Skip to main content

Self-motion perception training: thresholds improve in the light but not in the dark

Abstract

We investigated perceptual learning in self-motion perception. Blindfolded participants were displaced leftward or rightward by means of a motion platform and asked to indicate the direction of motion. A total of eleven participants underwent 3,360 practice trials, distributed over twelve (Experiment 1) or 6 days (Experiment 2). We found no improvement in motion discrimination in both experiments. These results are surprising since perceptual learning has been demonstrated for visual, auditory, and somatosensory discrimination. Improvements in the same task were found when visual input was provided (Experiment 3). The multisensory nature of vestibular information is discussed as a possible explanation of the absence of perceptual learning in darkness.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Notes

  1. The perception of passive whole-body motion is based on visual, auditory, vestibular, somatosensory, proprioceptive, and viscerosceptive signals. In the present study, participants were displaced in darkness and exposed to white noise. Therefore, we regard vestibular signals as the main source of self-motion information (see also Benson et al. 1986; Bertolini et al. 2012; Kingma 2005; Valko et al. 2012).

References

  • Aberg KC, Herzog MH (2012) Different types of feedback change decision criterion and sensitivity differently in perceptual learning. J Vis 12(3). doi:10.1167/12.3.3

  • Aberg KC, Tartaglia EM, Herzog MH (2009) Perceptual learning with Chevrons requires a minimal number of trials, transfers to untrained directions, but does not require sleep. Vision Res 49(16):2087–2094. doi:10.1016/j.visres.2009.05.020

    Article  PubMed  Google Scholar 

  • Adini Y, Sagi D, Tsodyks M (2002) Context-enabled learning in the human visual system. Nature 415(6873):790–793. doi:10.1038/415790a415790a

    Article  PubMed  Google Scholar 

  • Adini Y, Wilkonsky A, Haspel R, Tsodyks M, Sagi D (2004) Perceptual learning in contrast discrimination: the effect of contrast uncertainty. J Vis 4(12):993–1005. doi:10.1167/4.12.2/4/12/2/

    Article  PubMed  Google Scholar 

  • Ahissar M, Hochstein S (2002) The role of attention in learning simple visual tasks. In: Fahle M, Poggi T (eds) Perceptual learning. MIT Press, Cambridge, pp 253–271

    Google Scholar 

  • Ahn SC (2003) Short-term vestibular responses to repeated rotations in pilots. Aviat Space Environ Med 74(3):285–287

    PubMed  Google Scholar 

  • Alais D, Cass J (2010) Multisensory perceptual learning of temporal order: audiovisual learning transfers to vision but not audition. PLoS One 5(6):e11283

    Article  PubMed  Google Scholar 

  • Alpini D, Botta M, Mattei V, Tornese D (2009) Figure ice skating induces vestibulo-ocular adaptation specific to required athletic skills. Sport Sci Health 5(3):129–134

    Article  Google Scholar 

  • Bao S, Chang EF, Woods J, Merzenich MM (2004) Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. Nat Neurosci 7(9):974–981

    Article  PubMed  CAS  Google Scholar 

  • Beard BL, Levi DM, Reich LN (1995) Perceptual learning in parafoveal vision. Vision Res 35(12):1679–1690. doi:10.1016/0042-6989(94)00267-P

    Article  PubMed  CAS  Google Scholar 

  • Beer AL, Watanabe T (2009) Specificity of auditory-guided visual perceptual learning suggests crossmodal plasticity in early visual cortex. Exp Brain Res 198(2):353–361

    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(11):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(3):205–213

    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(1):209–223. doi:10.1152/jn.00154.2010

    Article  PubMed  CAS  Google Scholar 

  • Bertolini G, Ramat S, Bockisch CJ, Marti S, Straumann D, Palla A (2012) Is Vestibular self-motion perception controlled by the velocity storage? Insights from patients with chronic degeneration of the vestibulo-cerebellum. PLoS One 7(6):e36763

    Article  PubMed  CAS  Google Scholar 

  • Censor N, Sagi D (2009) Explaining training induced performance increments and decrements within a unified framework of perceptual learning. Learn Percept 1(1):3–17

    Article  Google Scholar 

  • Censor N, Karni A, Sagi D (2006) A link between perceptual learning, adaptation and sleep. Vision Res 46(23):4071–4074. doi:10.1016/j.visres.2006.07.022

    Article  PubMed  Google Scholar 

  • Clément G, Tilikete C, Courjon JH (2008) Retention of habituation of vestibulo-ocular reflex and sensation of rotation in humans. Exp Brain Res 190(3):307–315

    Article  PubMed  Google Scholar 

  • Cutfield NJ, Cousins S, Seemungal BM, Gresty MA, Bronstein AM (2011) Vestibular perceptual thresholds to angular rotation in acute unilateral vestibular paresis and with galvanic stimulation. Ann N Y Acad Sci 1233(1):256–262. doi:10.1111/j.1749-6632.2011.06159.x

    Article  PubMed  Google Scholar 

  • Dosher BA, Lu ZL (1998) Perceptual learning reflects external noise filtering and internal noise reduction through channel reweighting. PNAS 95(23):13988

    Article  PubMed  CAS  Google Scholar 

  • Fahle M (1997) Specificity of learning curvature, orientation, and vernier discriminations. Vision Res 37(14):1885–1895. doi:10.1016/S0042-6989(96)00308-2

    Article  PubMed  CAS  Google Scholar 

  • Fahle M (2004) Perceptual learning: a case for early selection. J Vis 4(10):879–890. doi:10.1167/4.10.4/4/10/4/

    Article  PubMed  Google Scholar 

  • Fahle M, Edelman S (1993) Long-term learning in vernier acuity: effects of stimulus orientation, range and of feedback. Vision Res 33(3):397–412

    Article  PubMed  CAS  Google Scholar 

  • Fahle M, Poggio T (2002) Perceptual learning. MIT Press, Cambridge

    Google Scholar 

  • Fasold O, von Brevern M, Kuhberg M, Ploner CJ, Villringer A, Lempert T, Wenzel R (2002) Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. Neuroimage 17(3):1384–1393

    Article  PubMed  Google Scholar 

  • Fine I, Jacobs RA (2002) Comparing perceptual learning tasks: a review. J Vis 2(2):190–203. doi:10.1167/2.2.52/2/5

    Article  PubMed  Google Scholar 

  • Gianna C, Heimbrand S, Gresty M (1996) Thresholds for detection of motion direction during passive lateral whole-body acceleration in normal subjects and patients with bilateral loss of labyrinthine function. Brain Res Bull 40(5–6):443–447

    Article  PubMed  CAS  Google Scholar 

  • 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(4):677–681. doi:10.1007/s00221-008-1350-8

    Article  PubMed  Google Scholar 

  • Hartmann M, Grabherr L, Mast FW (2012) Moving along the mental number line: interactions between whole-body motion and numerical cognition. J Exp Psychol Hum Percept Perform 38(6):1416–1427. doi:10.1037/a0026706

    Article  PubMed  Google Scholar 

  • Hauptmann B, Reinhart E, Brandt SA, Karni A (2005) The predictive value of the leveling off of within session performance for procedural memory consolidation. Brain Res Cogn Brain Res 24(2):181–189. doi:10.1016/j.cogbrainres.2005.01.012

    Article  PubMed  Google Scholar 

  • Herzog MH, Esfeld M (2009) How the mind constitutes itself through perceptual learning. Learn Percept 1(1):147–154. doi:10.1556/lp.1.2009.1.11

    Article  Google Scholar 

  • Herzog MH, Fahle M (1997) The role of feedback in learning a vernier discrimination task. Vision Res 37(15):2133–2141. doi:10.1016/S0042-6989(97)00043-6

    Article  PubMed  CAS  Google Scholar 

  • Herzog MH, Fahle M (1998) Modeling perceptual learning: difficulties and how they can be overcome. Biol Cybern 78(2):107–117

    Article  PubMed  CAS  Google Scholar 

  • Huang CB, Zhou Y, Lu ZL (2008) Broad bandwidth of perceptual learning in the visual system of adults with anisometropic amblyopia. PNAS 105(10):4068–4073. doi:10.1073/pnas.0800824105

    Article  PubMed  CAS  Google Scholar 

  • Hussain Z, Sekuler AB, Bennett PJ (2009) How much practice is needed to produce perceptual learning? Vision Res 49(21):2624–2634. doi:10.1016/j.visres.2009.08.022

    Article  PubMed  Google Scholar 

  • Jeter PE, Dosher BA, Liu SH (2007) Transfer (vs. specificity) following different amounts of perceptual learning in tasks differing in stimulus orientation and position. J Vis 7(9):84

    Article  Google Scholar 

  • Karni A, Sagi D (1991) Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. PNAS 88(11):4966

    Article  PubMed  CAS  Google Scholar 

  • Kingma H (2005) Thresholds for perception of direction of linear acceleration as a possible evaluation of the otolith function. BMC Ear Nose Throat Disord 5(1):5

    Article  PubMed  CAS  Google Scholar 

  • Kingma H, Kavelaars J, van Tienen N, Caris R (2001) Evaluation of the statolith function by measurement of ocular counterrolling? Oto-Rhino-Laryngologia Nova 11(2):68–79

    Article  Google Scholar 

  • Koyama S, Harner A, Watanabe T (2004) Task-dependent changes of the psychophysical motion-tuning functions in the course of perceptual learning. Perception 33(9):1139–1147

    Article  PubMed  Google Scholar 

  • Kuai S-G, Zhang J-Y, Klein SA, Levi DM, Yu C (2005) The essential role of stimulus temporal patterning in enabling perceptual learning. Nat Neurosci 8(11):1497–1499

    Article  PubMed  CAS  Google Scholar 

  • Lee MY, Kim MS, Park BR (2004) Adaptation of the horizontal vestibuloocular reflex in pilots. Laryngoscope 114(5):897–902. doi:10.1097/00005537-200405000-00021

    Article  PubMed  Google Scholar 

  • Leek MR (2001) Adaptive procedures in psychophysical research. Percept Psychophys 63(8):1279–1292

    Article  PubMed  CAS  Google Scholar 

  • Lempert T, Neuhauser H (2009) Epidemiology of vertigo, migraine and vestibular migraine. J Neurol 256(3):333–338. doi:10.1007/s00415-009-0149-2

    Article  PubMed  Google Scholar 

  • Li R, Polat U, Makous W, Bavelier D (2009) Enhancing the contrast sensitivity function through action video game training. Nat Neurosci 12(5):549–551

    Article  PubMed  Google Scholar 

  • Liu Z, Vaina LM (1998) Simultaneous learning of motion discrimination in two directions. Brain Res Cogn Brain Res 6(4):347–349. doi:10.1016/S0926-6410(98)00008-1

    Article  PubMed  CAS  Google Scholar 

  • Lopez C, Blanke O (2011) The thalamocortical vestibular system in animals and humans. Brain Res Rev 67(1–2):119–146. doi:10.1016/j.brainresrev.2010.12.002

    Article  PubMed  Google Scholar 

  • Lopez C, Blanke O, Mast FW (2012) The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neurosci 212:159–179. doi:10.1016/j.neuroscience.2012.03.028

    Article  CAS  Google Scholar 

  • Mallery R, Olomu O, Uchanski R, Militchin V, Hullar T (2010) Human discrimination of rotational velocities. Exp Brain Res 204(1):11–20. doi:10.1007/s00221-010-2288-1

    Article  PubMed  Google Scholar 

  • Merfeld DM (2012) Spatial orientation and the vestibular system. In: Wolfe JM, Kluender KR, Levi DM (eds) Sensation & Perception, 3rd edn. Sinauer Associates, Inc., Massachusetts

    Google Scholar 

  • Merfeld DM, Park S, Gianna-Poulin C, Black FO, Wood S (2005a) Vestibular perception and action employ qualitatively different mechanisms. I. Frequency response of VOR and perceptual responses during translation and tilt. J Neurophysiol 94(1):186–198

    Article  PubMed  Google Scholar 

  • Merfeld DM, Park S, Gianna-Poulin C, Black FO, Wood S (2005b) Vestibular perception and action employ qualitatively different mechanisms. II. VOR and perceptual responses during combined Tilt&Translation. J Neurophysiol 94(1):199–205

    Article  PubMed  Google Scholar 

  • Merfeld DM, Valko Y, Karmali F, Lim K, Priesol AJ, Lewis RF (2012) The contributions of the human vestibular system to direction-recognition thresholds as a function of frequency. Program No. 828.08. 2012 Neuroscience meeting planner. Society for Neuroscience, New Orleans, LA

  • Mittelstaedt H (1992) Somatic versus vestibular gravity reception in man. Ann N Y Acad Sci 656:124–139

    Article  PubMed  CAS  Google Scholar 

  • Mittelstaedt H (1996) Somatic graviception. Biol Psychol 42(1–2):53–74

    Article  PubMed  CAS  Google Scholar 

  • Neuhauser HK, Radtke A, von Brevern M, Lezius F, Feldmann M, Lempert T (2008) Burden of dizziness and vertigo in the community. Arch Intern Med 168(19):2118

    Article  PubMed  Google Scholar 

  • Okada T, Grunfeld E, Shallo-Hoffmann J, Bronstein A (1999) Vestibular perception of angular velocity in normal subjects and in patients with congenital nystagmus. Brain 122(7):1293–1303

    Article  PubMed  Google Scholar 

  • Osterhammel P, Terkildsen K, Zilstorff K (1968) Vestibular habituation in ballet dancers. Acta Otolaryngol 66(3):221–228

    Article  PubMed  CAS  Google Scholar 

  • Owen DH, Machamer PK (1979) Bias-free improvement in wine discrimination. Perception 8(2):199

    Article  PubMed  CAS  Google Scholar 

  • Poggio T, Fahle M, Edelman S (1992) Fast perceptual learning in visual hyperacuity. Science 256(5059):1018–1021

    Article  PubMed  CAS  Google Scholar 

  • Polat U (2009) Making perceptual learning practical to improve visual functions. Vision Res 49(21):2566–2573

    Article  PubMed  Google Scholar 

  • Quarck G, Denise P (2005) Caractéristiques du reflexe vestibulo-oculaire chez les gymnastes. Sci motricité 2:101–112

    Article  Google Scholar 

  • Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35(2):229–248

    Article  PubMed  CAS  Google Scholar 

  • Sathian K, Zangaladze A (1998) Perceptual learning in tactile hyperacuity: complete intermanual transfer but limited retention. Exp Brain Res 118(1):131–134

    Article  PubMed  CAS  Google Scholar 

  • Schoups AA, Vogels R, Orban GA (1995) Human perceptual learning in identifying the oblique orientation: retinotopy, orientation specificity and monocularity. J Physiol 483(Pt 3):797–810

    PubMed  CAS  Google Scholar 

  • Sinha N, Zaher N, Shaikh AG, Lasker AG, Zee DS, Tarnutzer AA (2008) Perception of self motion during and after passive rotation of the body around an earth-vertical axis. Progr Brain Res 171:277–281. doi:10.1016/S0079-6123(08)00639-0

    Article  CAS  Google Scholar 

  • Sowden PT, Rose D, Davies IR (2002) Perceptual learning of luminance contrast detection: specific for spatial frequency and retinal location but not orientation. Vision Res 42(10):1249–1258. doi:10.1016/S0042-6989(02)00019-6

    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. Exp Brain Res 209(1):95–107. doi:10.1007/s00221-010-2523-9

    Article  PubMed  Google Scholar 

  • Soyka F, Giordano P, Barnett-Cowan M, Bülthoff H (2012) Modeling direction discrimination thresholds for yaw rotations around an earth-vertical axis for arbitrary motion profiles. Exp Brain Res 220(1):89–99. doi:10.1007/s00221-012-3120-x

    Article  PubMed  Google Scholar 

  • Tanguy S, Quarck G, Etard O, Gauthier A, Denise P (2008) Vestibulo-ocular reflex and motion sickness in figure skaters. Eur J Appl Physiol 104(6):1031–1037

    Article  PubMed  Google Scholar 

  • Taylor MM, Creelman CD (1967) Pest—efficient estimates on probability functions. J Acoust Soc Am 4p1(41):782

    Article  Google Scholar 

  • Tschiassny K (1957) Studies concerning vestibular factors in the ballet dancer, the pigeon, and the blind person. Trans Am Acad Ophthalmol Otolaryngol 61(4):503–506

    PubMed  CAS  Google Scholar 

  • Tsodyks M, Gilbert C (2004) Neural networks and perceptual learning. Nature 431(7010):775–781. doi:10.1038/nature03013

    Article  PubMed  CAS  Google Scholar 

  • Valko Y, Lewis RF, Priesol AJ, Merfeld DM (2012) Vestibular labyrinth contributions to human whole-body motion discrimination. J Neurosci 32(39):13537–13542. doi:10.1523/JNEUROSCI.2157-12.2012

    Google Scholar 

  • Watanabe T, Náñez JE, Sasaki Y (2001) Perceptual learning without perception. Nature 413(6858):844–847

    Article  PubMed  CAS  Google Scholar 

  • Wilson DA, Stevenson RJ (2003) The fundamental role of memory in olfactory perception. Trends Neurosci 26(5):243–247

    Article  PubMed  CAS  Google Scholar 

  • Wright BA, Sabin AT (2007) Perceptual learning: how much daily training is enough? Exp Brain Res 180(4):727–736. doi:10.1007/s00221-007-0898-z

    Article  PubMed  Google Scholar 

  • Xiao L-Q, Zhang J-Y, Wang R, Klein SA, Levi DM, Yu C (2008) Complete transfer of perceptual learning across retinal locations enabled by double training. Curr Biol 18(24):1922–1926

    Article  PubMed  CAS  Google Scholar 

  • Yu C, Klein SA, Levi DM (2004) Perceptual learning in contrast discrimination and the (minimal) role of context. J Vis 4(3):169–182. doi:10.1167/4.3.44/3/4

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by the Swiss National Science Foundation (Pro*Doc grant PDFMP1_127238 and Sinergia grant CRSII1-125135/1). We thank Cora Bobst, Wilhelm Klatt, and Antje Stahnke for assistance in data collection.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Matthias Hartmann.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hartmann, M., Furrer, S., Herzog, M.H. et al. Self-motion perception training: thresholds improve in the light but not in the dark. Exp Brain Res 226, 231–240 (2013). https://doi.org/10.1007/s00221-013-3428-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-013-3428-1

Keywords

  • Self-motion thresholds
  • Whole-body motion
  • Perceptual learning
  • Vestibular thresholds
  • Vestibular learning