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Persistent perceptual delay for active head movement onset relative to sound onset with and without vision

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Abstract

Knowing when the head moves is crucial information for the central nervous system to maintain a veridical representation of the self in the world for perception and action. Previous studies have shown that active head movement onset has to precede a sound by approximately 80 ms to be perceived as simultaneous, suggesting that the perceived timing of head movement is slow. However, this research was conducted with closed eyes. Given that visual information is available for most natural head movements, could perceptual delays in head movement onset be related to removing vision? Here, we examined whether visual information affects the perceived timing of active head movement onset. Participants performed a series of temporal order judgment tasks between their active head movement and an auditory tone presented at various stimulus onset asynchronies. Visual information was either absent (eyes closed) or present while either maintaining fixation on an earth or head-fixed target in the dark or in the light. Results show that head movement onset has to precede a sound by ~76 ms with eyes closed confirming previous work. The results also suggest that head movement onset must still precede a sound when fixating targets in the dark with a trend for the head having to move with less lead time with visual information and with the vestibulo-ocular reflex active or suppressed (~70 to 48 ms). Together, these results suggest that the perception of head movement onset is persistently delayed and is not fully resolved even with full field visual input.

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References

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

    Article  CAS  PubMed  Google Scholar 

  • Aschersleben G, Müsseler J (1999) Dissociations in the timing of stationary and moving stimuli. J Exp Psychol Hum Percept Perform 25:1709–1720

    Article  Google Scholar 

  • Barnett-Cowan M (2013) Vestibular perception is slow: a review. Multisens Res 26:387–403

    PubMed  Google Scholar 

  • Barnett-Cowan M, Harris LR (2009) Perceived timing of vestibular stimulation relative to touch, light and sound. Exp Brain Res 198:221–231

    Article  PubMed  Google Scholar 

  • Barnett-Cowan M, Harris LR (2011) Temporal processing of active and passive head movement. Exp Brain Res 214:27–35

    Article  PubMed  Google Scholar 

  • Barnett-Cowan M, Raeder SM, Bülthoff HH (2012) Persistent perceptual delay for head movement onset relative to auditory stimuli of different durations and rise times. Exp Brain Res 220:41–50

    Article  PubMed  PubMed Central  Google Scholar 

  • Brooks JX, Cullen KE (2014) Early vestibular processing does not discriminate active from passive self-motion if there is a discrepancy between predicted and actual proprioceptive feedback. J Neurophysiol 111:2465–2478

    Article  PubMed  PubMed Central  Google Scholar 

  • Butler JS, Smith ST, Campos JL, Bülthoff HH (2010) Bayesian integration of visual and vestibular signals for heading. J Vis 10:23

    Article  PubMed  Google Scholar 

  • Carriot J, Brooks JX, Cullen KE (2013) Multimodal integration of self-motion cues in the vestibular system: active versus passive translations. J Neurosci 33:19555–19566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemens IAH, Selen LP, Pomante A, MacNeilage PR, Medendorp WP (2017) Eye movements in darkness modulate self-motion perception. ENeuro 4:1–12

    Article  Google Scholar 

  • Clément G, Maciel F (2004) Adjustment of the vestibulo-ocular reflex gain as a function of perceived target distance in humans. Neurosci Lett 366:115–119

    Article  PubMed  Google Scholar 

  • Cullen KE (2012) The vestibular system: multimodal integration and encoding of self-motion for motor control. Trends Neurosci 35:185–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fetsch CR, Turner AH, DeAngelis GC, Angelaki DE (2009) Dynamic reweighting of visual and vestibular cues during self-motion perception. J Neurosci 29:15601–15612

    Article  CAS  PubMed  PubMed Central  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

    Article  PubMed  Google Scholar 

  • Hine T, Thorn F (1987) Compensatory eye movements during active head rotation for near targets: effects of imagination, rapid head oscillation and vergence. Vis Res 27:1639–1657

    Article  CAS  PubMed  Google Scholar 

  • Huisman M (2000) Imputation of missing item responses: some simple techniques. Qual Quant 34:331–351

    Article  Google Scholar 

  • Karmali F, Lim K, Merfeld DM (2014) Visual and vestibular perceptual thresholds each demonstrate better precision at specific frequencies and also exhibit optimal integration. J Neurophysiol 111:2393–2403

    Article  PubMed  Google Scholar 

  • Kim J, Barnett-Cowan M, Macpherson EA (2013) Integration of auditory input with vestibular and neck proprioceptive information in the interpretation of dynamic sound localization cues. In: Proceedings of meetings on acoustics ICA2013, vol 19, no 1. ASA, p 050142

  • MacNeilage PR, Banks MS, Berger DR, Bülthoff HH (2007) A Bayesian model of the disambiguation of gravitoinertial force by visual cues. Exp Brain Res 179:263–290

    Article  PubMed  Google Scholar 

  • Medendorp WP, Van Gisbergen JAM, Van Pelt S, Gielen CCAM (2000) Context compensation in the vestibuloocular reflex during active head rotations. J Neurophysiol 84:2904–2917

    CAS  PubMed  Google Scholar 

  • Medrea I, Cullen KE (2013) Multisensory integration in early vestibular processing in mice: the encoding of passive versus active motion. J Neurophysiol 110:2704–2717

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohmi M (1996) Egocentric perception through interaction among many sensory systems. Cogn Brain Res 5:87–96

    Article  CAS  Google Scholar 

  • Paige GD, Telford L, Seidman SH, Barnes GR (1998) Human vestibuloocular reflex and its interactions with vision and fixation distance during linear and angular head movement. J Neurophysiol 80:2391–2404

    CAS  PubMed  Google Scholar 

  • Riecke BE, Cunningham DW, Bülthoff HH (2007) Spatial updating in virtual reality: the sufficiency of visual information. Psychol Res 71:298–313

    Article  PubMed  Google Scholar 

  • Roy JE, Cullen KE (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21:2131–2142

    CAS  PubMed  Google Scholar 

  • Roy JE, Cullen KE (2004) Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci 24:2102–2111

    Article  CAS  PubMed  Google Scholar 

  • Royden CS, Banks MS, Crowell JA (1992) The perception of heading during eye movements. Nature 360:583–585

    Article  CAS  PubMed  Google Scholar 

  • Sanders MC, Chang NYN, Hiss MM, Uchanski RM, Hullar TE (2011) Temporal binding of auditory and rotational stimuli. Exp Brain Res 210:539–547

    Article  PubMed  Google Scholar 

  • Soyka F, Giordano PR, Barnett-Cowan M, Bülthoff HH (2012) Modeling direction discrimination thresholds for yaw rotations around an earth-vertical axis for arbitrary motion profiles. Exp Brain Res 220:89–99

    Article  PubMed  PubMed Central  Google Scholar 

  • Tong J, Patel SS, Bedell HE (2006) The attenuation of perceived motion smear during combined eye and head movements. Vis Res 46:4387–4397

    Article  PubMed  PubMed Central  Google Scholar 

  • Tong J, Aydin M, Bedell HE (2007) Direction-of-motion discrimination is facilitated by visible motion smear. Atten Percept Psychophys 69:48–55

    Article  Google Scholar 

  • von Holst E, Mittelstaedt H (1950) Das Reafferenzprinzip. Naturwissenschaften 37:464–476

    Article  Google Scholar 

  • Warren WH, Hannon DJ (1988) Direction of self-motion is perceived from optical flow. Nature 336:162–163

    Article  Google Scholar 

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Acknowledgements

This work was generously supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant (#RGPIN-05435-2014) and a Canadian Foundation for Innovation (CFI) John R. Evans Leaders Fund Grant (#32618) to MB-C. We thank Adrienne Wise for helping to test participants and Jessy Parokaran Varghese for comments on an earlier version of the manuscript.

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Correspondence to William Chung or Michael Barnett-Cowan.

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Chung, W., Barnett-Cowan, M. Persistent perceptual delay for active head movement onset relative to sound onset with and without vision. Exp Brain Res 235, 3069–3079 (2017). https://doi.org/10.1007/s00221-017-5026-0

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  • DOI: https://doi.org/10.1007/s00221-017-5026-0

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