Experimental Brain Research

, Volume 210, Issue 3–4, pp 569–582 | Cite as

Extraction of visual motion information for the control of eye and head movement during head-free pursuit

  • Rochelle Ackerley
  • Graham R. BarnesEmail author
Research Article


We investigated how effectively briefly presented visual motion could be assimilated and used to track future target motion with head and eyes during target disappearance. Without vision, continuation of eye and head movement is controlled by internal (extra-retinal) mechanisms, but head movement stimulates compensatory vestibulo-ocular reflex (VOR) responses that must be countermanded for gaze to remain in the direction of target motion. We used target exposures of 50–200 ms at the start of randomised step-ramp stimuli, followed by >400 ms of target disappearance, to investigate the ability to sample target velocity and subsequently generate internally controlled responses. Subjects could appropriately grade gaze velocity to different target velocities without visual feedback, but responses were fully developed only when exposure was >100 ms. Gaze velocities were sustained or even increased during target disappearance, especially when there was expectation of target reappearance, but they were always less than for controls, where the target was continuously visible. Gaze velocity remained in the direction of target motion throughout target extinction, implying that compensatory (VOR) responses were suppressed by internal drive mechanisms. Regression analysis revealed that the underlying compensatory response remained active, but with gain slightly less than unity (0.85), resulting in head-free gaze responses that were very similar to, but slightly greater than, head-fixed. The sampled velocity information was also used to grade head velocity, but in contrast to gaze, head velocity was similar whether the target was briefly or continuously presented, suggesting that head motion was controlled by internal mechanisms alone, without direct influence of visual feedback.


Expectation Extra-retinal Head movement Prediction Smooth pursuit Vestibulo-ocular reflex 



This work was supported by a grant from the Medical Research Council, UK.


  1. Barborica A, Ferrera VP (2003) Estimating invisible target speed from neuronal activity in monkey frontal eye field. Nat Neurosci 6:66–74PubMedCrossRefGoogle Scholar
  2. Barnes GR (1993) Visual-Vestibular interaction in the control of head and eye movement: the role of visual feedback and predictive mechanisms. Prog Neurobiol 41:435–472PubMedCrossRefGoogle Scholar
  3. Barnes GR (2008) Cognitive processes involved in smooth pursuit eye movements. Brain Cogn 68:309–326PubMedCrossRefGoogle Scholar
  4. Barnes GR, Asselman PT (1991) The mechanism of prediction in human smooth pursuit eye movements. J Physiol (Lond) 439:439–461Google Scholar
  5. Barnes GR, Collins CJS (2008a) Evidence for a link between the extra-retinal component of random-onset pursuit and the anticipatory pursuit of predictable object motion. J Neurophysiol 100:1135–1146PubMedCrossRefGoogle Scholar
  6. Barnes GR, Collins CJS (2008b) The influence of briefly presented randomised target motion on the extra-retinal component of ocular pursuit. J Neurophysiol 99:831–842PubMedCrossRefGoogle Scholar
  7. Barnes GR, Collins CJS (2008c) Internally generated smooth eye movement: its dynamic characteristics and role in randomised and predictable pursuit. Prog Brain Res 171:441–449PubMedCrossRefGoogle Scholar
  8. Barnes GR, Eason RD (1988) Effects of visual and non-visual mechanisms on the vestibulo-ocular reflex during pseudo-random head movements in man. J Physiol (Lond) 395:383–400Google Scholar
  9. Barnes GR, Benson AJ, Prior ARJ (1978) Visual-vestibular interaction in the control of eye movement. Aviat Space Environ Med 49:557–564PubMedGoogle Scholar
  10. Barnes GR, Schmid AM, Jarrett CB (2002) The role of expectancy and volition in smooth pursuit eye movements. Prog Brain Res 140:239–254PubMedCrossRefGoogle Scholar
  11. Barr CC, Scultheis LW, Robinson DA (1976) Voluntary, non-visual control of the vestibulo-ocular reflex. Acta Otolaryngol (Stockh) 81:365–375Google Scholar
  12. Becker W, Fuchs AF (1985) Prediction in the oculomotor system: smooth pursuit during transient disappearance of a visual target. Exp Brain Res 57:562–575PubMedCrossRefGoogle Scholar
  13. Bennett SJ, Barnes GR (2003) Human ocular pursuit during the transient disappearance of a moving target. J Neurophysiol 90:2504–2520PubMedCrossRefGoogle Scholar
  14. Bennett SJ, Barnes GR (2004) Predictive smooth ocular pursuit during the transient disappearance of a visual target. J Neurophysiol 92:578–590PubMedCrossRefGoogle Scholar
  15. Bennett SJ, Barnes GR (2006) Smooth ocular pursuit during the transient disappearance of an accelerating visual target: the role of reflexive and voluntary control. Exp Brain Res 175:1–10PubMedCrossRefGoogle Scholar
  16. Bennett SJ, Barnes GR, Orban de Xivry JJ, Lefèvre P (2004) Ocular pursuit to a predictable velocity and/or position change during the occlusion of a moving target. Soc Neurosci Abstr 33:712–716Google Scholar
  17. Carl JR, Gellman RS (1987) Human smooth pursuit: stimulus-dependent responses. J Neurophysiol 57:1446–1463PubMedGoogle Scholar
  18. Collins CJS, Barnes GR (2006) The occluded onset pursuit paradigm: prolonging anticipatory smooth pursuit in the absence of visual feedback. Exp Brain Res 175:11–20PubMedCrossRefGoogle Scholar
  19. Cullen KE, Roy JE (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91:1919–1933. doi: 10.1152/jn.00988.2003 PubMedCrossRefGoogle Scholar
  20. Etchells PJ, Benton CP, Ludwig CJ, Gilchrist ID (2010) The target velocity integration function for saccades. J Vis 10:7PubMedCrossRefGoogle Scholar
  21. Huebner WP, Leigh RJ, Seidman SH, Thomas CW, Billian C, DiScenna AO, Dell’Osso LF (1992a) Experimental tests of a superposition hypothesis to explain the relationship between the vestibulo-ocular reflex and smooth pursuit during combined eye-head tracking in humans. J Neurophysiol 68:1775–1791PubMedGoogle Scholar
  22. Huebner WP, Leigh RJ, Thomas CW (1992b) An adjustment to eye movement measurements that compensated for the eccentric position of the eye relative to the center of the head. J Vestib Res 2:167–173PubMedGoogle Scholar
  23. Kowler E (1989) Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit. Vis Res 29:1049–1057PubMedCrossRefGoogle Scholar
  24. Krauzlis RJ, Lisberger SG (1994) A model of visually-guided smooth pursuit eye movements based on behavioral observations. J Comput Neurosci 1:265–283PubMedCrossRefGoogle Scholar
  25. Krauzlis RJ, Miles FA (1994) Similar changes in the latency of pursuit and saccadic eye movements observed with the “Gap Paradigm”. In: Delgado-Garcia JM (ed) Information processing underlying gaze control. Pergamon Press, Oxford, pp 269–277Google Scholar
  26. Krauzlis RJ, Miles FA (1996) Transitions between pursuit eye movements and fixation in the monkey: dependence on context. J Neurophysiol 76:1622–1638PubMedGoogle Scholar
  27. Lanman J, Bizzi E, Allum J (1978) The coordination of eye and head movement during smooth pursuit. Brain Res 153:39–53PubMedCrossRefGoogle Scholar
  28. Lefevre P, Bottermanne I, Roucoux A (1992) Experimental study and modelling of vestibulo-ocular reflex modulation during large shifts of gaze in humans. Exp Brain Res 91:496–508PubMedCrossRefGoogle Scholar
  29. Lisberger SG, Westbrook LE (1985) Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys. J Neurosci 6:1662–1673Google Scholar
  30. Lisberger SG, Morris EJ, Tychsen L (1987) Visual motion processing and sensory-motor integration for smooth pursuit eye movements. Ann Rev Neurosci 10:97–129PubMedCrossRefGoogle Scholar
  31. Meyer CH, Lasker AG, Robinson DA (1985) The upper limit of human smooth pursuit velocity. Vis Res 25:561–563PubMedCrossRefGoogle Scholar
  32. Mitrani L, Dimitrov G (1978) Pursuit eye movements of a disappearing moving target. Vis Res 18:537–539PubMedCrossRefGoogle Scholar
  33. Orban de Xivry JJ, Bennett SJ, Lefevre PP, Barnes GR (2006) Evidence for synergy between saccades and smooth pursuit during transient target disappearance. J Neurophysiol 95:418–427PubMedCrossRefGoogle Scholar
  34. Osborne LC, Bialek W, Lisberger SG (2004) Time course of information about motion direction in visual area mt of macaque monkeys. J Neurosci 24:3210–3222PubMedCrossRefGoogle Scholar
  35. Rashbass C (1961) The relationship between saccadic and smooth tracking eye movements. J Physiol (Lond) 159:326–338Google Scholar
  36. Robinson DA (1982) A model of cancellation of the vestibulo-ocular reflex. In: Lennerstrand G, Zee DS, Keller EL (eds) Functional basis of ocular motility disorders. Pergamon Press, Oxford, pp 5–13Google Scholar
  37. Robinson DA, Gordon JL, Gordon SE (1986) A model of the smooth pursuit eye movement system. Biol Cybern 55:43–57PubMedCrossRefGoogle Scholar
  38. Roy JE, Cullen KE (2002) Vestibuloocular reflex signal modulation during voluntary and passive head movements. J Neurophysiol 87:2337–2357PubMedGoogle Scholar
  39. Roy JE, Cullen KE (2004) Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci 24:2102–2111. doi: 10.1523/JNEUROSCI.3988-03.2004 PubMedCrossRefGoogle Scholar
  40. Tavassoli A, Ringach DL (2009) Dynamics of Smooth Pursuit Maintenance. J Neurophysiol 102:110–118. doi: 10.1152/jn.91320.2008 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Faculty of Life SciencesUniversity of ManchesterManchesterUK

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