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An area for vergence eye movement in primate frontal cortex

Abstract

To view objects at different distances, humans rely on vergence eye movements to appropriately converge or diverge the eyes and on ocular accommodation to focus the object1,2. Despite the importance of these coordinated eye movements (the ‘near response’) very little is known about the role of the cerebral cortex in their control. As near-response neurons exist within the nucleus reticularis tegmenti pontis3, which receives input from the frontal eye field region of frontal cortex4,5,6, and this cortical region is known to be involved in saccadic7,8,9 and smooth-pursuit eye movements10,11,12, we propose that a nearby region might play a role in vergence and ocular accommodation. Here we provide evidence from rhesus monkeys that a region of frontal cortex located immediately anterior to the saccade-related frontal eye field region is involved in vergence and ocular accommodation, and in the sensorimotor transformations required for these eye movements. We conclude that the macaque frontal cortex is involved in the control of all voluntary eye movements, and suggest that the definition of the frontal eye fields should be expanded to include this region.

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Figure 1: Response properties of a prearcuate vergence-related neuron.
Figure 2: Response properties of a prearcuate visuo-vergence neuron.
Figure 3: Effects of electrical microstimulation at the site of a convergence-related neuron.
Figure 4: Location of near- and far-response neurons.

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References

  1. Rashbass, C. & Westheimer, G. Disjunctive eye movements. J. Physiol. 159, 339–360 (1961).

    Article  CAS  Google Scholar 

  2. Schor, C. M. A dynamic model of cross-coupling between accommodation and convergence: Simulations of step and frequency responses. Optom. Vis. Sci. 69 , 258–269 (1992).

    Article  CAS  Google Scholar 

  3. Gamlin, P. D. R. & Clarke, R. J. Single-unit activity in the nucleus reticularis tegmenti pontis related to vergence and ocular accommodation. J. Neurophysiol. 73, 2115–2119 (1995).

    Article  CAS  Google Scholar 

  4. Leichnetz, G. R., Smith, D. J. & Spencer, R. F. Cortical projections to the paramedian tegmental and basilar pons in the monkey. J. Comp. Neurol. 228 , 388–408 (1984).

    Article  CAS  Google Scholar 

  5. Huerta, M. F., Krubitzer, L. H. & Kaas, J. H. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys: I. Subcortical connections. J. Comp. Neurol. 253, 415– 439 (1986).

    Article  CAS  Google Scholar 

  6. Stanton, G. B., Goldberg, M. E. & Bruce, C. J. Frontal eye field efferents in the macaque monkey: I. Subcortical pathways and topography of striatal and thalamic terminal fields. J. Comp. Neurol. 271, 473– 492 (1988).

    Article  CAS  Google Scholar 

  7. Bizzi, E. Discharge of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys. Exp. Brain Res. 6, 69–80 (1968).

    Article  CAS  Google Scholar 

  8. Bruce, C. J. & Goldberg, M. E. Primate frontal eye fields. I. Single neurons discharging before saccades. J. Neurophysiol. 53, 603–635 ( 1985).

    Article  CAS  Google Scholar 

  9. Dias, E. C., Kiesau, M. & Segraves, M. A. Acute activation and inactivation of macaque frontal eye field with GABA-related drugs. J. Neurophysiol. 74, 2744–2748 (1995).

    Article  CAS  Google Scholar 

  10. Lynch, J. C. Frontal eye field lesions in monkeys disrupt visual pursuit. Exp. Brain Res. 68, 437–441 ( 1987).

    Article  CAS  Google Scholar 

  11. 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 

  12. 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 

  13. Leigh, R. J. & Zee, D. S. The Neurology of Eye Movements (Davis, Philadelphia, 1999).

    Google Scholar 

  14. Gamlin, P. D. R., Yoon, K. & Zhang, H. The role of cerebro-ponto-cerebellar pathways in the control of vergence eye movements. Eye 10, 167– 171 (1996).

    Article  Google Scholar 

  15. Gamlin, P. D. Subcortical neural circuits for ocular accommodation and vergence in primates. Ophthalmic. Physiol. Opt. 19, 81– 89 (1999).

    Article  CAS  Google Scholar 

  16. Judge, S. J. & Cumming, B. G. Neurons in the monkey midbrain with activity related to vergence eye movement and accommodation. J. Neurophysiol. 55, 915–930 (1986).

    Article  CAS  Google Scholar 

  17. Zhang, Y., Mays, L. E. & Gamlin, P. D. R. Characteristics of near response cells projecting to the oculomotor nucleus. J. Neurophysiol. 67, 944–960 (1992).

    Article  CAS  Google Scholar 

  18. Newsome, W. T., Wurtz, R. H. & Komatsu, H. Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. J. Neurophysiol. 60, 604–620 (1988).

    Article  CAS  Google Scholar 

  19. Mustari, M. J., Fuchs, A. F. & Wallman, J. Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque. J. Neurophysiol. 60, 664–686 (1988).

    Article  CAS  Google Scholar 

  20. Mays, L. E. & Sparks, D. L. Dissociation of visual and saccade-related responses in superior colliculus neurons. J. Neurophysiol. 42, 207–232 (1980).

    Article  Google Scholar 

  21. Gnadt, J. W. & Andersen, R. A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp. Brain Res. 70, 216–220 ( 1988).

    CAS  PubMed  Google Scholar 

  22. Gamlin, P. D. R., Zhang, Y., Clendaniel, R. A. & Mays, L. E. Behavior of identified Edinger-Westphal neurons during ocular accommodation. J. Neurophysiol. 72, 2368– 2382 (1994).

    Article  CAS  Google Scholar 

  23. Zhang, H. & Gamlin, P. D. R. Neurons in the posterior interposed nucleus of the cerebellum related to vergence and accommodation. I. Steady-state characteristics. J. Neurophysiol. 79, 1255 –1269 (1998).

    Article  CAS  Google Scholar 

  24. Ferraina, S., Pare, M. & Wurtz, R. H. Disparity sensitivity of frontal eye field neurons. J. Neurophysiol. 83, 625–629 (2000).

    Article  CAS  Google Scholar 

  25. Fischer, B. & Poggio, G. F. Depth sensitivity of binocular cortical neurons of behaving monkeys. Proc. R. Soc. Lond. B 204, 409–414 (1979).

    Article  ADS  CAS  Google Scholar 

  26. Munoz, D. P. & Wurtz, R. H. Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J. Neurophysiol. 73, 2313–2333 (1995).

    Article  CAS  Google Scholar 

  27. Judge, S. J., Richmond, B. S. & Chu, F. C. Implantation of magnetic search coils for measurement of eye position: An improved method. Vision Res. 20 , 535–538 (1980).

    Article  CAS  Google Scholar 

  28. Gamlin, P. D. R. & Mays, L. E. Dynamic properties of medial rectus motoneurons during vergence eye movements. J. Neurophysiol. 67, 64–74 (1992).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank S. Hayley and K. Winston for assistance. This work was supported by the National Eye Institute.

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Correspondence to Paul D. Gamlin.

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Gamlin, P., Yoon, K. An area for vergence eye movement in primate frontal cortex. Nature 407, 1003–1007 (2000). https://doi.org/10.1038/35039506

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