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Premotor commands encode monocular eye movements

Abstract

Binocular coordination of eye movements is essential for stereopsis (depth perception) and to prevent double vision. More than a century ago, Hering and Helmholtz debated the neural basis of binocular coordination. Helmholtz1 believed that each eye is controlled independently and that binocular coordination is learned. Hering2 believed that both eyes are innervated by common command signals that yoke the eye movements (Hering's law of equal innervation). Here we provide evidence that Hering's law is unlikely to be correct. We show that premotor neurons in the paramedian pontine reticular formation that were thought to encode conjugate3,4,5,6 velocity commands for saccades (rapid eye movements) actually encode monocular commands for either right or left eye saccades. However, 66% of the abducens motor neurons, which innervate the ipsilateral lateral rectus muscle, fire as a result of movements of either eye. The distribution of sensitivity to ipsilateral and contralateral eye movements across the abducens motor neuron pool may provide a basis for learning binocular coordination in infancy and adapting it throughout life.

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Figure 1: Discharge pattern of a binocular abducens motor neuron recorded in the VIth nerve.
Figure 2: Discharge pattern of a monocular abducens motor neuron.
Figure 3: The distribution of regression coefficients relating neuronal discharge to contralateral or ipsilateral eye position or saccade amplitude.
Figure 4: Excitatory burst neurons in the left PPRF encode monocular eye movements.
Figure 5: Examples of monocular discharge patterns of 2 EBNs.

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Acknowledgements

We thank J. Cai for writing the data acquisition software; C. Drake for care of our animals; B.-F. Tang and J. Alison for technical support; and M. Goldberg and P. May for comments on a preliminary version of this manuscript. This research was supported by NIH and ONR grants to W.M.K.

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Correspondence to Wu Zhou.

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Zhou, W., King, W. Premotor commands encode monocular eye movements. Nature 393, 692–695 (1998). https://doi.org/10.1038/31489

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