F, Guariglia P, Silvetti M, Siegler I, Doricchi F (2005) Effects of vestibular rotatory accelerations on covert attentional orienting in vision and touch. J Cogn Neurosci 17:1638–1651

    PubMed  Article  Google Scholar 

  • Fitzpatrick RC, Day BL (2004) Probing the human vestibular system with galvanic stimulation. J App Physiol 96:2301–2316

    Article  Google Scholar 

  • Gibbon J, Rutschmann R (1969) Temporal order judgment and reaction time. Science 165:413–415

    PubMed  Article  CAS  Google Scholar 

  • Goldberg JM, Smith CE, Fernandez C (1984) Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol 51:1236–1256

    PubMed  CAS  Google Scholar 

  • Grant P, Lee PTS (2007) Motion–visual phase-error detection in a flight simulator. J Aircr 44:927–935

    Article  Google Scholar 

  • Guldin WO, Grüsser OJ (1998) Is there a vestibular cortex? Trends Neurosci 21:254–259

    PubMed  Article  CAS  Google Scholar 

  • Harrar V, Harris LR (2005) Simultaneity constancy: detecting events with touch and vision. Exp Brain Res 166:465–473

    PubMed  Article  Google Scholar 

  • Harrar V, Harris LR (2008) The effect of exposure to asynchronous audio, visual, and tactile stimulus combinations on the perception of simultaneity. Exp Brain Res 186:517–524

    PubMed  Article  Google Scholar 

  • Hirsh IJ, Sherrick CE Jr (1961) Perceived order in different sense modalities. J Exp Psychol 62:423–432

    PubMed  Article  CAS  Google Scholar 

  • Israël I, Capelli A, Sablé D, Laurent C, Lecoq C, Bredin J (2004) Multifactorial interactions involved in linear self-transport distance estimate: a place for time. Int J Psychophysiol 53:21–28

    PubMed  Article  Google Scholar 

  • Jaekl PM, Harris LR (2007) Auditory–visual temporal integration measured by shifts in perceived temporal location. Neurosci Lett 417:219–224

    PubMed  Article  CAS  Google Scholar 

  • Jaskowski P, Jaroszyk F, Hojan-Jezierska D (1990) Temporal-order judgments and reaction time for stimuli of different modalities. Psychol Res 52:35–38

    PubMed  Article  CAS  Google Scholar 

  • Keetels M, Stekelenburg J, Vroomen J (2007) Auditory grouping occurs prior to intersensory pairing: evidence from temporal ventriloquism. Exp Brain Res 180:449–456

    PubMed  Article  Google Scholar 

  • King AJ, Palmer AR (1985) Integration of visual and auditory information in bimodal neurones in the guinea-pig superior colliculus. Exp Brain Res 60:492–500

    PubMed  Article  CAS  Google Scholar 

  • Kopinska A, Harris LR (2004) Simultaneity constancy. Perception 33:1049–1060

    PubMed  Article  Google Scholar 

  • Kuffler SW (1953) Discharge patterns and functional organization of mammalian retina. J Neurophysiol 16:37–68

    PubMed  CAS  Google Scholar 

  • Lewald J, Karnath HO (2000) Vestibular influence on human auditory space perception. J Neurophysiol 84:1107–1111

    PubMed  CAS  Google Scholar 

  • Lewald J, Karnath HO (2001) Sound lateralization during passive whole-body rotation. Eur J NeuroSci 13:2268–2272

    PubMed  Article  CAS  Google Scholar 

  • Lobel E, Kleine JF, Bihan DL, Leroy-Willig A, Berthoz A (1998) Functional MRI of galvanic vestibular stimulation. J Neurophysiol 80:2699–2709

    PubMed  CAS  Google Scholar 

  • Lorente de No R (1933) Vestibulo-ocular reflex arc. Arch Neurol Psychiat 30:245–291

    Google Scholar 

  • Lund S, Broberg C (1983) Effects of different head positions on postural sway in man induced by a reproducible vestibular error signal. Acta Physiol Scand 117:307–309

    PubMed  Article  CAS  Google Scholar 

  • Mitrani L, Shekerdjiiski S, Yakimoff N (1986) Mechanisms and asymmetries in visual perception of simultaneity and temporal order. Biol Cybern 54:159–165

    PubMed  Article  CAS  Google Scholar 

  • Navarra J, Soto-Faraco S, Spence C (2007) Adaptation to audiotactile asynchrony. Neurosci Lett 413:72–76

    PubMed  Article  CAS  Google Scholar 

  • Pfaltz CR (1967) Recherches nystagmographiques sur la réaction galvanique vestibulaire. Rev Neurol 117:309–315

    PubMed  CAS  Google Scholar 

  • Phillips-Silver J, Trainor LJ (2005) Feeling the beat: movement influences infant rhythm perception. Science 308:1430

    PubMed  Article  CAS  Google Scholar 

  • Phillips-Silver J, Trainor LJ (2007) Hearing what the body feels: auditory encoding of rhythmic movement. Cognition 105:533–546

    PubMed  Article  Google Scholar 

  • Pöppel E, Schill K, von Steinbüchel N (1990) Sensory integration within temporally neutral systems states: a hypothesis. Naturwissenschaften 77:89–91

    PubMed  Article  Google Scholar 

  • Rains JD (1963) Signal luminance and position effects in human reaction time. Vis Res 61:239–251

    PubMed  Article  CAS  Google Scholar 

  • Roll R, Velay JL, Roll JP (1991) Eye and neck proprioceptive messages contribute to the spatial coding of retinal input in visually oriented activities. Exp Brain Res 85:423–431

    PubMed  Article  CAS  Google Scholar 

  • Roufs JAJ (1963) Perception lag as a function of stimulus luminance. Vis Res 3:81–91

    Article  Google Scholar 

  • Rutschmann J, Link R (1964) Perception of temporal order of stimuli differing in sense mode and simple reaction time. Percept Mot Skills 18:345–352

    PubMed  CAS  Google Scholar 

  • Schiefer U, Strasburger H, Becker ST, Vonthein R, Schiller J, Dietrich TJ, Hart W (2001) Reaction time in automated kinetic perimetry: effects of stimulus luminance, eccentricity, and movement direction. Vis Res 41:2157–2164

    PubMed  Article  CAS  Google Scholar 

  • Schneider KA, Bavelier D (2003) Components of visual prior entry. Cogn Psychol 47:333–366

    PubMed  Article  Google Scholar 

  • Shore DI, Barnes ME, Spence C (2006) Temporal aspects of the visuotactile congruency effect. Neurosci Lett 392:96–100

    PubMed  Article  CAS  Google Scholar 

  • Snyder LH, Grieve KL, Brotchie P, Andersen RA (1998) Separate body- and world-referenced representations of visual space in parietal cortex. Nature 394:887–891

    PubMed  Article  CAS  Google Scholar 

  • Spence C, Shore DI, Klein RM (2001) Multisensory prior entry. J Exp Psychol Gen 130:799–832

    PubMed  Article  CAS  Google Scholar 

  • Spence C, Baddeley R, Zampini M, James R, Shore DI (2003) Multisensory temporal order judgments: when two locations are better than one. Percept Psychophys 65:318–328

    PubMed  Google Scholar 

  • Sugita Y, Suzuki Y (2003) Implicit estimation of sound-arrival time. Nature 421:911

    PubMed  Article  CAS  Google Scholar 

  • Taylor JL, McCloskey DI (1991) Illusions of head and visual target displacement induced by vibration of neck muscles. Brain 114:755–759

    PubMed  Article  Google Scholar 

  • Titchener EB (1908) Lectures on the elementary psychology of feeling and attention. Macmillan, New York

    Book  Google Scholar 

  • Trainor LJ, Gao X, Lei JJ, Lehtovaara K, Harris LR (2009) The primal role of the vestibular system in determining musical rhythm. Cortex 45:35–43

    PubMed  Article  Google Scholar 

  • van Eijk RLJ, Kohlrausch A, Juola JF, van de Par S (2008) Audiovisual synchrony and temporal order judgments: effects of experimental method and stimulus type. Percept Psychophys 70:955–968

    PubMed  Article  Google Scholar 

  • Vatakis A, Navarra J, Soto-Faraco S, Spence C (2008) Audiovisual temporal adaptation of speech: temporal order versus simultaneity judgments. Exp Brain Res 185:521–529

    PubMed  Article  Google Scholar 

  • Watson SRD, Colebatch JG (1998) Vestibulocollic reflexes evoked by short-duration galvanic stimulation in man. J Physiol 513:587–597

    PubMed  Article  CAS  Google Scholar 

  • Wilson JA, Anstis SM (1969) Visual delay as a function of luminance. Am J Psychol 82:350–358

    PubMed  Article  CAS  Google Scholar 

  • Zampini M, Brown T, Shore DI, Maravita A, Röder B, Spence C (2005) Audiotactile temporal order judgments. Acta Psychol 118:277–291

    Article  Google Scholar 

  • Zeki S (1998) The asynchrony of consciousness. Proc R Soc B Biol Sci 265:1583–1585

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC). M. Barnett-Cowan was supported by a PGS-D3 NSERC Scholarship and a Canadian Institutes of Health Research Vision Health Science Training Grant. Our thanks go to Michael Jenkin for technical assistance, to Jeff Sanderson who helped conduct experiments and to David Shore for comments on this project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael Barnett-Cowan.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Barnett-Cowan, M., Harris, L.R. Perceived timing of vestibular stimulation relative to touch, light and sound. Exp Brain Res 198, 221–231 (2009). https://doi.org/10.1007/s00221-009-1779-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-009-1779-4

Keywords

  • Audition
  • Galvanic vestibular stimulation
  • Multisensory
  • Simultaneity judgments
  • Temporal order judgments
  • Touch
  • Vestibular
  • Vision