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Coding of smooth eye movements in three-dimensional space by frontal cortex

Abstract

Through the development of a high-acuity fovea, primates with frontal eyes have acquired the ability to use binocular eye movements to track small objects moving in space1. The smooth-pursuit system moves both eyes in the same direction to track movement in the frontal plane (frontal pursuit), whereas the vergence system moves left and right eyes in opposite directions to track targets moving towards or away from the observer (vergence tracking). In the cerebral cortex and brainstem, signals related to vergence eye movements—and the retinal disparity and blur signals that elicit them—are coded independently of signals related to frontal pursuit2,3,4,5,6. Here we show that these types of signal are represented in a completely different way in the smooth-pursuit region of the frontal eye fields7,8,9,10,11. Neurons of the frontal eye field modulate strongly during both frontal pursuit and vergence tracking, which results in three-dimensional cartesian representations of eye movements. We propose that the brain creates this distinctly different intermediate representation to allow these neurons to function as part of a system that enables primates to track and manipulate objects moving in three-dimensional space.

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Figure 1: Representative activity of a pursuit neuron in the caudal frontal eye field.
Figure 3: Linear summation of frontal pursuit and vergence tracking responses and maintenance of discharge during target blanking.
Figure 2: Eye velocity and vergence velocity sensitivity of caudal FEF neurons during frontal pursuit and vergence tracking.
Figure 4: Three-dimensional sensitivity vectors of caudal FEF neurons and recording locations.

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Acknowledgements

We thank B. Cumming, M. Goldberg, S. Lisberger, F. Miles and P. Strick for comments on the manuscript, and T. Akao and F. Sato for participation in some experiments. This work was supported in part by CREST of JST, Japanese Ministry of Education, Science, Culture and Sports, and Marna Cosmetics.

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Correspondence to Kikuro Fukushima.

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Fukushima, K., Yamanobe, T., Shinmei, Y. et al. Coding of smooth eye movements in three-dimensional space by frontal cortex. Nature 419, 157–162 (2002). https://doi.org/10.1038/nature00953

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