Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Serial linkage of target selection for orienting and tracking eye movements

Nature Neuroscience volume 5, pages 892–899 (2002)Cite this article

Abstract

Many natural actions require the coordination of two different kinds of movements. How are targets chosen under these circumstances: do central commands instruct different movement systems in parallel, or does the execution of one movement activate a serial chain that automatically chooses targets for the other movement? We examined a natural eye tracking action that consists of orienting saccades and tracking smooth pursuit eye movements, and found strong physiological evidence for a serial strategy. Monkeys chose freely between two identical spots that appeared at different sites in the visual field and moved in orthogonal directions. If a saccade was evoked to one of the moving targets by microstimulation in either the frontal eye field (FEF) or the superior colliculus (SC), then the same target was automatically chosen for pursuit. Our results imply that the neural signals responsible for saccade execution can also act as an internal command of target choice for other movement systems.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Example of saccade-induced target choice for pursuit at a single stimulation site.
Figure 2: Saccade-induced target choice for pursuit is selective for the direction of motion of the target and not the direction of the saccade.
Figure 3: Trial-by-trial analysis of target choice for pursuit by saccades.
Figure 4: Target choice for pursuit by saccades, averaged across all trials.
Figure 5: Target choice for pursuit by saccades is not a transient phenomenon.
Figure 6: Subthreshold stimulation of the FEF does not enhance pursuit.
Figure 7: Saccades elicited from the SC also cause target selection for pursuit.

Similar content being viewed by others

References

  1. Glimcher, P.W. Making choices: the neurophysiology of visual-saccadic decision making. Trends Neurosci. 24, 654–659 (2001).

    Article  CAS  Google Scholar 

  2. Schall, J.D. Neural basis of deciding, choosing and acting. Nat. Rev. Neurosci. 2, 33–42 (2001).

    Article  CAS  Google Scholar 

  3. Keller, E.L. & Heinen, S.J. Generation of smooth-pursuit eye movements: neuronal mechanisms and pathways. Neurosci. Res. 11, 79–107 (1991).

    Article  CAS  Google Scholar 

  4. Wurtz, R.H. & Goldberg, M.E. The Neurobiology of Saccadic Eye Movements (Elsevier, New York, 1989).

    Google Scholar 

  5. Glimcher, P.W. & Sparks, D.L. Movement selection in advance of action in the superior colliculus. Nature 355, 542–545 (1992).

    Article  CAS  Google Scholar 

  6. Schall, J.D. & Hanes, D.P. Neural basis of saccade target selection in frontal eye field during visual search. Nature 366, 467–469 (1993).

    Article  CAS  Google Scholar 

  7. Schall, J.D., Hanes, D.P., Thompson, K.G. & King, D.J. Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation. J. Neurosci. 15, 6905–6918 (1995).

    Article  CAS  Google Scholar 

  8. Ferrera, V.P. Task-dependent modulation of the sensorimotor transformation for smooth pursuit eye movements. J. Neurophysiol. 84, 2725–2738 (2000).

    Article  CAS  Google Scholar 

  9. Krauzlis, R.J., Zivotofsky, A.Z. & Miles, F.A. Target selection for pursuit and saccadic eye movements in humans. J. Cogn. Neurosci. 11, 641–649 (1999).

    Article  CAS  Google Scholar 

  10. Recanzone, G.H. & Wurtz, R.H. Effects of attention on MT and MST neuronal activity during pursuit initiation. J. Neurophysiol. 83, 777–790 (2000).

    Article  CAS  Google Scholar 

  11. Gardner, J.L. & Lisberger, S.G. Linked target selection for saccadic and smooth pursuit eye movements. J. Neurosci. 21, 2075–2084 (2001).

    Article  CAS  Google Scholar 

  12. Lisberger, S.G. & Ferrera, V.P. Vector averaging for smooth pursuit eye movements initiated by two moving targets in monkeys. J. Neurosci. 17, 7490–7502 (1997).

    Article  CAS  Google Scholar 

  13. Robinson, D.A. Eye movements evoked by collicular stimulation in the alert monkey. Vision Res. 12, 1795–1808 (1972).

    Article  CAS  Google Scholar 

  14. Robinson, D.A. & Fuchs, A.F. Eye movements evoked by stimulation of frontal eye fields. J. Neurophysiol. 32, 637–648 (1969).

    Article  CAS  Google Scholar 

  15. Bruce, C.J., Goldberg, M.E., Bushnell, M.C. & Stanton, G.B. Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. J. Neurophysiol. 54, 714–734 (1985).

    Article  CAS  Google Scholar 

  16. Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12, 4745–4765 (1992).

    Article  CAS  Google Scholar 

  17. Green, D.M. & Swets, J.A. Signal Detection Theory and Psychophysics (Wiley, New York, 1966).

    Google Scholar 

  18. Chou, I.H. & Lisberger, S.G. Spatial generalization of learning in smooth pursuit eye movements: implications for the coordinate frame and sites of learning. J. Neurosci. 22, 4728–4739 (2002).

    Article  CAS  Google Scholar 

  19. Von Helmholtz, H. Helmholtz's Treatise on Physiological Optics (ed. Southall, J. P. C.) (The Optical Society of America, Rochester, New York, 1867/1924).

    Google Scholar 

  20. Sperry, R. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482–489 (1950).

    Article  CAS  Google Scholar 

  21. Von Holst, E. & Mittelstaedt, H. Das reafferenzprinzip. Wechselwirkung zwischen zentralnervensystem and peripherie. Naturwissenschaften 37, 464–476 (1950).

    Article  Google Scholar 

  22. Ross, J., Morrone, M.C., Goldberg, M.E. & Burr, D.C. Changes in visual perception at the time of saccades. Trends Neurosci. 24, 113–121 (2001).

    Article  CAS  Google Scholar 

  23. Shepherd, M., Findlay, J.M. & Hockey, R.J. The relationship between eye movements and spatial attention. Q. J. Exp. Psychol. 38A, 475–491 (1986).

    Article  Google Scholar 

  24. Hoffman, J.E. & Subramaniam, B. The role of visual attention in saccadic eye movements. Percept. Psychophys. 57, 787–795 (1995).

    Article  CAS  Google Scholar 

  25. Kowler, E., Anderson, E., Dosher, B. & Blaser, E. The role of attention in the programming of saccades. Vision Res. 35, 1897–1916 (1995).

    Article  CAS  Google Scholar 

  26. Deubel, H. & Schneider, W.X. Saccade target selection and object recognition: evidence for a common attentional mechanism. Vision Res. 36, 1827–1837 (1996).

    Article  CAS  Google Scholar 

  27. Sheliga, B.M., Riggio, L. & Rizzolatti, G. Orienting of attention and eye movements. Exp. Brain Res. 98, 507–522 (1994).

    Article  CAS  Google Scholar 

  28. Kustov, A.A. & Robinson, D.L. Shared neural control of attentional shifts and eye movements. Nature 384, 74–77 (1996).

    Article  CAS  Google Scholar 

  29. Moore, T. & Fallah, M. Control of eye movements and spatial attention. Proc. Natl. Acad. Sci. USA 98, 1273–1276 (2001).

    Article  CAS  Google Scholar 

  30. Recanzone, G.H. & Wurtz, R.H. Shift in smooth pursuit initiation and MT and MST neuronal activity under different stimulus conditions. J. Neurophysiol. 82, 1710–1727 (1999).

    Article  CAS  Google Scholar 

  31. Johansson, R.S., Göran, W., Bäckström, A. & Flanagan, J.R. Eye-hand coordination in object manipulation. J. Neurosci. 21, 6917–6932 (2001).

    Article  CAS  Google Scholar 

  32. Lisberger, S.G., Morris, E.J. & Tychsen, L. Visual motion processing and sensory-motor integration for smooth pursuit eye movements. Annu. Rev. Neurosci. 10, 97–129 (1987).

    Article  CAS  Google Scholar 

  33. Miles, F.A., Schwarz, U. & Busettini, C. in Representations of Vision: Trends and Tacit Assumptions in Vision Research (ed. Gorea, A.) 185–199 (Cambridge University Press, 1991).

    Google Scholar 

  34. Kowler, E., Steen, J.V.D., Tamminga, E.P. & Collewijn, H. Voluntary selection of the target for smooth eye movement in the presence of superimposed, full-field stationary and moving stimuli. Vision Res. 24, 1789–1798 (1984).

    Article  CAS  Google Scholar 

  35. Ferrera, V.P. & Lisberger, S.G. Attention and target selection for smooth pursuit eye movements. J. Neurosci. 15, 7472–7484 (1995).

    Article  CAS  Google Scholar 

  36. Komatsu, H. & Wurtz, R.H. Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. J. Neurophysiol. 62, 31–47 (1989).

    Article  CAS  Google Scholar 

  37. Treue, S. & Maunsell, J.H. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382, 539–541 (1996).

    Article  CAS  Google Scholar 

  38. Seidemann, E. & Newsome, W.T. Effect of spatial attention on the responses of area MT neurons. J. Neurophysiol. 81, 1783–1794 (1999).

    Article  CAS  Google Scholar 

  39. Treue, S. & Maunsell, J.H. Effects of attention on the processing of motion in macaque middle temporal and medial superior temporal visual cortical areas. J. Neurosci. 19, 7591–7602 (1999).

    Article  CAS  Google Scholar 

  40. Duhamel, J.-R., Colby, C.L. & Goldberg, M.E. The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255, 90–92 (1992).

    Article  CAS  Google Scholar 

  41. Kahlon, M. & Lisberger, S.G. Vector averaging occurs downstream from learning in smooth pursuit eye movements of monkeys. J. Neurosci. 19, 9039–9053 (1999).

    Article  CAS  Google Scholar 

  42. Tanaka, M. & Lisberger, S.G. Role of arcuate frontal pursuit area of monkeys in smooth pursuit eye movements, II. Relation to vector averaging pursuit of two-target stimuli. J. Neurophysiol. 87, 2700–2714 (2002).

    Article  Google Scholar 

  43. Krauzlis, R.J., Basso, M.A. & Wurtz, R.H. Shared motor error for multiple eye movements. Science 276, 1693–1695 (1997).

    Article  CAS  Google Scholar 

  44. Missal, M., de Brouwer, S., Lefevre, P. & Olivier, E. Activity of mesencephalic vertical burst neurons during saccades and smooth pursuit. J. Neurophysiol. 83, 2080–2092 (2000).

    Article  CAS  Google Scholar 

  45. Morris, E.J. & Lisberger, S.G. Different responses to small visual errors during initiation and maintenance of smooth-pursuit eye movements in monkeys. J. Neurophysiol. 58, 1351–1369 (1987).

    Article  CAS  Google Scholar 

  46. Krauzlis, R.J. & Dill, N. Neural correlates of target choice for pursuit and saccades in the primate superior colliculus. Neuron (in press).

  47. Salzman, C.D., Britten, K.H. & Newsome, W.T. Cortical microstimulation influences perceptual judgements of motion direction. Nature 346, 174–177 (1990).

    Article  CAS  Google Scholar 

  48. Romo, R., Hernandez, A., Zainos, A. & Salinas, E. Somatosensory discrimination based on cortical microstimulation. Nature 392, 387–390 (1998).

    Article  CAS  Google Scholar 

  49. Lisberger, S.G. Postsaccadic enhancement of initiation of smooth pursuit eye movements in monkeys. J. Neurophysiol. 79, 1918–1930 (1998).

    Article  CAS  Google Scholar 

  50. Gottlieb, J.P., Bruce, C.J. & MacAvoy, M.G. Smooth eye movements elicited by microstimulation in the primate frontal eye field. J. Neurophysiol. 69, 786–799 (1993).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to P. Glimcher, M. Shadlen and the Lisberger lab for helpful discussions, and to A. Doupe and I. Chou for comments on an earlier version of the paper. We also thank J. Horton for surgical assistance, K. MacLeod, E. Montgomery and S. Tokiyama for surgical, animal and technical assistance, M. Meneses for animal husbandry, K. McGary for electronics, L. Bocskai for machining, S. Ruffner for computer programming, D. Kleinhesselink for network management and E. Molyneaux for administrative support. Research was supported by the Howard Hughes Medical Institute, National Eye Institute grant EY03878, and a Burroughs Welcome Fund training grant in Quantitative Biology (J.L.G.).

Author information

Authors and Affiliations

  1. Department of Physiology, Howard Hughes Medical Institute, W.M. Keck Foundation Center for Integrative Neuroscience, and Bioengineering Graduate Group, University of California, Box 0444, San Francisco, 94143, California, USA

    Justin L. Gardner & Stephen G. Lisberger

Authors
  1. Justin L. Gardner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen G. Lisberger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Justin L. Gardner.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gardner, J., Lisberger, S. Serial linkage of target selection for orienting and tracking eye movements. Nat Neurosci 5, 892–899 (2002). https://doi.org/10.1038/nn897

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn897

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing