Skip to main content
SpringerLink
Log in

Fore–aft translation aftereffects

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

A general theme in sensory perception is that exposure to a stimulus makes it seem more neutral such that perception of subsequent stimuli is shifted in the opposite direction. The visual motion aftereffect (MAE) is an extensively studied example of this. Although similar effects have been described in other sensory systems, it has not previously been described in the vestibular system. Velocity storage has been extensively studied in the vestibular system and suggests a persistence of perception in the direction of the initial movement. The current study sought to determine how motion perception is influenced by prior movement in darkness. Thirteen human subjects (mean age 41, range 21–68) underwent whole-body fore–aft translation. The threshold of vestibular motion discrimination perception was measured using a single interval (1I) of motion lasting 0.5 s in which subjects identified their direction of motion as forward or backward using an adaptive staircase. The translation aftereffect (TAE) was measured in 2-interval (2I) experiments: The adapting stimulus moved 15 cm in 1.5 s (peak velocity 20 cm/s, peak acceleration 42 cm/s2). After a fixed inter-stimulus interval (ISI) of 0.5, 1.0, 1.5, or 3 s, a second stimulus lasting 0.5 s was delivered and the subject identified the perceived direction of the second test stimulus. The test stimulus was determined using an adaptive staircase. The ISI was constant within the block, but adapting stimuli directions were randomly interleaved. During the 1I condition, the response bias was near zero in all subjects. With a 2I stimulus, 8 of 13 subjects demonstrated a significant bias. At an ISI of 0.5 s, a minority of subjects demonstrated a bias in the same direction as the adapter. When the ISI was 1, 1.5, or 3 s, all subjects who demonstrated a significant TAE had one in the opposite direction of the adapter, similar to that seen for MAE. When averaged across subjects, the TAE was significant with ISIs of 1.0 s and above. These findings demonstrate that perception of vestibular stimuli depends on prior motion. This has important implications for understanding and quantifying vestibular perception.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Addams R (1834) An account of a peculiar optical phenomenon seen after having looked at a moving body etc. Mag J Sci 5:373–374 (3rd series)

    Google Scholar 

  • Andersen GJ, Braunstein ML (1985) Induced self-motion in central vision. J Exp Psychol Hum Percept Perform 11:122–132

    Article  PubMed  CAS  Google Scholar 

  • Angelaki DE, Dickman JD (2000) Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. J Neurophysiol 84:2113–2132

    PubMed  CAS  Google Scholar 

  • Angelaki DE, Gu Y, Deangelis GC (2009) Multisensory integration: psychophysics, neurophysiology, and computation. Curr Opin Neurobiol 19:1–7

    Google Scholar 

  • Anstis S, Verstraten FA, Mather G (1998) The motion aftereffect. Trends Cogn Sci 2:111–117

    Article  PubMed  CAS  Google Scholar 

  • Barlow HB (1990) A theory about the functional role and synaptic mechanism of visual aftereffects. In: Blakemore C (ed) Vision: coding and efficiency. Cambridge University Press, Cambridge, pp 363–375

    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. doi:10.1007/s00221-009-1779-4

    Article  PubMed  Google Scholar 

  • Benson AJ, Spencer MB, Stott JR (1986) Thresholds for the detection of the direction of whole-body, linear movement in the horizontal plane. Aviat Space Environ Med 57:1088–1096

    PubMed  CAS  Google Scholar 

  • Benson AJ, Hutt EC, Brown SF (1989) Thresholds for the perception of whole body angular movement about a vertical axis. Aviat Space Environ Med 60:205–213

    PubMed  CAS  Google Scholar 

  • Bertolini G, Bockisch CJ, Straumann D, Zee DS, Ramat S (2008) Do humans show velocity-storage in the vertical rVOR? Prog Brain Res 171:207–210. doi:10.1016/S0079-6123(08)00628-6

    Article  PubMed  CAS  Google Scholar 

  • Bertolini G, Ramat S, Laurens J, Bockisch CJ, Marti S, Straumann D, Palla A (2011) Velocity storage contribution to vestibular self-motion perception in healthy human subjects. J Neurophysiol 105:209–223. doi:10.1152/jn.00154.2010

    Article  PubMed  CAS  Google Scholar 

  • Bestelmeyer PE, Rouger J, DeBruine LM, Belin P (2010) Auditory adaptation in vocal affect perception. Cognition 117:217–223. doi:10.1016/j.cognition.2010.08.008

    Article  PubMed  Google Scholar 

  • Clement G, Moore ST, Raphan T, Cohen B (2001) Perception of tilt (somatogravic illusion) in response to sustained linear acceleration during space flight. Exp Brain Res 138:410–418

    Article  PubMed  CAS  Google Scholar 

  • Cohen H, Cohen B, Raphan T, Waespe W (1992) Habituation and adaptation of the vestibuloocular reflex: a model of differential control by the vestibulocerebellum. Exp Brain Res 90:526–538

    Article  PubMed  CAS  Google Scholar 

  • Crane BT, Demer JL (2000) Effect of adaptation to telescopic spectacles on the initial human horizontal vestibuloocular reflex. J Neurophysiol 83:38–49

    PubMed  CAS  Google Scholar 

  • Eatock RA (2000) Adaptation in hair cells. Annu Rev Neurosci 23:285–314. doi:10.1146/annurev.neuro.23.1.285

    Article  PubMed  CAS  Google Scholar 

  • Ercoline WR, Devilbiss CA, Yauch DW, Brown DL (2000) Post-roll effects on attitude perception: “the Gillingham Illusion”. Aviat Space Environ Med 71:489–495

    PubMed  CAS  Google Scholar 

  • Fernandez C, Goldberg JM (1976) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J Neurophysiol 39:970–984

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gescheider GA, Wright JH (1969) Effects of vibrotactile adaptation on the perception of stimuli of varied intensity. J Exp Psychol 81:449–453

    Article  PubMed  CAS  Google Scholar 

  • Gianna CC, Heimbrand S, Nakamura T, Gresty MA (1995) Thresholds for perception of lateral motion in normal subjects and patients with bilateral loss of vestibular function. Acta Otolaryngol Suppl 520(Pt 2):343–346

    Article  PubMed  Google Scholar 

  • Gibson JJ (1950) The perception of the visual world. Houghton Mifflin, Boston

    Google Scholar 

  • Glasser DM, Tsui JM, Pack CC, Tadin D (2011) Perceptual and neural consequences of rapid motion adaptation. In: Proceedings of the National Academy of Sciences of the United States of America. doi:10.1073/pnas.1101141108

  • Grabherr L, Nicoucar K, Mast FW, Merfeld DM (2008) Vestibular thresholds for yaw rotation about an earth-vertical axis as a function of frequency. Exp Brain Res 186:677–681

    Article  PubMed  Google Scholar 

  • Gu Y, Fetsch CR, Adeyemo B, Deangelis GC, Angelaki DE (2010) Decoding of MSTd population activity accounts for variations in the precision of heading perception. Neuron 66:596–609. doi:10.1016/j.neuron.2010.04.026

    Article  PubMed  CAS  Google Scholar 

  • Harris LR, Morgan MJ, Still AW (1981) Moving and the motion after-effect. Nature 293:139–141

    Article  PubMed  CAS  Google Scholar 

  • Hershenson M (1989) Duration, time constant, and decay of the linear motion aftereffect as a function of inspection duration. Percept Psychophys 45:251–257

    Article  PubMed  CAS  Google Scholar 

  • Hess BJ, Angelaki DE (1997) Inertial vestibular coding of motion: concepts and evidence. Curr Opin Neurobiol 7:860–866

    Article  PubMed  CAS  Google Scholar 

  • Johansson G (1977) Studies on visual perception of locomotion. Perception 6:365–376

    Article  PubMed  CAS  Google Scholar 

  • Kanai R, Verstraten FA (2005) Perceptual manifestations of fast neural plasticity: motion priming, rapid motion aftereffect and perceptual sensitization. Vision Res 45:3109–3116. doi:10.1016/j.visres.2005.05.014

    Article  PubMed  Google Scholar 

  • Lundstrom RJ (1986) Responses of mechanoreceptive afferent units in the glabrous skin of the human hand to vibration. Scand J Work Environ Health 12:413–416

    Article  PubMed  CAS  Google Scholar 

  • Lyons TJ, Ercoline WR, Freeman JE, Gillingham KK (1994) Classification problems of U.S. Air Force spatial disorientation accidents, 1989–9191. Aviat Space Environ Med 65:147–152

    PubMed  CAS  Google Scholar 

  • MacNeilage PR, Banks MS, DeAngelis GC, Angelaki DE (2010) Vestibular heading discrimination and sensitivity to linear acceleration in head and world coordinates. J Neurosci 30:9084–9094. doi:10.1523/JNEUROSCI.1304-10.2010

    PubMed  CAS  Google Scholar 

  • Merfeld DM, Gong W, Morrissey J, Saginaw M, Haburcakova C, Lewis RF (2006) Acclimation to chronic constant-rate peripheral stimulation provided by a vestibular prosthesis. IEEE Trans Biomed Eng 53:2362–2372. doi:10.1109/TBME.2006.883645

    Article  PubMed  Google Scholar 

  • Miles FA, Eighmy BB (1980) Long-term adaptive changes in primate vestibuloocular reflex. I. Behavioral observations. J Neurophysiol 43:1406–1425

    PubMed  CAS  Google Scholar 

  • Nooij SA, Groen EL (2011) Rolling into spatial disorientation: simulator demonstration of the post-roll (Gillingham) illusion. Aviat Space Environ Med 82:505–512

    Article  PubMed  Google Scholar 

  • Ohmi M, Howard IP (1988) Effect of stationary objects on illusory forward self-motion induced by a looming display. Perception 17:5–11

    Article  PubMed  CAS  Google Scholar 

  • Paige GD, Tomko DL (1991) Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. J Neurophysiol 65:1170–1182

    PubMed  CAS  Google Scholar 

  • Pinkus A, Pantle A (1997) Probing visual motion signals with a priming paradigm. Vision Res 37:541–552

    Article  PubMed  CAS  Google Scholar 

  • Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Experimental brain research. Experimentelle Hirnforschung. Experimentation cerebrale 35:229–248

    PubMed  CAS  Google Scholar 

  • Reinhardt-Rutland AH (1998) Increasing-loudness aftereffect following decreasing-intensity adaptation: spectral dependence in interotic and monotic testing. Perception 27:473–482

    Article  PubMed  CAS  Google Scholar 

  • Roditi RE, Crane BT (2012) Directional asymmetries and age effects in human self-motion perception. J Assoc Res Otolaryngol [Epub ahead of print]

  • Seizova-Cajic T, Smith JL, Taylor JL, Gandevia SC (2007) Proprioceptive movement illusions due to prolonged stimulation: reversals and aftereffects. PLoS ONE 2:e1037. doi:10.1371/journal.pone.0001037

    Article  PubMed  Google Scholar 

  • Seno T, Ito H, Sunaga S (2010) Vection aftereffects from expanding/contracting stimuli. Seeing perceiving 23:273–294

    Article  PubMed  Google Scholar 

  • Soyka F, Robuffo Giordano P, Beykirch K, Bulthoff HH (2011) Predicting direction detection thresholds for arbitrary translational acceleration profiles in the horizontal plane. Experimental brain research. Experimentelle Hirnforschung. Experimentation cerebrale 209:95–107. doi:10.1007/s00221-010-2523-9

    PubMed  Google Scholar 

  • Thompson P, Burr D (2009) Visual aftereffects. Current biology: CB 19:R11–R14. doi:10.1016/j.cub.2008.10.014

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson RD, McConville KM, Na EQ (1996) Behavior of cells without eye movement sensitivity in the vestibular nuclei during combined rotational and translational stimuli. J Vestib Res 6:145–158

    Article  PubMed  CAS  Google Scholar 

  • Ullman S, Schechtman G (1982) Adaptation and gain normalization. Proceedings of the Royal Society of London. Series B, Containing papers of a biological character. Royal Soc 216:299–313

    Article  CAS  Google Scholar 

  • Wade NJ (1994) A selective history of the study of visual motion aftereffects. Perception 23:1111–1134

    Article  PubMed  CAS  Google Scholar 

  • Wallach H, Flaherty EW (1975) A compensation for field expansion caused by moving forward. Percept Psychophys 17:445–449

    Article  Google Scholar 

  • Walsh EG (1961) Role of the vestibular apparatus in the perception of motion on a parallel swing. J Physiol 155:506–513

    PubMed  CAS  Google Scholar 

  • Wang Q, Webber RM, Stanley GB (2010) Thalamic synchrony and the adaptive gating of information flow to cortex. Nat Neurosci 13:1534–1541. doi:10.1038/nn.2670

    Article  PubMed  CAS  Google Scholar 

  • Wichmann FA, Hill NJ (2001a) The psychometric function: I. Fitting, sampling, and goodness of fit. Percept Psychophys 63:1293–1313

    Article  PubMed  CAS  Google Scholar 

  • Wichmann FA, Hill NJ (2001b) The psychometric function: II. Bootstrap-based confidence intervals and sampling. Percept Psychophys 63:1314–1329

    Article  PubMed  CAS  Google Scholar 

  • Young LR, Oman CM (1969) Model for vestibular adaptation to horizontal rotation. Aerosp Med 40:1076–1080

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by a grant from the National Institute on Deafness and Other Communication Disorders K23 DC011298. Additional support was provided by the American Otological Society and a grant from the Triological Society. Technical support was provided by Shawn Olmstead-Leahey.

Author information

Authors and Affiliations

  1. Department of Otolaryngology, University of Rochester, 601 Elmwood Avenue, Box 629, Rochester, NY, 14642, USA

    Benjamin T. Crane

  2. Department of Neurobiology and Anatomy, University of Rochester, Rochester, NY, USA

    Benjamin T. Crane

  3. Department of Bioengineering, University of Rochester, Rochester, NY, USA

    Benjamin T. Crane

Authors
  1. Benjamin T. Crane
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benjamin T. Crane.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crane, B.T. Fore–aft translation aftereffects. Exp Brain Res 219, 477–487 (2012). https://doi.org/10.1007/s00221-012-3105-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-012-3105-9

Keywords

Search

Navigation