Experimental Brain Research

, Volume 99, Issue 3, pp 507–523

Eye-head-hand coordination in pointing at visual targets: spatial and temporal analysis

  • J. L. Vercher
  • G. Magenes
  • C. Prablanc
  • G. M. Gauthier
Original Paper

Abstract

This study investigated whether the execution of an accurate pointing response depends on a prior saccade orientation towards the target, independent of the vision of the limb. A comparison was made between the accuracy of sequential responses (in which the starting position of the hand is known and the eye centred on the target prior to the onset of the hand pointing movement) and synergetic responses (where both hand and gaze motions are simultaneously initiated on the basis of unique peripheral retinal information). The experiments were conducted in visual closed-loop (hand visible during the pointing movement) and in visual openloop conditions (vision of hand interrupted as the hand started to move). The latter condition eliminated the possibility of a direct visual evaluation of the error between hand and target during pointing. Three main observations were derived from the present work: (a) the timing of coordinated eye-head-hand pointing at visual targets can be modified, depending on the executed task, without a deterioration in the accuracy of hand pointing; (b) mechanical constraints or instructions such as preventing eye, head or trunk motion, which limit the redundancy of degrees of freedom, lead to a decrease in accuracy; (c) the synergetic movement of eye, head and hand for pointing at a visible target is not trivially the superposition of eye and head shifts added to hand pointing. Indeed, the strategy of such a coordinated action can modify the kinematics of the head in order to make the movements of both head and hand terminate at approximately the same time. The main conclusion is that eye-head coordination is carried out optimally by a parallel processing in which both gaze and hand motor responses are initiated on the basis of a poorly defined retinal signal. The accuracy in hand pointing is not conditioned by head movement per se and does not depend on the relative timing of eye, head and hand movements (synergetic vs sequential responses). However, a decrease in the accuracy of hand pointing was observed in the synergetic condition, when target fixation was not stabilised before the target was extinguished. This suggests that when the orienting saccade reaches the target before hand movement onset, visual updating of the hand motor control signal may occur. A rapid processing of this final input allows a sharper redefinition of the hand landing point.

Key words

Visuomanual pointing Eye-head-hand coordination Visual direction coding Human 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bahill AT, Clark MR, Stark L (1975) The main sequence. A tool for studying human eye movements. Math Biosci 24:191–204CrossRefGoogle Scholar
  2. Bahill AT, Stark L (1979) The trajectories of saccadic eye movements. Sci Am 240:108–117Google Scholar
  3. Bahill AT, Brockenbrough A, Troost BT (1981) Variability and development of a normative data base for saccadic eye movements. Invest Ophthalmol Vis Sci 21:116–125Google Scholar
  4. Bard C, Paillard J, Fleury M, Hay L, Larue J (1990) Positional versus directional control loops in visuomotor pointing. Eur Bull Cognitive Psychol 10:145–156Google Scholar
  5. Beaubaton D, Hay L (1986) Contribution of visual information to feedforward and feedback processes in rapid pointing movements. Hum Mov Sci 5:19–34Google Scholar
  6. Biguer B, Jeannerod M, Prablanc C (1982) The coordination of eye, head, and arm movements during reaching at a single visual target. Exp Brain Res 46:301–304Google Scholar
  7. Biguer B, Prablanc C, Jeannerod M (1984) The contribution of coordinated eye and head movements in hand pointing accuracy. Exp Brain Res 55:462–469Google Scholar
  8. Biguer B, Donaldson IM, Hein A, Jeannerod M (1988) Neck muscle vibration modifies the representation of visual motion and direction in man. Brain 111:1405–1424Google Scholar
  9. Bizzi E, Kalil RE, Morasso P, Tagliasco V (1972) Central programming and peripheral feedback during eye-head coordination in monkeys. Bibl Ophthalmol 82:220–232Google Scholar
  10. Bizzi E, Polit A, Morasso P (1976) Mechanisms underlying achievement of final head position. J Neurophysiol 39:435–443Google Scholar
  11. Blouin J, Bard C, Teasdale N, Paillard J, Fleury M, Forget R, Lamarre Y (1993a) Reference systems for coding spatial information in normal subjects and a deafferented patient. Exp Brain Res 93:324–331Google Scholar
  12. Blouin J, Teasdale N, Bard C, Fleury M (1993b) Directional control of rapid arm movements: the role of kinetic visual feedback system. Can J Exp Psychol 47:678–696Google Scholar
  13. Bridgeman B, Stark L (1991) Ocular proprioception and efference copy in registering visual direction. Vision Res 31:1903–1913CrossRefPubMedGoogle Scholar
  14. Brindley GS, Goodwin GM, Kulikowski JJ, Leghton D (1976) Stability of vision with a paralysed eye. J Physiol (Lond) 258:65–66Google Scholar
  15. Carlton LG (1981) Processing visual feedback information for movement control. J Exp Psychol Hum Percept Perform 7:1019–1030Google Scholar
  16. Carnahan H, Marteniuk RG (1991) The temporal organization of hand, eye, and head movements during reaching and pointing. J Mot Behav 23 (2):109–119Google Scholar
  17. Elliot D, Allard F (1985) The utilization of visual feedback information during rapid pointing movements. Q J Exp Psychol [A] 37:407–425Google Scholar
  18. Fitts PM (1954) The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol 47:381–391PubMedGoogle Scholar
  19. Flanagan JR, Feldman AG, Ostry DA (1991) Equilibrium control vectors subserving rapid goal-directed arm movements. In: Requin J, Stelmach GE (eds) Tutorials in motor neuroscience. Kluwer Academic Publishers, The Netherlands, pp 357–367Google Scholar
  20. Flash T, Henis E (1991) Arm trajectory modifications during reaching towards visual targets. J Cognitive Neurosci 3:220–230Google Scholar
  21. Gandevia SC (1982) The perception of motor commands or effort during muscular paralysis. Brain 105:151–159Google Scholar
  22. Gauthier GM, Nommay D, Vercher JL (1990a) The role of ocular muscle proprioception in visual localization of targets. Science 249:58–61Google Scholar
  23. Gauthier GM, Nommay D, Vercher JL (1990b) Ocular muscle proprioception and visual localization of targets in man. Brain 113:1857–1871Google Scholar
  24. Georgopoulos AP, Kalaska JF, Massey JT (1981) Spatial trajectories and reaction times of aimed movements: effects of practice, uncertainty and change in target location. J Neurophysiol 46:725–743Google Scholar
  25. Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15:20–25CrossRefPubMedGoogle Scholar
  26. Ghez C, Gordon J, Ghilardi MF, Christakos CN, Cooper SE (1990) Roles of proprioceptive input in the programming of arm trajectories. Cold Spring Harb Symp Quant Biol 55:837–847Google Scholar
  27. Guitton D, Volle M (1987) Gaze control in human: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. J Neurophysiol 58:427–459PubMedGoogle Scholar
  28. Guthrie BL, Porter JD, Sparks DL (1983) Corollary discharge provides accurate eye position information to the oculomotor system. Science 221:1193–1195Google Scholar
  29. Hoff B, Arbib MA (1992) A model of the speed-accuracy and perturbation on visually guided reaching. In Caminiti R, Johnson PB, Burnod Y (eds) Control of arm movement in space. Neurophysiological and computational approaches. (Exp Brain Res series, vol 22) Springer, Berlin, Heidelberg, New York, pp 285–306Google Scholar
  30. Holst E von, Mittelstaed H (1980) The reafference principle. In: Gallistel CR (eds) The organization of action. New York, Wiley, pp 176–209Google Scholar
  31. Jeannerod M (1986) Are corrections in accurate arm movements corrective? Prog Brain Res 64:353–360Google Scholar
  32. Jeannerod M (1991) The interaction of visual and proprioceptive cues in controlling reaching movements. In: Humphrey DR, Freund HJ (eds) Motor control: concepts and issues. Wiley, New York, pp 277–291Google Scholar
  33. Jürgens R, Becker W, Kornhuber HH (1981) Natural and drug-induced variations of velocity and duration of human saccadic eye movements: evidence for a control of the neural pulse generator by local feedback. Biol Cybern 39:87–96PubMedGoogle Scholar
  34. Keele SW (1981) Behavioural analysis of movement. In: Brooks VB (eds) Motor Control. (Handbook of physiology, sect 1, The nervous system, vol II) Am Physiol Soc, Washington DC, pp 1391–1414Google Scholar
  35. Laurutis VP, Robinson DA (1986) The vestibulo-ocular reflex during human saccadic eye movements. J Physiol (Lond) 373:209–233Google Scholar
  36. Matin L (1982) Visual localization and eye movements. In: Wertheim AH, Wagenaar WA, Leibowitz HW (eds) Tutorials on motion perception. Plenum, New-York, pp 101–156Google Scholar
  37. Merton PA (1964) Absence of conscious position sense in the human eyes. In: Bender MB (eds) The oculomotor system. Harper and Row, New-York, pp 314–320Google Scholar
  38. Paillard J (1982) The contribution of peripheral and central vision to visually guided reaching. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT press, Cambridge, Mass., pp 367–385Google Scholar
  39. Paulignan Y, MacKenzie C, Marteniuk R, Jeannerod M (1990) The coupling of arm and finger movements during prehension. Exp Brain Res 79:431–435Google Scholar
  40. Pelisson D, Prablanc C (1988) Kinematics of centrifugal and centripetal saccadic eye movements in Man. Vision Res 28:87–94Google Scholar
  41. Pelisson D, Prablanc C, Goodale MA, Jeannerod M (1986) Visual control of reaching movements without vision of the limb. II. Evidence of fast unconscious processes correcting the trajectory of the hand to the final position of a double step stimulus. Exp Brain Res 62:303–311PubMedGoogle Scholar
  42. Pelisson D, Prablanc C, Urquizar C (1988) Vestibuloocular reflex inhibition and gaze saccade control characteristics during eye- head orientation in humans. J Neurophysiol 59:997–1013Google Scholar
  43. Polit A, Bizzi E (1979) Characteristics of motor programming underlying arm movements in monkeys. J Neurophysiol 42 (1): 183–194Google Scholar
  44. Prablanc C, Jeannerod M (1974) Latence et précision des saccades en fonction de l'intensité, de la durée et de la position rétinienne d'un stimulus. Rev EEG (Paris) 4 (j3): 484–488Google Scholar
  45. Prablanc C, Martin O (1992) Automatic control during hand reaching at undetected twodimensional target displacements. J Neurophysiol 67 (2): 455–469Google Scholar
  46. Prablanc C, Echallier JF, Komilis E, Jeannerod M (1979) Optimal response of eye and hand motor systems in pointing at a visual target. Biol Cybern 35:113–124Google Scholar
  47. Prablanc C, Pelisson D, Goodale MA (1986a) Visual control of reaching movements without vision of the limb. I. Role of retinal feedback of target position in guiding the hand. Exp Brain Res 62:293–302Google Scholar
  48. Prablanc C, Bailly C, Pelisson D (1986b) Etude des mouvements oculaires chez l'Homme par la technique electro-oculographique. Bull Soc Ophtalmol Fr 12:1447–1452Google Scholar
  49. Rollero R, Ouaknine M, Vercher JL, Semmlow JL, Gauthier GM (1990) Ultrasonic two axis rotation detector. IEEE Trans Biomed Eng 37 (3): 450–457Google Scholar
  50. Schmid R, Zambarbieri D (1991) Strategies of eye-head coordination. In: Schmid R, Zambarbieri D (eds) Oculomotor control and cognitive processes: normal and pathological aspects. Elsevier, Amsterdam, pp 229–246Google Scholar
  51. Schmidt RA (1988) Motor control and learning, a behavioral emphasis. Human Kinetics, Champaign, ILGoogle Scholar
  52. Sherrington CS (1918) Observations of the sensual role of the proprioceptive nerve-supply of the extrinsic ocular muscles. Brain 41:332–342PubMedGoogle Scholar
  53. Soechting JF (1984) Effect of target size on spatial and temporal characteristics of a pointing movement in man. Exp Brain Res 54:121–132PubMedGoogle Scholar
  54. Soechting JF, Lacquaniti F (1983) Modification of trajectory of a pointing movement in response to a change in target location. J Neurophysiol 49:548–564Google Scholar
  55. Sperry RW (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol 43:482–489Google Scholar
  56. Von Helmoltz HLF (1867) Optique physiologique. Massion, ParisGoogle Scholar
  57. Whitaker D, Mäkela P, Rovamo J, Latham K (1992) The influence of eccentricity on position and movement acuities as revealed by spatial scaling. Vision Res 32 (10): 1913–1930Google Scholar
  58. Woodworth RS (1899) The accuracy of voluntary movements. Psychol Rev Monogr [Suppl 3]Google Scholar
  59. Zangemeister WH, Stark L (1982) Types of gaze movement: variable interactions of eye and head movements. Exp Neurol 77:563–577Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • J. L. Vercher
    • 1
  • G. Magenes
    • 2
  • C. Prablanc
    • 3
  • G. M. Gauthier
    • 1
  1. 1.Laboratoire de Contrôles Sensorimoteurs, Université de ProvenceMarseille cedex 20France
  2. 2.Dipartimento di Informatica e SistemisticaUniversità di PaviaPaviaItaly
  3. 3.Laboratoire Vision et Motricité, INSERM U-94BronFrance

Personalised recommendations