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Experimental Brain Research

, Volume 204, Issue 4, pp 493–504 | Cite as

Oculomotor prediction of accelerative target motion during occlusion: long-term and short-term effects

  • Simon J. BennettEmail author
  • Jean-Jacques Orban de Xivry
  • Philippe Lefèvre
  • Graham R. Barnes
Research Article

Abstract

The present study examined the influence of long-term (i.e., between-trial) and short-term (i.e., within-trial) predictive mechanisms on ocular pursuit during transient occlusion. To this end, we compared ocular pursuit of accelerative and decelerative target motion in trials that were presented in random or blocked-order. Catch trials in which target acceleration was unexpectedly modified were randomly interleaved in blocked-order trials. Irrespective of trial order, eye velocity decayed following target occlusion and then recovered towards the different levels of target velocity at reappearance. However, the recovery was better scaled in blocked-order trials than random-order trials. In blocked-order trials only, the reduced gain of smooth pursuit during occlusion was compensated by a change in saccade amplitude and resulted in total eye displacement (TED) that was well matched to target displacement. Subsidiary analysis indicated that three repeats of blocked-order trials was sufficient for participants to modify eye displacement compared to that exhibited in random-order trials, although more trials were required before end-occlusion eye velocity was better scaled. Finally, we found that participants exhibited evidence of a scaled response to an unexpected change in target acceleration (i.e., catch trials), although there were also transfer effects from the preceding blocked-order trials. These findings are consistent with the suggestion that on-the-fly prediction (short-term effect) is combined with memorised information from previous trials (long-term effect) to generate a persistent and veridical prediction of occluded target motion.

Keywords

Smooth pursuit Saccades Prediction Occlusion Acceleration 

Notes

Acknowledgments

This work was supported by the Leverhulme Trust (UK), the Medical Research Council (MRC), the Fonds National de la Recherche Scientifique, the Fondation pour la Recherche Scientifique Médicale, the Belgian Program on Interuniversity Attraction Poles initiated by the Belgian Federal Science Policy Office, internal research grant (Fonds Spéciaux de Recherche) of the Université catholique de Louvain, the European Space Agency (ESA) of the European Union, and the Belgian-American Educational Foundation. The scientific responsibility rests with its authors.

References

  1. Babler TG, Dannemiller JL (1993) Role of image acceleration in judging landing location of free-falling projectiles. J Exp Psychol Hum Percept Perform 19:15–31CrossRefPubMedGoogle Scholar
  2. Bahill AT, McDonald JD (1983) Model emulates human smooth pursuit system producing zero-latency target tracking. Bio Cybernet 48:213–222CrossRefGoogle Scholar
  3. Barborica A, Ferrera VP (2003) Estimating invisible target speed from neuronal activity in monkey frontal eye field. Nat Neurosci 6:66–74CrossRefPubMedGoogle Scholar
  4. Barnes GR (2008) Cognitive processes involved in smooth pursuit eye movements. Brain Cogn 68(3):309–326CrossRefPubMedGoogle Scholar
  5. Barnes GR, Schmid AM (2002) Sequence learning in human ocular smooth pursuit. Exp Brain Res 144:322–335CrossRefPubMedGoogle Scholar
  6. Barnes GR, Barnes DM, Chakraborti SR (2000) Ocular pursuit responses to repeated, single-cycle sinusoids reveal behaviour compatible with predictive pursuit. J Neurophysiol 84:2340–2355PubMedGoogle Scholar
  7. Becker W, Fuchs AF (1985) Prediction in the oculomotor system: smooth pursuit during transient disappearance of a visual target. Exp Brain Res 57:562–575CrossRefPubMedGoogle Scholar
  8. Bennett SJ, Barnes GR (2003) Human ocular pursuit during the transient disappearance of a visual target. J Neurophysiol 90:2504–2520CrossRefPubMedGoogle Scholar
  9. Bennett SJ, Barnes GR (2004) Predictive smooth ocular pursuit during the transient disappearance of a visual target. J Neurophysiol 92:578–590CrossRefPubMedGoogle Scholar
  10. Bennett SJ, Barnes GR (2006a) Combined smooth and saccadic ocular pursuit during the transient occlusion of a moving visual object. Exp Brain Res 168:313–321CrossRefPubMedGoogle Scholar
  11. Bennett SJ, Barnes GR (2006b) Smooth ocular pursuit during the transient disappearance of an accelerating visual target: the role of reflexive and voluntary control. Exp Brain Res 175:1–10CrossRefPubMedGoogle Scholar
  12. Bennett SJ, Orban de Xivry JJ, Barnes GR, Lefevre P (2007) Target acceleration can be extracted and represented within the predictive drive to ocular pursuit. J Neurophys 98:1405–1414CrossRefGoogle Scholar
  13. Brouwer AM, Brenner E, Smeets JBJ (2002) Perception of acceleration with short presentation time: can acceleration be used in interception? Percept Psychophys 64:1160–1168PubMedGoogle Scholar
  14. Cerminara N, Apps R, Marple-Horvat DE (2009) An internal model of a moving visual target in the lateral cerebellum. J Physiol 587(2):429–442CrossRefPubMedGoogle Scholar
  15. Churchland MM, Chou IH, Lisberger SG (2003) Evidence for object permanence in the smooth-pursuit eye movements of monkeys. J Neurophysiol 90(4):2205–2218CrossRefPubMedGoogle Scholar
  16. Collins CJS, Barnes GR (2005) Scaling of anticipatory smooth eye velocity in response to sequences of discrete target movements in humans. Exp Brain Res 20:1–10Google Scholar
  17. Dallos P, Jones R (1963) Learning behaviour of the eye fixation control system. IEEE Trans Autom Contr AC-8:218–227CrossRefGoogle Scholar
  18. de Brouwer S, Missal M, Barnes G, Lefèvre P (2002) Quantitative analysis of catch-up saccades during sustained pursuit. J Neurophysiol 87:1772–1780PubMedGoogle Scholar
  19. Deno DC, Crandall WF, Sherman K, Keller EL (1995) Characterization of prediction in the primate visual smooth pursuit system. BioSys 34:107–128CrossRefGoogle Scholar
  20. Leigh RJ, Zee DS (1991) The neurology of eye movements. F.A. Davis Company, PhiladelphiaGoogle Scholar
  21. Madelain L, Krauzlis RJ (2003) Pursuit of the ineffable: perceptual and motor reversals during the tracking of apparent motion. J Vision 3:642–653CrossRefGoogle Scholar
  22. Nagel M, Sprenger A, Zapf S, Erdmann C, Kömpf D, Heide W, Binkofski F, Lencer R (2006) Parametric modulation of cortical activation during smooth pursuit with and without blanking. An fMRI study. Neuroimage 29(4):1319–1325CrossRefPubMedGoogle Scholar
  23. Orban de Xivry JJ, Bennett SJ, Lefèvre P, Barnes GR (2006) Evidence for synergy between saccades and smooth pursuit during transient target disappearance. J Neurophysiol 95:418–427CrossRefPubMedGoogle Scholar
  24. Orban de Xivry JJ, Missal M, Lefèvre P (2008) A dynamic internal representation of target motion drives predictive smooth pursuit during target blanking. J Vision 8(15):1–13CrossRefGoogle Scholar
  25. Orban de Xivry JJ, Missal M, Lefèvre P (2009) Smooth pursuit performance during target blanking does not influence the trigger of predictive saccades. J Vision 9(11):1–16CrossRefGoogle Scholar
  26. Poulton EC (1975) Range effects in experiments on people. Am J Psych 88(1):3–32CrossRefGoogle Scholar
  27. Werkhoven P, Snippe H, Toet A (1992) Visual processing of optic acceleration. Vis Res 32:2313–2329CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Simon J. Bennett
    • 1
    Email author
  • Jean-Jacques Orban de Xivry
    • 3
    • 4
  • Philippe Lefèvre
    • 3
    • 4
  • Graham R. Barnes
    • 2
  1. 1.Research Institute for Exercise and Sport SciencesLiverpool John Moores UniversityLiverpoolUK
  2. 2.Faculty of Life SciencesUniversity of ManchesterManchesterUK
  3. 3.CESAME, Université Catholique de LouvainLouvain-la-NeuveBelgium
  4. 4.Laboratory of NeurophysiologyUniversité Catholique de LouvainBrusselsBelgium

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