Skip to main content
SpringerLink
Log in

Comparing limb proprioception and oculomotor signals during hand-guided saccades

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We previously showed that saccades tend to overshoot briefly flashed targets that were manually displaced in the dark (Ren et al. 2006). However it was not clear if the overshoot originated from a sensory error in measuring hand displacement or from a premotor error in saccade programming, because gaze and hand position started at the same central position. Here, we tested between these hypotheses by dissociating the initial eye and hand position. Five hand/target positions (center, far, near, right, left) on a frontally-placed horizontal surface were used in four paradigms: Center or Peripheral Eye-hand Association (CA or PA, both gaze and right hand started from the center or a same peripheral location) and Hand or Eye Dissociation (HD or ED, hand or gaze started from one of three non-target peripheral locations). Subjects never received any visual feedback about the final target location and the subjects’ hand displacement. In the CA paradigm, subjects showed the same overshoot that we showed previously. However, changing both initial eye and hand positions relative to the final target (PA) affected the pattern, significantly altering the directions of overshoots. Changing only the initial position of hand (HD) did not have this effect, whereas changing only initial eye position (ED) had the same effect as the PA condition (CA ≈ HD, PA ≈ ED). Furthermore, multiple regression analysis showed that the direction of the ideal saccade contributed significantly to the endpoint direction error, not the direction of the hand path. These results suggest that these errors do not primarily arise from misestimates of the hand trajectory, but rather from a process of comparing the initial eye position and the limb proprioceptive signal during saccade programming.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abrams RA, Meyer DE, Kornblum S (1990) Eye-hand coordination: oculomotor control in rapid aimed limb movements. J Exp Psychol Hum Percept Perform 16(2):248–267

    Article  PubMed  CAS  Google Scholar 

  • Andersen RA, Buneo CA (2002) Intentional maps in posterior parietal cortex. Annu Rev Neurosci 25:189–220

    Article  PubMed  CAS  Google Scholar 

  • Batista AP, Buneo CA, Snyder LH, Andersen RA (1999) Reach plans in eye-centered coordinates. Science 285(5425):257–260

    Article  PubMed  CAS  Google Scholar 

  • Buneo CA, Jarvis MR, Batista AP, Andersen RA (2002) Direct visuomotor transformations for reaching. Nature 416(6881):632–636

    Article  PubMed  CAS  Google Scholar 

  • Clark FJ (1992) How accurately can we perceive the positions of our limbs? Behav Brain Sci 15:725–726

    Google Scholar 

  • Clark FJ, Larwood KJ, Davis ME, Deffenbacher KA (1995) A metric for assessing acuity in positioning joints and limbs. Exp Brain Res 107:73–79

    Article  PubMed  CAS  Google Scholar 

  • Colby CL, Duhamel JR, Goldberg ME (1995) Oculocentric spatial representation in parietal cortex. Cereb Cortex 5:470–481

    Article  PubMed  CAS  Google Scholar 

  • Deubel H (1987) Adaptivity of gain and direction in oblique saccades. In: O’Regan J, Levy-Schoen A (eds) Eye movements: from physiology to cognition. Elsevier, Amsterdam, pp 181–190

    Google Scholar 

  • Dickinson AR, Calton JL, Snyder LH (2003) Nonspatial saccade-specific activation in area LIP of monkey parietal cortex. J Neurophysiol 90(4):2460–2464

    Article  PubMed  CAS  Google Scholar 

  • Duhamel JR, Colby CL, Goldberg ME (1992) The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255(5040):90–92

    Article  PubMed  CAS  Google Scholar 

  • Flanagan JR, Johansson RS (2003) Action plans used in action observation. Nature 424(6950):769–771

    Article  PubMed  CAS  Google Scholar 

  • Heide W, Binkofski F, Seitz RJ, Posse S, Nitschke MF, Freund HJ, Kompf D (2001) Activation of frontoparietal cortices during memorized triple-step sequences of saccadic eye movements: an fMRI study. Eur J Neurosci 13(6):1177–1189

    Article  PubMed  CAS  Google Scholar 

  • Helsen WF, Elliott D, Starkes JL, Ricker KL (2000) Coupling of eye, finger, elbow, and shoulder movements during manual aiming. J Mot Behav 32(3):241–248

    Article  PubMed  CAS  Google Scholar 

  • Henriques DYP, Crawford JD (2001) Testing the three-dimensional reference frame transformation for express and memory-guided saccades. Neurocomputing 38–40:1267–1280

    Article  Google Scholar 

  • Henriques DY, Klier EM, Smith MA, Lowy D, Crawford JD (1998) Gaze-centered remapping of remembered visual space in an open-loop pointing task. J Neurosci 18(4):1583–1594

    PubMed  CAS  Google Scholar 

  • Hogan N (1985) The mechanics of multi-joint posture and movement control. Biol Cybern 52:315–331

    Article  PubMed  CAS  Google Scholar 

  • Johansson RS, Westling G, Backstrom A, Flanagan JR (2001) Eye-hand coordination in object manipulation. J Neurosci 21(17):6917–6932

    PubMed  CAS  Google Scholar 

  • Medendorp WP, Goltz HC, Vilis T, Crawford JD (2003) Gaze-centered updating of visual space in human parietal cortex. J Neurosci 23(15):6209–6214

    PubMed  CAS  Google Scholar 

  • Nakamura K, Colby CL (2002) Updating of the visual representation in monkey striate and extrastriate cortex during saccades. Proc Natl Acad Sci USA 99(6):4026–4031

    Article  PubMed  CAS  Google Scholar 

  • Nanayakkara T, Shadmehr R (2003) Saccade adaptation in response to altered arm dynamics. J Neurophysiol 90(6):4016–4021

    Article  PubMed  Google Scholar 

  • Neggers SF, Bekkering H (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J Neurophysiol 83(2):639–651

    PubMed  CAS  Google Scholar 

  • 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(2):961–970

    PubMed  CAS  Google Scholar 

  • Ren L, Khan AZ, Blohm G, Henriques DYP, Sergio LE, Crawford JD (2006) Proprioceptive guidance of saccades in eye-hand coordination. J Neurophysiol 96:1464–1477

    Article  PubMed  CAS  Google Scholar 

  • Sabes PN, Jordan MI, Wolpert DM (1998) The role of inertial sensitivity in motor planning. J Neurosci 18(15):5948–5957

    PubMed  CAS  Google Scholar 

  • Scheidt RA, Conditt MA, Secco EL, Mussa-Ivaldi FA (2005) Interaction of visual and proprioceptive feedback during adaptation of human reaching movements. J Neurophysiol 93(6):3200–3213

    Article  PubMed  Google Scholar 

  • Scott SH, Loeb GE (1994) The computation of position sense from spindles in mono- and multiarticular muscles. J Neurosci 14:7529–7540

    PubMed  CAS  Google Scholar 

  • Snyder LH, Batista AP, Andersen RA (1997) Coding of intention in the posterior parietal cortex. Nature 386(6621):167–170

    Article  PubMed  CAS  Google Scholar 

  • Soechtinge JF, Buneo CA, Herrmann U, Flanders M (1995) Moving effortlessly in three dimensions: does Donders’ law apply to arm movement? J Neurosci 15(9):6271–6280

    Google Scholar 

  • Tweed D, Cadera W, Vilis T (1990) Computing three-dimensional eye position quaternions and eye velocity from search coil signals. Vision Res 30(1):97–110

    Article  PubMed  CAS  Google Scholar 

  • Van Beers RJ, Sittig AC, Denier van der Gon JJ (1998) The precision of proprioceptive position sense. Exp Brain Res 122:367–377

    Article  PubMed  Google Scholar 

  • Van Opstal AJ, van Gisbergen JA (1990) Role of monkey superior colliculus in saccade averaging. Exp Brain Res 79:143–149

    PubMed  Google Scholar 

  • Vercher JL, Quaccia D, Gauthier GM (1995) Oculo-manual coordination control: respective role of visual and non-visual information in ocular tracking of self-moved targets. Exp Brain Res 103:311–322

    Article  PubMed  CAS  Google Scholar 

  • White JM, Sparks DL, Stanford TR (1994) Saccades to remembered target locations: an analysis of systematic and variable errors. Vision Res 34(1):79–92

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank S. Sun and H. Wang for technical support. This work was supported by the Canadian Institutes of Health Research (CIHR). LR was supported by Ontario Graduate Scholarship, GB was supported by a Marie Curie International fellowship within the 6th European Community Framework Program and CIHR (Canada), and JDC holds a Canada Research Chair.

Author information

Authors and Affiliations

  1. Centre for Vision Research, York University, Rm. 0003C, Computer Science and Engineering Bldg, 4700 Keele Street, M3J 1P3, Toronto, ON, Canada

    L. Ren, G. Blohm & J. D. Crawford

  2. Departments of Kinesiology and Health Science, York University, 4700 Keele Street, M3J 1P3, Toronto, ON, Canada

    L. Ren & J. D. Crawford

Authors
  1. L. Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Blohm
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. D. Crawford
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Ren.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ren, L., Blohm, G. & Crawford, J.D. Comparing limb proprioception and oculomotor signals during hand-guided saccades. Exp Brain Res 182, 189–198 (2007). https://doi.org/10.1007/s00221-007-0981-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-007-0981-5

Keywords

Search

Navigation