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.
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Glimcher, P.W. Making choices: the neurophysiology of visual-saccadic decision making. Trends Neurosci. 24, 654–659 (2001).
Schall, J.D. Neural basis of deciding, choosing and acting. Nat. Rev. Neurosci. 2, 33–42 (2001).
Keller, E.L. & Heinen, S.J. Generation of smooth-pursuit eye movements: neuronal mechanisms and pathways. Neurosci. Res. 11, 79–107 (1991).
Wurtz, R.H. & Goldberg, M.E. The Neurobiology of Saccadic Eye Movements (Elsevier, New York, 1989).
Glimcher, P.W. & Sparks, D.L. Movement selection in advance of action in the superior colliculus. Nature 355, 542–545 (1992).
Schall, J.D. & Hanes, D.P. Neural basis of saccade target selection in frontal eye field during visual search. Nature 366, 467–469 (1993).
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).
Ferrera, V.P. Task-dependent modulation of the sensorimotor transformation for smooth pursuit eye movements. J. Neurophysiol. 84, 2725–2738 (2000).
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).
Recanzone, G.H. & Wurtz, R.H. Effects of attention on MT and MST neuronal activity during pursuit initiation. J. Neurophysiol. 83, 777–790 (2000).
Gardner, J.L. & Lisberger, S.G. Linked target selection for saccadic and smooth pursuit eye movements. J. Neurosci. 21, 2075–2084 (2001).
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).
Robinson, D.A. Eye movements evoked by collicular stimulation in the alert monkey. Vision Res. 12, 1795–1808 (1972).
Robinson, D.A. & Fuchs, A.F. Eye movements evoked by stimulation of frontal eye fields. J. Neurophysiol. 32, 637–648 (1969).
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).
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).
Green, D.M. & Swets, J.A. Signal Detection Theory and Psychophysics (Wiley, New York, 1966).
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).
Von Helmholtz, H. Helmholtz's Treatise on Physiological Optics (ed. Southall, J. P. C.) (The Optical Society of America, Rochester, New York, 1867/1924).
Sperry, R. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482–489 (1950).
Von Holst, E. & Mittelstaedt, H. Das reafferenzprinzip. Wechselwirkung zwischen zentralnervensystem and peripherie. Naturwissenschaften 37, 464–476 (1950).
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).
Shepherd, M., Findlay, J.M. & Hockey, R.J. The relationship between eye movements and spatial attention. Q. J. Exp. Psychol. 38A, 475–491 (1986).
Hoffman, J.E. & Subramaniam, B. The role of visual attention in saccadic eye movements. Percept. Psychophys. 57, 787–795 (1995).
Kowler, E., Anderson, E., Dosher, B. & Blaser, E. The role of attention in the programming of saccades. Vision Res. 35, 1897–1916 (1995).
Deubel, H. & Schneider, W.X. Saccade target selection and object recognition: evidence for a common attentional mechanism. Vision Res. 36, 1827–1837 (1996).
Sheliga, B.M., Riggio, L. & Rizzolatti, G. Orienting of attention and eye movements. Exp. Brain Res. 98, 507–522 (1994).
Kustov, A.A. & Robinson, D.L. Shared neural control of attentional shifts and eye movements. Nature 384, 74–77 (1996).
Moore, T. & Fallah, M. Control of eye movements and spatial attention. Proc. Natl. Acad. Sci. USA 98, 1273–1276 (2001).
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).
Johansson, R.S., Göran, W., Bäckström, A. & Flanagan, J.R. Eye-hand coordination in object manipulation. J. Neurosci. 21, 6917–6932 (2001).
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).
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).
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).
Ferrera, V.P. & Lisberger, S.G. Attention and target selection for smooth pursuit eye movements. J. Neurosci. 15, 7472–7484 (1995).
Komatsu, H. & Wurtz, R.H. Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. J. Neurophysiol. 62, 31–47 (1989).
Treue, S. & Maunsell, J.H. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382, 539–541 (1996).
Seidemann, E. & Newsome, W.T. Effect of spatial attention on the responses of area MT neurons. J. Neurophysiol. 81, 1783–1794 (1999).
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).
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).
Kahlon, M. & Lisberger, S.G. Vector averaging occurs downstream from learning in smooth pursuit eye movements of monkeys. J. Neurosci. 19, 9039–9053 (1999).
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).
Krauzlis, R.J., Basso, M.A. & Wurtz, R.H. Shared motor error for multiple eye movements. Science 276, 1693–1695 (1997).
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).
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).
Krauzlis, R.J. & Dill, N. Neural correlates of target choice for pursuit and saccades in the primate superior colliculus. Neuron (in press).
Salzman, C.D., Britten, K.H. & Newsome, W.T. Cortical microstimulation influences perceptual judgements of motion direction. Nature 346, 174–177 (1990).
Romo, R., Hernandez, A., Zainos, A. & Salinas, E. Somatosensory discrimination based on cortical microstimulation. Nature 392, 387–390 (1998).
Lisberger, S.G. Postsaccadic enhancement of initiation of smooth pursuit eye movements in monkeys. J. Neurophysiol. 79, 1918–1930 (1998).
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).
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.).
The authors declare no competing financial interests.
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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
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