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.
Your institute does not have access to this article
Open Access articles citing this article.
Nature Communications Open Access 05 April 2022
Nature Communications Open Access 24 October 2018
Decomposing sensorimotor variability changes in ageing and their connection to falls in older people
Scientific Reports Open Access 28 September 2018
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Fitts, P. M. The information capacity of the human motor system in controlling the amplitude of movement. J. Exp. Psychol. 47, 381–391 (1954), reprinted in. J. Exp. Psychol. 121, 262–269 (1992)
Gordon, J., Ghilardi, M. F. & Ghez, C. Accuracy of planar reaching movements. I. Independence of direction and extent variability. Exp. Brain Res. 99, 97–111 (1994)
Messier, J. & Kalaska, J. F. Comparison of variability of initial kinematics and endpoints of reaching movements. Exp. Brain Res. 125, 129–152 (1999)
Harris, C. M. & Wolpert, D. M. Signal-dependent noise determines motor planning. Nature 394, 780–784 (1998)
d'Avella, A. & Bizzi, E. Low dimensionality of surpaspinally induced force fields. Proc. Natl Acad. Sci. USA 95, 7711–7714 (1998)
Santello, M., Flanders, M. & Soechting, J. F. Postural hand strategies for tool use. J. Neurosci. 18, 10105–10115 (1998)
Sanger, T. D. Human arm movements described by a low-dimensional superposition of principal components. J. Neurosci. 20, 1066–1072 (2000)
Todorov, E. & Jordan, M. I. Optimal feedback control as a theory of motor coordination. Nature Neurosci. 5, 1226–1235 (2002)
Donchin, O., Francis, J. T. & Shadmehr, R. Quantifying generalization from trial-by-trial behaviour of adaptive systems that learn with basis functions: theory and experiments in human motor control. J. Neurosci. 23, 9032–9045 (2003)
Lisberger, S. G., Morris, E. J. & Tyschen, L. Visual motion processing and sensory-motor integration for smooth pursuit eye movements. Annu. Rev. Neurosci. 10, 97–129 (1987)
Lisberger, S. G. & Westbrook, L. E. Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys. J. Neurosci. 5, 1662–1673 (1985)
de Bruyn, B. & Orban, G. A. Human velocity and direction discrimination measured with random dot patterns. Vision Res. 28, 1323–1335 (1988)
Watamaniuk, S. N. J. & Heinen, S. J. Human smooth pursuit direction discrimination. Vision Res. 39, 59–70 (1999)
Kowler, E. & McKee, S. P. Sensitivity of smooth eye movement to small differences in target velocity. Vision Res. 27, 993–1015 (1987)
Gegenfurter, K. R., Xing, D., Scott, B. H. & Hawken, M. J. A comparison of pursuit eye movement and perceptual performance in speed discrimination. J. Vis. 3, 865–876 (2003)
Purushothaman, G. & Bradley, D. C. Neural population code for fine perceptual decisions in area MT. Nature Neurosci. 8, 99–106 (2005)
Liu, J. & Newsome, W. T. Correlation between speed perception and neural activity in the medial temporal visual area. J. Neurosci. 25, 711–722 (2005)
Newsome, W. T., Britten, K. H. & Movshon, J. A. Neuronal correlates of a perceptual decision. Nature 341, 52–54 (1989)
Green, D. M. & Swets, J. A. Signal Detection Theory and Psychophysics (Wiley, New York, 1966)
Stone, L. S. & Krauzlis, R. J. Shared motion signals for human perceptual decisions and oculomotor actions. J. Vis. 3, 725–736 (2003)
Carpenter, R. H. S. in Eye Movements: Cognition and Visual Perception (eds Fisher, D. F., Monty, R. A. & Senders, J. W.) 237–246 (Lawrence Erlbaum Associates, Hillsdale, New Jersey, 1981)
Osborne, L. C., Bialek, W. & Lisberger, S. G. Time course of information about motion direction in visual area MT. J. Neurosci. 24, 3210–3222 (2004)
Roitman, J. D. & Shadlen, M. N. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 22, 9475–9489 (2002)
Hanes, D. P. & Schall, J. D. Neural control of voluntary movement initiation. Science 274, 427–430 (1996)
Ross, J., Morrone, M. C., Goldberg, M. E. & Burr, D. C. Changes in visual perception at the time of saccades. Trends Neurosci. 24, 316–318 (2001)
Fuchs, A. F. & Luschei, E. S. Firing patterns of abducens neurons of alert monkeys in relationship to horizontal eye movement. J. Neurophysiol. 33, 382–392 (1970)
Bialek, W. in Physics of Biomolecules and Cells: Les Houches Session LXXV (eds Flyvbjerg, H., Julicher, F., Ormos, P. & David, F.) 485–577 (EDP Sciences, Les Ulis and Springer-Verlag, Berlin, 2002)
Bialek, W. Physical limits to sensation and perception. Annu. Rev. Biophys. Biophys. Chem. 16, 455–478 (1987)
Barlow, H. B. Critical limiting factors in the design of the eye and visual cortex. Proc. R. Soc. Lond. B 212, 1–34 (1981)
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.
Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
About this article
Cite this article
Osborne, L., Lisberger, S. & Bialek, W. A sensory source for motor variation. Nature 437, 412–416 (2005). https://doi.org/10.1038/nature03961
Nature Communications (2022)
Neural Computing and Applications (2020)
Varied movement errors drive learning of dynamic balance control during walking in people with incomplete spinal cord injury: a pilot study
Experimental Brain Research (2020)
Nature Human Behaviour (2019)
The intrinsic attractor manifold and population dynamics of a canonical cognitive circuit across waking and sleep
Nature Neuroscience (2019)