Advertisement

Experimental Brain Research

, Volume 195, Issue 2, pp 273–283 | Cite as

Eye–hand coordination in a sequential target contact task

  • Miles C. Bowman
  • Roland S. Johannson
  • John Randall Flanagan
Research Article
First Online:

Abstract

Most object manipulation tasks involve a series of actions demarcated by mechanical contact events, and gaze is typically directed to the locations of these events as the task unfolds. Here, we examined the timing of gaze shifts relative to hand movements in a task in which participants used a handle to contact sequentially five virtual objects located in a horizontal plane. This task was performed both with and without visual feedback of the handle position. We were primarily interested in whether gaze shifts, which in our task shifted from a given object to the next about 100 ms after contact, were predictive or triggered by tactile feedback related to contact. To examine this issue, we included occasional catch contacts where forces simulating contact between the handle and object were removed. In most cases, removing force did not alter the timing of gaze shifts irrespective of whether or not vision of handle position was present. However, in about 30% of the catch contacts, gaze shifts were delayed. This percentage corresponded to the fraction of contacts with force feedback in which gaze shifted more than 130 ms after contact. We conclude that gaze shifts are predictively controlled but timed so that the hand actions around the time of contact are captured in central vision. Furthermore, a mismatch between the expected and actual tactile information related to the contact can lead to a reorganization of gaze behavior for gaze shifts executed greater than 130 ms after a contact event.

Keywords

Eye–hand coordination Object manipulation Visually guided Reaching Sensorimotor control 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This work was supported by the Canadian Institutes of Health Research. MCB was supported by a scholarship from the Natural Sciences and Engineering Research Council of Canada. We thank Martin York for technical support.

References

  1. Akerfelt A, Colonius H, Diederich A (2006) Visual–tactile saccadic inhibition. Exp Brain Res 169:554–563PubMedCrossRefGoogle Scholar
  2. Ballard DH, Hayhoe MM, Li F, Whitehead SD (1992) Hand–eye coordination during sequential tasks. Philos Trans R Soc Lond B Biol Sci 337:331–339PubMedCrossRefGoogle Scholar
  3. Berkinblit MB, Fookson OI, Smetanin B, Adamovich SV, Poizner H (1995) The interaction of visual and proprioceptive inputs in pointing to actual and remembered targets. Exp Brain Res 107:326–330PubMedCrossRefGoogle Scholar
  4. Carlton LG (1981) Processing visual feedback information for movement control. J Exp Psychol Hum Percept Perform 7:1019–1030PubMedCrossRefGoogle Scholar
  5. Crawford JD, Medendorp WP, Marotta JJ (2004) Spatial transformations for eye–hand coordination. J Neurophysiol 92:10–19PubMedCrossRefGoogle Scholar
  6. Cuijpers RH, Smeets JB, Brenner E (2004) On the relation between object shape and grasping kinematics. J Neurophysiol 91:2598–2606PubMedCrossRefGoogle Scholar
  7. Desmurget M, Pelisson D, Rossetti Y, Prablanc C (1998) From eye to hand: planning goal-directed movements. Neurosci Biobehav Rev 22:761–788PubMedCrossRefGoogle Scholar
  8. Epelboim JL, Steinman RM, Kowler E, Edwards M, Pizlo Z, Erkelens CJ, Collewijn H (1995) The function of visual search and memory in sequential looking tasks. Vision Res 35:3401–3422PubMedCrossRefGoogle Scholar
  9. Flanagan JR, Johansson RS (2003) Action plans used in action observation. Nature 424:769–771PubMedCrossRefGoogle Scholar
  10. Flanagan JR, Bowman MC, Johansson RS (2006) Control strategies in object manipulation tasks. Curr Opin Neurobiol 16:650–659PubMedCrossRefGoogle Scholar
  11. Gordon AM, Forssberg H, Johansson RS, Westling G (1991) Integration of sensory information during the programming of precision grip: comments on the contributions of size cues. Exp Brain Res 85:226–229PubMedCrossRefGoogle Scholar
  12. Gribble PL, Everling S, Ford K, Mattar A (2002) Hand–eye coordination for rapid pointing movements: arm movement direction and distance are specified prior to saccade onset. Exp Brain Res 145:372–382PubMedCrossRefGoogle Scholar
  13. Groh JM, Sparks D (1996) Saccades to somatosensory targets. I. Behavioural characteristsics. J Neurophysiol 75:412–427PubMedGoogle Scholar
  14. Hayhoe M, Ballard D (2005) Eye movements in natural behavior. Trends Cogn Sci 9:188–194PubMedCrossRefGoogle Scholar
  15. Jeannerod M (1988) The neural and behavioural organization of goal-directed movements, OUP Psychology Series No 5. Oxford, New YorkGoogle Scholar
  16. Jenmalm P, Johansson RS (1997) Visual and somatosensory information about object shape control manipulative fingertip forces. J Neurosci 17:4486–4499PubMedGoogle Scholar
  17. Jenmalm P, Dahlstedt S, Johansson RS (2000) Visual and tactile information about object curvature control fingertip forces and grasp kinematics in human dexterous manipulation. J Neurophysiol 84:2984–2997PubMedGoogle Scholar
  18. Johansson RS, Birznieks I (2004) First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat Neurosci 7:170–177PubMedCrossRefGoogle Scholar
  19. Johansson RS, Flanagan JR (2007)Tactile sensory control of object manipulation in humans. In: Kass JH, Gardner EP (eds) The senses: a comprehensive reference. Vol 6. Somatosensation. Elsevier, Oxford, pp 67–86Google Scholar
  20. Johansson RS, Westling G (1984) Roles of glabrous skin receptors and sensorimotor memory in automatic-control of precision grip when lifting rougher or more slippery objects. Exp Brain Res 56:550–564PubMedCrossRefGoogle Scholar
  21. Johansson RS, Westling G (1988) Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip. Exp Brain Res 71:59–71PubMedGoogle Scholar
  22. Johansson RS, Westling G, Backstrom A, Flanagan JR (2001) Eye–hand coordination in object manipulation. J Neurosci 21:6917–6932PubMedGoogle Scholar
  23. Kleinholdermann U, Brenner E, Franz VH, Smeets JB (2007) Grasping trapezoidal objects. Exp Brain Res 180:415–420PubMedCrossRefGoogle Scholar
  24. Land M, Mennie N, Rusted J (1999) The roles of vision and eye movements in the control of activities of daily living. Perception 28:1311–1328PubMedCrossRefGoogle Scholar
  25. Neggers SF, Bekkering H (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J Neurophysiol 83:639–651PubMedGoogle Scholar
  26. Neggers SF, Bekkering H (2001) Gaze anchoring to a pointing target is present during the entire pointing movement and is driven by a non-visual signal. J Neurophysiol 86:961–970PubMedGoogle Scholar
  27. Paillard J (1996) Fast and slow feedback loops for the visual correction of spatial errors in a pointing task: a reappraisal. Can J Physiol Pharmacol 74:401–417PubMedCrossRefGoogle Scholar
  28. Prablanc C, Martin O (1992) Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67:455–469PubMedGoogle Scholar
  29. Prablanc C, Echallier JF, Komilis E, Jeannerod M (1979) Optimal response of eye and hand motor systems in pointing at a visual target. I. Spatio-temporal characteristics of eye and hand movements and their relationships when varying the amount of visual information. Biol Cybern 35:113–124PubMedCrossRefGoogle Scholar
  30. Prablanc C, Pelisson D, Goodale MA (1986) Visual control of reaching movements without vision of the limb.1. Role of retinal feedback of target position in guiding the hand. Exp Brain Res 62:293–302PubMedCrossRefGoogle Scholar
  31. Prablanc C, Desmurget M, Grea H (2003) Neural control of on-line guidance of hand-reaching movements. Prog Brain Res 142:155–170PubMedCrossRefGoogle Scholar
  32. Sarlegna F, Blouin J, Vercher JL, Bresciani JP, Bourdin C, Gauthier GM (2004) Online control of the direction of rapid reaching movements. Exp Brain Res 157:468–471PubMedCrossRefGoogle Scholar
  33. Saunders JA, Knill DC (2004) Visual feedback control of hand movements. J Neurosci 24:3223–3234PubMedCrossRefGoogle Scholar
  34. Smeets JB, Brenner E (1999) A new view on grasping. Motor Control 3:237–271PubMedGoogle Scholar
  35. Smeets JB, Brenner E (2001) Independent movements of the digits in grasping. Exp Brain Res 139:92–100PubMedCrossRefGoogle Scholar
  36. Wolpert DM, Flanagan JR (2001) Motor prediction. Curr Biol 11:R729–R732PubMedCrossRefGoogle Scholar
  37. Wolpert DM, Ghahramani Z (2000) Computational principles of movement neuroscience. Nat Neurosci 3(Suppl):1212–1217PubMedCrossRefGoogle Scholar
  38. Wolpert DM, Ghahramani Z, Flanagan JR (2001) Perspectives and problems in motor learning. Trends Cogn Sci 5:487–494PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Miles C. Bowman
    • 1
  • Roland S. Johannson
    • 2
  • John Randall Flanagan
    • 1
  1. 1.Centre for Neuroscience Studies and Department of PsychologyQueen’s UniversityKingstonCanada
  2. 2.Section for Physiology, Department of Integrative Medical BiologyUmeå UniversityUmeåSweden

Personalised recommendations

Cite article

Buy options