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Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex

Abstract

In studies of the neural mechanisms giving rise to behaviour, changes in the neural and behavioural responses produced by a given stimulus have been widely reported. This ‘gain control’ can boost the responses to sensory inputs that are particularly relevant1,2,3,4, select among reflexes for execution by motoneurons5,6 or emphasize specific movement targets7. Gain control is also an integral part of the smooth-pursuit eye movement system8,9,10,11,12,13. One signature of gain control is that a brief perturbation of a stationary target during fixation causes tiny eye movements, whereas the same perturbation of a moving target during the active state of accurate pursuit causes large responses9. Here we show that electrical stimulation of the smooth-pursuit eye movement region in the arcuate sulcus of the frontal lobe (‘the frontal pursuit area’, FPA) mimics the active state of pursuit. Such stimulation enhances the response to a brief perturbation of target motion, regardless of the direction of motion. We postulate that the FPA sets the gain of pursuit, thereby participating in target selection for pursuit.

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Figure 1: Smooth eye movements evoked by electrical stimulation.
Figure 2: Enhancement of the response to target motion caused by stimulation in the FPA.
Figure 3: Summary of the enhancement for 33 stimulation sites in 32 penetrations.

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References

  1. Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193– 222 (1995).

    Article  CAS  Google Scholar 

  2. Maunsell, J. H. The brain's visual world: representation of visual targets in cerebral cortex. Science 270, 764–769 (1995).

    Article  ADS  CAS  Google Scholar 

  3. Treue, S. & Martinez Trujillo, J. C. Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399, 575–579 ( 1999).

    Article  ADS  CAS  Google Scholar 

  4. Posner, M. I. Attention: the mechanisms of consciousness. Proc. Natl Acad. Sci. USA 91, 7398–7403 ( 1994).

    Article  ADS  CAS  Google Scholar 

  5. Pearson, K. G. Proprioceptive regulation of locomotion. Curr. Opin. Neurobiol. 5, 786–791 ( 1995).

    Article  CAS  Google Scholar 

  6. Roy, J. E. & Cullen, K. E. A neural correlate for vestibulo-ocular reflex suppression during voluntary eye-head gaze shifts. Nature Neurosci. 1, 404–410 ( 1998).

    Article  CAS  Google Scholar 

  7. Wurtz, R. H. & Mohler, C. W. Organization of monkey superior colliculus: enhanced visual response of superficial layer cells. J. Neurophysiol. 39, 745–765 (1976).

    Article  CAS  Google Scholar 

  8. Grasse, K. L. & Lisberger, S. G. Analysis of a naturally occurring asymmetry in vertical smooth pursuit eye movements in a monkey. J. Neurophysiol. 67, 164–179 (1992).

    Article  CAS  Google Scholar 

  9. Schwartz, J. D. & Lisberger, S. G. Initial tracking conditions modulate the gain of visuo-motor transmission for smooth pursuit eye movements in monkeys. Vis. Neurosci. 11, 411–424 (1994).

    Article  CAS  Google Scholar 

  10. Krauzlis, R. J. & Miles, F. A. Transitions between pursuit eye movements and fixation in the monkey: dependence on context. J. Neurophysiol. 76, 1622–1638 (1996).

    Article  CAS  Google Scholar 

  11. Keating, E. G. & Pierre, A. Architecture of a gain controller in the pursuit system. Behav. Brain Res. 81, 173–181 (1996).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Gardner, J. & Lisberger, S. G. Linked target selection for saccadic and smooth pursuit eye movements. Soc. Neurosci. Abstr. 25, 1398 (1999).

    Google Scholar 

  14. MacAvoy, M. G., Gottlieb, J. P. & Bruce, C. J. Smooth-pursuit eye movement representation in the primate frontal eye field. Cereb. Cortex 1, 95–102 (1991).

    Article  CAS  Google Scholar 

  15. 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 

  16. Groh, J. M., Born, R. T. & Newsome, W. T. How is a sensory map read out? Effects of microstimulation in visual area MT on saccades and smooth pursuit eye movements. J. Neurosci. 17, 4312–4330 (1997).

    Article  CAS  Google Scholar 

  17. 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 

  18. May, J. G., Keller, E. L. & Crandall, W. F. Changes in eye velocity during smooth pursuit tracking induced by microstimulation in the dorsolateral pontine nucleus of the macaque. Soc. Neurosci. Abstr. 11, 79 (1985).

    Google Scholar 

  19. Krauzlis, R. J. & Miles, F. A. Role of the oculomotor vermis in generating pursuit and saccades: effects of microstimulation. J. Neurophysiol. 80, 2046–2062 (1998).

    Article  CAS  Google Scholar 

  20. Gottlieb, J. P., MacAvoy, M. G. & Bruce, C. J. Neural responses related to smooth-pursuit eye movements and their correspondence with electrically elicited smooth eye movements in the primate frontal eye field. J. Neurophysiol. 72, 1634–1653 (1994).

    Article  CAS  Google Scholar 

  21. Tanaka, M. & Fukushima, K. Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J. Neurophysiol. 80, 28– 47 (1998).

    Article  CAS  Google Scholar 

  22. Fukushima, K., Sato, T., Fukushima, J., Shinmei, Y. & Kaneko, C. R. Activity of smooth pursuit-related neurons in the monkey periarcuate cortex during pursuit and passive whole-body rotation. J. Neurophysiol. 83, 563– 587 (2000).

    Article  CAS  Google Scholar 

  23. Keating, E. G. Frontal eye field lesions impair predictive and visually-guided pursuit eye movements. Exp. Brain Res. 86, 311– 323 (1991).

    Article  CAS  Google Scholar 

  24. Shi, D., Friedman, H. R. & Bruce, C. J. Deficits in smooth-pursuit eye movements after muscimol inactivation within the primate's frontal eye field. J. Neurophysiol. 80, 458–464 ( 1998).

    Article  CAS  Google Scholar 

  25. 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 

  26. Adler, S. A., Bala, J. K. & Krauzlis, R. J. Effects of prior sensory and motor information on the initiation of pursuit and saccades. Soc. Neurosci. Abstr. 26, 1716 (2000).

    Google Scholar 

  27. Goldberg, M. E. & Segraves, M. A. in The Neurobiology of Saccadic Eye Movements, Reviews of Oculomotor Research Vol. III (eds Wurtz, R. H. & Goldberg, M. E.) 283–313 (Elsevier, Amsterdam, 1989).

    Google Scholar 

  28. Schall, J. D. & Thompson, K. G. Neural selection and control of visually guided eye movements. Annu. Rev. Neurosci. 22, 241–259 (1999).

    Article  CAS  Google Scholar 

  29. Lisberger, S. G. & Westbrook, L. E. Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys. J. Neurosci. 5, 1662– 1673 (1985).

    Article  CAS  Google Scholar 

  30. Carl, J. R. & Gellman, R. S. Human smooth pursuit: stimulus-dependent responses. J. Neurophysiol. 57, 1446– 1463 (1987).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank J. Maunsell and A. Doupe for comments on the manuscript; S. Tokiyama for technical assistance; K. MacLeod and L. Montgomery for surgical assistance; M. Meneses for animal care; S. Ruffner for computer programs; D. Kleinhesselink for network management; K. McGary for electronic devices; and L. Bocskai for machinery. This work was supported by HHMI and by a NIH grant to S.G.L.

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Correspondence to Masaki Tanaka.

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Tanaka, M., Lisberger, S. Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex. Nature 409, 191–194 (2001). https://doi.org/10.1038/35051582

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