Advertisement

Experimental Brain Research

, Volume 232, Issue 9, pp 2753–2765 | Cite as

Segment interdependency and gaze anchoring during manual two-segment sequences

  • Miya K. Rand
Research Article

Abstract

This study examined two-segment pointing movements with various accuracy constraints to test whether there is segment interdependency in saccadic eye movements that accompany manual actions. The other purpose was to examine how planning of movement accuracy and amplitude for the second pointing influences the timing of gaze shift to the second target at the transition between two segments. Participants performed a rapid two-segment pointing task, in which the first segment had two target sizes, and the second segment had two target sizes and two movement distances. The results showed that duration and peak velocity of the initial pointing were influenced by altered kinematic characteristics of the second pointing due to task manipulations of the second segment, revealing segment interdependency in hand movements. In contrast, saccade duration and velocity did not show such segment interdependency. Thus, unlike hand movements, saccades are planned and organized independently for each segment during sequential manual actions. In terms of the timing of gaze shift to the second target, this was delayed when the initial pointing was made to the smaller first target, indicating that gaze anchoring to the initial target is used to verify the pointing termination. Importantly, the gaze shift was delayed when the second pointing was made to the smaller or farther second target. This suggests that visual information of the hand position at the initial target is important for the planning of movement distance and accuracy of the next pointing. Furthermore, timings of gaze shift and pointing initiation to the second target were highly correlated. Thus, at the transition between two segments, gazes and hand movements are highly coupled in time, which allows the sensorimotor system to process visual and proprioceptive information for the verification of pointing termination and planning of the next pointing.

Keywords

Eye–hand coordination Context dependency Accuracy constraint Saccade Reaching 

Notes

Acknowledgments

This research was supported by Grant Ra 2183/1-1 of the German Research Foundation (DFG). I thank Maia Iobidze for her support in data collection. The author declares no competing financial interests.

References

  1. Abrams R, Meyer D, Kornblum S (1990) Eye–hand coordination: oculomotor control in rapid aimed limb movements. J Exp Psychol Hum Percept Perform 15:248–267CrossRefGoogle Scholar
  2. Adam JJ, Paas FGWC, Eyssen ICJM, Slingerland H, Bekkering H, Drost M (1995) The control of two-element, reciprocal aiming movements: evidence for chunking. Hum Mov Sci 14:1–11CrossRefGoogle Scholar
  3. Adam JJ, Buetti S, Kerzel D (2012) Coordinated flexibility: how initial gaze position modulates eye–hand coordination and reaching. J Exp Psychol Hum Percept Perform 38:891–901PubMedCrossRefGoogle Scholar
  4. Bekkering H, Adam JJ, Kingma H, Huson A, Whiting HTA (1994) Reaction time latencies of eye and hand movements in single- and dual-task conditions. Exp Brain Res 97:471–476PubMedCrossRefGoogle Scholar
  5. Bekkering H, Adam JJ, van den Aarssen A, Kingma H, Whiting HTA (1995) Interference between saccadic eye and goal-directed hand movements. Exp Brain Res 106:475–484PubMedCrossRefGoogle Scholar
  6. Bowman MC, Johansson RS, Flanagan JR (2009) Eye–hand coordination in a sequential target contract task. Exp Brain Res 195:273–283PubMedCrossRefGoogle Scholar
  7. Clark FJ, Horch KW (1986) Kinesthesia. In: Boff KR, Kaufman L, Thomas JP (eds) Handbook of perception and human performance. Sensory processes and perception, vol 1. Wiley, New York, pp 13-1–13-62Google Scholar
  8. Clark FJ, Burgess RC, Chapin JW, Lipscomb WT (1985) Role of intramuscular receptors in the awareness of limb position. J Neurophysiol 54:1529–1540PubMedGoogle Scholar
  9. Collins T, Schicke T, Röder B (2008) Action goal selection and motor planning can be dissociated by tool use. Cognition 109:363–371PubMedCrossRefGoogle Scholar
  10. Crawford JD, Medendorp WP, Marotta JJ (2004) Spatial transformations for eye–hand coordination. J Neurophysiol 92:10–19PubMedCrossRefGoogle Scholar
  11. Desmurget M, Rossetti Y, Prablanc C, Stelmach GE, Jeannerod M (1995) Representation of hand position prior to movement and motor variability. Can J Physiol Pharmacol 73:262–272PubMedGoogle Scholar
  12. Epelboim J (1998) Gaze and retinal-image-stability in two kinds of sequential looking tasks. Vis Res 38:3773–3784PubMedCrossRefGoogle Scholar
  13. Epelboim J, Steinman RM, Kowler E, Pizlo Z, Erkelens CJ, Collewijn H (1997) Gaze-shift dynamics in two kinds of sequential looking tasks. Vis Res 37:2597–2607PubMedCrossRefGoogle Scholar
  14. Fitts PM (1954) The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol 47:381–391PubMedCrossRefGoogle Scholar
  15. Flanagan JR, Johansson RS (2003) Action plans used in action observation. Nature 424:769–771PubMedCrossRefGoogle Scholar
  16. Flanagan JR, Bowman MC, Johansson RS (2006) Control strategies in object manipulation tasks. Curr Opin Neurobiol 16:650–659PubMedCrossRefGoogle Scholar
  17. Gaveau V, Pélisson D, Blangero A, Urquizar C, Prablanc C, Vighetto A, Pisella L (2008) Saccade control and eye–hand coordination in optic ataxia. Neuropsychologia 46:475–486PubMedCrossRefGoogle Scholar
  18. Gielen CCAM, Van den Heuvel PJM, Van Gisbergen JAM (1984) Coordination of fast eye and arm movements in a tracking task. Exp Brain Res 56:156–161CrossRefGoogle Scholar
  19. Hayhoe MM, Shrivastava A, Mruczek R, Pelz JB (2003) Visual memory and motor planning in a natural task. J Vis 3:49–63PubMedCrossRefGoogle Scholar
  20. Heuer H, Hegele M, Rand MK (2013) Age-related variations in the control of electronic tools. In: Schlick C, Frieling E, Wegge J (eds) Age-differentiated work systems. Springer, Heidelberg, pp 369–390CrossRefGoogle Scholar
  21. Johansson RS, Westling G, Bäckström A, Flanagan JR (2001) Eye–hand coordination in object manipulation. J Neurosci 21:6917–6932PubMedGoogle Scholar
  22. Knoblich G, Kircher TTJ (2004) Deceiving oneself about being in control: conscious detection of changes in visuomotor coupling. J Exp Psychol Hum Percept Perform 30:657–666PubMedCrossRefGoogle Scholar
  23. Lünenburger L, Kutz DF, Hoffmann KP (2000) Influence of arm movements on saccades in humans. Eur J Neurosci 12:4107–4116PubMedCrossRefGoogle Scholar
  24. Marteniuk RG, MacKenzie CL, Jeannerod M, Athenes S, Dugas C (1987) Constraints on human arm movement trajectories. Can J Psychol 41:365–378PubMedCrossRefGoogle Scholar
  25. Ma-Wyatt A, Stritzke M, Trommershäuser J (2010) Eye–hand coordination while pointing rapidly under risk. Exp Brain Res 203:131–145PubMedCrossRefGoogle Scholar
  26. McIntyre J, Stratta F, Lacquaniti F (1998) Short-term memory for reaching to visual targets: psychophysical evidence for body-centered reference frames. J Neurosci 18:8423–8435PubMedGoogle Scholar
  27. Müsseler J, Sutter C (2009) Perceiving one’s own movements when using a tool. Conscious Cogn 18:359–365PubMedCrossRefGoogle Scholar
  28. Neggers SFW, Bekkering H (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J Neurophysiol 83:639–651PubMedGoogle Scholar
  29. Paillard J (1982) The contribution of peripheral and central vision to visually guided reaching. In: Ingle D, Goodale M, Mansfield R (eds) Analysis of visual behaviour. MIT Press, Cambridge, pp 367–385Google Scholar
  30. Paillard J, Brouchon M (1968) Active and passive movements in the calibration of position sense. In: Freedman SJ (ed) The neuropsychology of spatially oriented behavior. Dorsey Press, IL, pp 37–55Google Scholar
  31. Paillard J, Brouchon M (1974) A proprioceptive contribution to the spatial encoding of position cues for ballistic movements. Brain Res 71:273–284PubMedGoogle Scholar
  32. Pelz J, Hayhoe M, Loeber R (2001) The coordination of eye, head, and hand movements in a natural task. Exp Brain Res 139:266–277PubMedCrossRefGoogle Scholar
  33. Prablanc C, Echallier JE, Jeannerod M, Komilis E (1979) Optimal response of eye and hand motor systems in pointing at a visual target. Biol Cybern 35:183–187PubMedCrossRefGoogle Scholar
  34. Prablanc C, Pelisson D, Goodale MA (1986) Visual control of reaching movements without vision of the limb. Role of retinal feedback of target position in guiding the hand. Exp Brain Res 62:293–302PubMedCrossRefGoogle Scholar
  35. Pratt J, Shen J, Adam J (2004) The planning and execution of sequential eye movements: saccades do not show the one target advantage. Hum Mov Sci 22:679–688PubMedCrossRefGoogle Scholar
  36. Rand MK, Heuer H (2013) Implicit and explicit representations of hand position in tool use. PLoS One 8:e68471PubMedCentralPubMedCrossRefGoogle Scholar
  37. Rand MK, Shimansky YP (2013) Two-phase strategy of neural control for planar reaching movements. I. XY coordination variability and its relation to end-point variability. Exp Brain Res 225:55–73PubMedCrossRefGoogle Scholar
  38. Rand MK, Stelmach GE (2000) Segment interdependency and difficulty in two-stroke sequences. Exp Brain Res 134:228–236PubMedCrossRefGoogle Scholar
  39. Rand MK, Stelmach GE (2010) Effects of hand termination and accuracy constraint on eye–hand coordination during sequential two-segment movements. Exp Brain Res 207:197–211PubMedCrossRefGoogle Scholar
  40. Rand MK, Stelmach GE (2011) Adaptation of gaze anchoring through practice in young and older adults. Neurosci Lett 492:47–51PubMedCentralPubMedCrossRefGoogle Scholar
  41. Rand MK, Alberts JL, Stelmach GE, Bloedel JR (1997) The influence of movement segment difficulty on movements with two-stroke sequence. Exp Brain Res 115:137–146PubMedCrossRefGoogle Scholar
  42. Rand MK, Van Gemmert AWA, Stelmach GE (2002) Segment difficulty in two-stroke movements in patients with Parkinson’s disease. Exp Brain Res 143:383–393PubMedCrossRefGoogle Scholar
  43. Reed CL, Betz R, Garza JP, Roberts RJ Jr (2010) Grab it! Biased attention in functional hand and tool space. Atten Percept Psychophys 72:236–245PubMedGoogle Scholar
  44. Romero DH, Van Gemmert AW, Adler CH, Bekkering H, Stelmach GE (2003a) Altered aiming movements in Parkinson’s disease patients and elderly adults as a function of delays in movement onset. Exp Brain Res 151:249–261PubMedCrossRefGoogle Scholar
  45. Romero DH, Van Gemmert AW, Adler CH, Bekkering H, Stelmach GE (2003b) Time delays prior to movement alter the drawing kinematics of elderly adults. Hum Mov Sci 22:207–220PubMedCrossRefGoogle Scholar
  46. Rosonbaum DA (1991) Human motor control. Academic Press, San DiegoGoogle Scholar
  47. Rossetti Y, Stelmach G, Desmurget M, Prablanc C, Jeannerod M (1994) The effect of viewing the static hand prior to movement onset on pointing kinematics and variability. Exp Brain Res 101:323–330PubMedCrossRefGoogle Scholar
  48. Sailer U, Flanagan JR, Johansson RS (2005) Eye–hand coordination during learning of a novel visuomotor task. J Neurosci 25:8833–8842PubMedCrossRefGoogle Scholar
  49. Short MW, Fischman MG, Wang YT (1996) Cinematographical analysis of movement pathway constraints in rapid target-striking tasks. J Mot Behav 28:157–163PubMedCrossRefGoogle Scholar
  50. Sidaway B, Sekiya H, Fairweather M (1995) Movement variability as a function accuracy demand in programmed serial aiming responses. J Mot Behav 27:67–76CrossRefGoogle Scholar
  51. Teasdale N, Bard C, Fleury M, Young D, Proteau L (1993) Determining movement onsets from temporal series. J Mot Behav 25:97–106PubMedCrossRefGoogle Scholar
  52. Van Donkelaar P (1997) Eye–hand interactions during goal-directed pointing movements. NeuroReport 8:2139–2142PubMedCrossRefGoogle Scholar
  53. Van Donkelaar P, Lee JH, Drew AS (2000) Transcranial magnetic stimulation disrupts eye–hand interactions in the posterior parietal cortex. J Neurophysiol 84:1677–1680PubMedGoogle Scholar
  54. Vercher JL, Magenes G, Prablanc C, Gauthier GM (1994) Eye–head–hand coordination in pointing at visual targets: spatial and temporal analysis. Exp Brain Res 99:507–523PubMedCrossRefGoogle Scholar
  55. Vesia M, Crawford JD (2012) Specialization of reach function in human posterior parietal cortex. Exp Brain Res 221:1–18PubMedCrossRefGoogle Scholar
  56. Vindras P, Desmurget M, Prablanc C, Viviani P (1998) Pointing errors reflect biases in the perception of the initial hand position. J Neurophysiol 79:3290–3294PubMedGoogle Scholar
  57. Vindras P, Desmurget M, Viviani P (2005) Error parsing in visuomotor pointing reveals independent processing of amplitude and direction. J Neurophysiol 94:1212–1224PubMedCrossRefGoogle Scholar
  58. Weiss P, Stelmach GE, Hefter H (1997) Programming of a movement sequence in Parkinson’s disease. Brain 120:91–102PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Leibniz Research Centre for Working Environment and Human Factors (IfADo)DortmundGermany

Personalised recommendations