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Experimental Brain Research

, Volume 195, Issue 4, pp 611–620 | Cite as

Manual and oculomotor performance develop contemporaneously but independently during continuous tracking

  • Eric D. Vidoni
  • Jason S. McCarley
  • Jodi D. Edwards
  • Lara A. Boyd
Research Article

Abstract

The coordination of the oculomotor and manual effector systems is an important component of daily motor behavior. Previous work has primarily examined oculomotor/manual coordination in discrete targeting tasks. Here we extend this work to learning a tracking task that requires continuous response and movement update. Over two sessions, participants practiced controlling a computer mouse with movements of their arm to follow a target moving in a repeated sequence. Eye movements were also recorded. In a retention test, participants demonstrated sequence-specific learning with both effector systems, but differences between effectors also were apparent. Time series analysis and multiple linear regression were employed to probe spatial and temporal contributions to overall tracking accuracy within each effector system. Sequence-specific oculomotor learning occurred only in the spatial domain. By contrast, sequence-specific learning at the arm was evident only in the temporal domain. There was minimal interdependence in error rates for the two effector systems, underscoring their independence during tracking. These findings suggest that the oculomotor and manual systems learn contemporaneously, but performance improvements manifest differently and rely on different elements of motor execution. The results may in part be a function of what the motor learning system values for each effector as a function of its effector’s inertial properties.

Keywords

Visual motor coordination Learning Motor skills 

Notes

Acknowledgments

We appreciate the helpful comments of Jeff Radel and Robyn Honea and the thoughtful and constructive reviewers of the manuscript. Funding was provided by start-up monies from the University of Kansas Medical Center awarded to LAB.

References

  1. Aron A, Aron EA (1999) Statistics for psychology. Prentice-Hall, Upper Saddle RiverGoogle Scholar
  2. Barnes GR, Schmid AM (2002) Sequence learning in human ocular smooth pursuit. Exp Brain Res 144:322–335PubMedCrossRefGoogle Scholar
  3. Binsted G, Elliott D (1999) Ocular perturbations and retinal/extraretinal information: the coordination of saccadic and manual movements. Exp Brain Res 127:193–206PubMedCrossRefGoogle Scholar
  4. Boyd LA, Winstein CJ (2004) Cerebellar stroke impairs temporal but not spatial accuracy during implicit motor learning. Neurorehabil Neural Rep 18:134–143CrossRefGoogle Scholar
  5. Burke MR, Barnes GR (2007) Sequence learning in two-dimensional smooth pursuit eye movements in humans. J Vis 7:5PubMedCrossRefGoogle Scholar
  6. Day BL, Marsden CD (1982) Two strategies for learning a visually guided motor task. Percept Mot Skills 55:1003–1016PubMedGoogle 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 J, Steinman RM, Kowler E, Pizlo Z, Erkelens CJ, Collewijn H (1997) Gaze-shift dynamics in two kinds of sequential looking tasks. Vision Res 37:2597–2607PubMedCrossRefGoogle Scholar
  9. Gordon J, Ghilardi MF, Cooper SE, Ghez C (1994) Accuracy of planar reaching movements. II. Systematic extent errors resulting from inertial anisotropy. Exp Brain Res 99:112–130PubMedCrossRefGoogle Scholar
  10. Hatada Y, Rossetti Y, Miall RC (2006) Long-lasting aftereffect of a single prism adaptation: shifts in vision and proprioception are independent. Exp Brain Res 173:415–424PubMedCrossRefGoogle Scholar
  11. Helsen WF, Elliott D, Starkes JL, Ricker KL (2000) Coupling of eye, finger, elbow and shoulder movements during manual aiming. J Mot Behav 32:241–248PubMedGoogle Scholar
  12. Helsen WF, Tremblay L, Van den Berg M, Elliott D (2004) The Role of oculomotor information in the learning of sequential aiming movements. J Mot Behav 36:82–90PubMedCrossRefGoogle Scholar
  13. Hikosaka O, Rand MK, Miyachi S, Miyashita K (1995) Learning of sequential movements in the monkey: process of learning and retention of memory. J Neurophysiol 74:1652–1661PubMedGoogle Scholar
  14. Hirata C, Yoshida S (2000) Visual dominance in amending the directional parameter of feedforward control. J Mot Behav 32:17–25PubMedCrossRefGoogle Scholar
  15. Johansson RS, Westling G, Backstrom A, Flanagan JR (2001) Eye-hand coordination in object manipulation. J Neurosci 21:6917–6932PubMedGoogle Scholar
  16. Kowler E, Steinman RM (1979a) The effect of expectations on slow oculomotor control. I. Periodic target steps. Vision Res 19:619–632PubMedCrossRefGoogle Scholar
  17. Kowler E, Steinman RM (1979b) The effect of expectations on slow oculomotor control. II. Single target displacements. Vision Res 19:633–646PubMedCrossRefGoogle Scholar
  18. Kowler E, Steinman RM (1981) Th effect of expectations on slow oculomotor control. III. Guessing unpredictable target displacements. Vision Res 21:191–203PubMedCrossRefGoogle Scholar
  19. Kowler E, Martins AJ, Pavel M (1984) The effect of expectations on slow oculomotor control. IV. Anticipatory smooth eye movements depend on prior target motions. Vision Res 24:197–210PubMedCrossRefGoogle Scholar
  20. Land MF, Hayhoe M (2001) In what ways do eye movements contribute to everyday activities? Vision Res 41:3559–3565PubMedCrossRefGoogle Scholar
  21. Lateiner JE, Sainburg RL (2003) Differential contributions of vision and proprioception to movement accuracy. Exp Brain Res 151:446–454PubMedCrossRefGoogle Scholar
  22. Lazzari S, Vercher JL, Buizza A (1997) Manuo-ocular coordination in target tracking. I. A model simulating human performance. Biol Cybern 77:257–266PubMedCrossRefGoogle Scholar
  23. Leigh JR, Zee DS (2006) The neurology of eye movement. Oxford University Press, New YorkGoogle Scholar
  24. Mackrous I, Proteau L (2007) Specificity of practice results from differences in movement planning strategies. Exp Brain Res 183:181–193PubMedCrossRefGoogle Scholar
  25. Marcus DJ, Karatekin C, Markiewicz S (2006) Oculomotor evidence of sequence learning on the serial reaction time task. Mem Cognit 34:420–432PubMedGoogle Scholar
  26. McHugh DE, Bahill AT (1985) Learning to track predictable target waveforms without a time delay. Invest Ophthalmol Vis Sci 26:932–937PubMedGoogle Scholar
  27. Miall RC, Jenkinson EW (2005) Functional imaging of changes in cerebellar activity related to learning during a novel eye-hand tracking task. Exp Brain Res 166:170–183PubMedCrossRefGoogle Scholar
  28. Miall RC, Reckess GZ, Imamizu H (2001) The cerebellum coordinates eye and hand tracking movements. Nat Neurosci 4:638–644PubMedCrossRefGoogle Scholar
  29. Miyashita K, Rand MK, Miyachi S, Hikosaka O (1996) Anticipatory saccades in sequential procedural learning in monkeys. J Neurophysiol 76:1361–1366PubMedGoogle Scholar
  30. Pew RW (1974) Levels of analysis in motor control. Brain Res 71:393–400PubMedCrossRefGoogle Scholar
  31. Ren L, Khan AZ, Blohm G, Henriques DY, Sergio LE, Crawford JD (2006) Proprioceptive guidance of saccades in eye-hand coordination. J Neurophysiol 96:1464–1477PubMedCrossRefGoogle Scholar
  32. Sailer U, Flanagan JR, Johansson RS (2005) Eye-hand coordination during learning of a novel visuomotor task. J Neurosci 25:8833–8842PubMedCrossRefGoogle Scholar
  33. Salmoni AW, Schmidt RA, Walter CB (1984) Knowledge of results and motor learning: a review and critical reappraisal. Psychol Bull 95:355–386PubMedCrossRefGoogle Scholar
  34. Schmidt RA, Lee TD (1999) Motor control and learning: a behavioral approach. Human Kinetics, ChampaignGoogle Scholar
  35. Shea CH, Park JH, Braden HW (2006) Age-related effects in sequential motor learning. Phys Ther 86:478–488PubMedGoogle Scholar
  36. S-R Research Ltd (2006) Eyelink II Users Manual V 2.12Google Scholar
  37. Starkes J, Helsen W, Elliott D (2002) A menage a trois: the eye, the hand and on-line processing. J Sports Sci 20:217–224PubMedCrossRefGoogle Scholar
  38. van Donkelaar P (1997) Eye–hand interactions during goal-directed pointing movements. Neuroreport 8:2139–2142PubMedCrossRefGoogle Scholar
  39. Vaziri S, Diedrichsen J, Shadmehr R (2006) Why does the brain predict sensory consequences of oculomotor commands? Optimal integration of the predicted and the actual sensory feedback. J Neurosci 26:4188–4197PubMedCrossRefGoogle Scholar
  40. Vercher JL, Lazzari S, Gauthier G (1997) Manuo-ocular coordination in target tracking. II. Comparing the model with human behavior. Biol Cybern 77:267–275PubMedCrossRefGoogle Scholar
  41. Vidoni ED, Boyd LA (2008) Motor sequence learning occurs despite disrupted visual and proprioceptive feedback. Behav Brain Funct 4:32PubMedCrossRefGoogle Scholar
  42. Wulf G, Schmidt RA (1997) Variability of practice and implicit motor learning. J Exp Psychol Learn Mem Cogn 23:987–1006CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Eric D. Vidoni
    • 1
  • Jason S. McCarley
    • 2
  • Jodi D. Edwards
    • 3
  • Lara A. Boyd
    • 4
  1. 1.Department of NeurologyUniversity of Kansas Medical CenterKansas CityUSA
  2. 2.2251 Beckman Institute University of Illinois, Urbana-ChampaignUrbanaUSA
  3. 3.Graduate Program in EpidemiologyUniversity of British ColumbiaVancouverCanada
  4. 4.Department of Physical Therapy and Brain Research CentreUniversity of British ColumbiaVancouverCanada

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