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Neurons compute internal models of the physical laws of motion

Nature volume 430, pages 560–564 (2004)Cite this article

Abstract

A critical step in self-motion perception and spatial awareness is the integration of motion cues from multiple sensory organs that individually do not provide an accurate representation of the physical world. One of the best-studied sensory ambiguities is found in visual processing, and arises because of the inherent uncertainty in detecting the motion direction of an untextured contour moving within a small aperture1,2,3,4. A similar sensory ambiguity arises in identifying the actual motion associated with linear accelerations sensed by the otolith organs in the inner ear5,6. These internal linear accelerometers respond identically during translational motion (for example, running forward) and gravitational accelerations experienced as we reorient the head relative to gravity (that is, head tilt). Using new stimulus combinations, we identify here cerebellar and brainstem motion-sensitive neurons that compute a solution to the inertial motion detection problem. We show that the firing rates of these populations of neurons reflect the computations necessary to construct an internal model representation of the physical equations of motion.

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Figure 1: Neural responses that encode either the net gravito-inertial acceleration or the inertial component of linear acceleration.
Figure 2: Summary of peak firing rates during (a) tilt-only and (b, c) the combined protocols as a function of the respective responses during translation-only motion.
Figure 3: Cerebellar FN neurons more closely encode the inertial component of acceleration than does the brainstem VN cell population.
Figure 4: An internal model of equation (3) accounts best for the modulation in neural firing rates.

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Acknowledgements

The work was supported by grants from NIH and NASA. We thank E. Klier, C. Fetsch, G. DeAngelis and L. Snyder for aid in preparation of the manuscript.

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Authors and Affiliations

  1. Department of Neurobiology, Washington University School of Medicine, Saint Louis, Missouri, 63110, USA

    Dora E. Angelaki, Aasef G. Shaikh, Andrea M. Green & J. David Dickman

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  1. Dora E. Angelaki
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  2. Aasef G. Shaikh
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  3. Andrea M. Green
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  4. J. David Dickman
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Correspondence to Dora E. Angelaki.

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Supplementary information

Supplementary Information

This file contains two supplemental figures that provide further theoretical and experimental details. Supplemental Fig. 1 shows a schematic representation of the computations to estimate translational acceleration for the motion stimuli used in the manuscript. Supplemental Fig. 2 shows additional data about the phase distribution of the populations of neurons. (DOC 188 kb)

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Angelaki, D., Shaikh, A., Green, A. et al. Neurons compute internal models of the physical laws of motion. Nature 430, 560–564 (2004). https://doi.org/10.1038/nature02754

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