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A sensory source for motor variation

Nature volume 437, pages 412–416 (2005)Cite this article

Abstract

Suppose that the variability in our movements1,2,3,4,5,6,7,8,9 is caused not by noise in the motor system itself, nor by fluctuations in our intentions or plans, but rather by errors in our sensory estimates of the external parameters that define the appropriate action. For tasks in which precision is at a premium, performance would be optimal if no noise were added in movement planning and execution: motor output would be as accurate as possible given the quality of sensory inputs. Here we use visually guided smooth-pursuit eye movements in primates10 as a testing ground for this notion of optimality. In response to repeated presentations of identical target motions, nearly 92% of the variance in eye trajectory can be accounted for as a consequence of errors in sensory estimates of the speed, direction and timing of target motion, plus a small background noise that is observed both during eye movements and during fixations. The magnitudes of the inferred sensory errors agree with the observed thresholds for sensory discrimination by perceptual systems, suggesting that the very different neural processes of perception and action are limited by the same sources of noise.

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Figure 1: Example of the variability in pursuit for a given target motion.
Figure 2: Analysis of variation in pursuit trajectory for a single day's experiment.
Figure 3: Reconstruction of individual pursuit trials from the model described by equation (1).

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Acknowledgements

This work was supported in part by a National Institutes of Health Grant and by the Howard Hughes Medical Institute. We thank S. Tokiyama, E. Montgomery and K. MacLeod for assistance with animal monitoring and maintenance, and S. Ruffner for computer programming. W.B. thanks the Sloan-Swartz Center at UCSF for its hospitality during critical stages of this collaboration.

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Authors and Affiliations

  1. Sloan-Swartz Center for Theoretical Neurobiology, W. M. Keck Foundation Center for Integrative Neuroscience, Department of Physiology,

    Leslie C. Osborne & Stephen G. Lisberger

  2. Howard Hughes Medical Institute, University of California at San Francisco, California, 94143-0444, San Francisco, USA

    Stephen G. Lisberger

  3. Joseph Henry Laboratories of Physics and the Lewis-Sigler Institute for Integrative Genomics, Princeton University, New Jersey, 08544, Princeton, USA

    William Bialek

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  1. Leslie C. Osborne
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  2. Stephen G. Lisberger
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Correspondence to Leslie C. Osborne.

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Osborne, L., Lisberger, S. & Bialek, W. A sensory source for motor variation. Nature 437, 412–416 (2005). https://doi.org/10.1038/nature03961

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