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The proprioceptive representation of eye position in monkey primary somatosensory cortex

Nature Neuroscience volume 10, pages 640–646 (2007)Cite this article

Abstract

The cerebral cortex must have access to an eye position signal, as humans can report passive changes in eye position in total darkness, and visual responses in many cortical areas are modulated by eye position. The source of this signal is unknown. Here we demonstrate a representation of eye position in monkey primary somatosensory cortex, in the representation of the trigeminal nerve, near cells with a tactile representation of the contralateral brow. The neurons have eye position signals that increase monotonically with increasing orbital eccentricity from near the center of gaze, with directionally selectivity tuned in a Gaussian manner. All directions of eye position are represented in a single hemisphere. The signal is proprioceptive, because it can be obliterated by anesthetizing the contralateral orbit. It is not related to foveal or peripheral visual stimulation, and it represents the position of the eye in the head and not the angle of gaze in space.

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Figure 1: Activity of a tonic eye position neuron in monkey SI.
Figure 2: Location and tuning of eye position neurons.
Figure 3: Tonic and phasic responses of S1 eye position neurons.
Figure 4: Effect of retrobulbar block on neural activity.
Figure 5: Gradual effect of partial block on the eye position signal.
Figure 6: Independence of signal from gaze in space and foveal visual stimulation.
Figure 7: Independence of activity from background illumination.

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Acknowledgements

We are grateful to H. Eggers for teaching us how to perform retrobulbar blocks, G. Duncan for electronic and computer support, Y. Pavlova for dedicated animal maintenance, M. Osman and G. Asfaw for veterinary care, S. Dashnaw and J. Hirsch for MRI, and L. Palmer for facilitating everything. This research was supported by grants from the James S. McDonnell Foundation, the US National Eye Institute (1 R01 EY014978-01 and 1 R24 EY015634-01), and the Whitehall, Keck, Dana and Kavli Foundations.

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Author notes

  1. Xiaolan Wang and Mingsha Zhang: These authors contributed equally to this work.

Authors and Affiliations

  1. Mahoney Center for Brain and Behavior, Center for Neurobiology and Behavior, Columbia University College of Physicians and Surgeons, and the New York State Psychiatric Institute, 1051 Riverside Drive, Unit 87, New York, 10032, New York, USA

    Xiaolan Wang, Mingsha Zhang, Ian S Cohen & Michael E Goldberg

  2. Departments of Neurology and Psychiatry, Columbia University College of Physicians and Surgeons, 1051 Riverside Drive, Unit 87, New York, 10032, New York, USA

    Michael E Goldberg

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  1. Xiaolan Wang
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Contributions

X.W. and M.W. recorded all the neural activity, did much of the data analysis and made the figures. I.S.C. wrote many of the data analysis programs and did some of the preliminary data analysis. M.E.G. dreamed up the project, worked out the retrobulbar block technique with H. Eggers and supervised the entire project.

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Correspondence to Mingsha Zhang.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Table 1

Effect of eye eccentricity on cell response. (PDF 37 kb)

Supplementary Table 2

The effect of the retrobulbar block on each cell. (PDF 33 kb)

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Wang, X., Zhang, M., Cohen, I. et al. The proprioceptive representation of eye position in monkey primary somatosensory cortex. Nat Neurosci 10, 640–646 (2007). https://doi.org/10.1038/nn1878

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