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Humans use internal models to estimate gravity and linear acceleration

Nature volume 398, pages 615–618 (1999)Cite this article

Abstract

Because sensory systems often provide ambiguous information, neural processes must exist to resolve these ambiguities. It is likely that similar neural processes are used by different sensory systems. For example, many tasks require neural processing to distinguish linear acceleration from gravity1, but Einstein's equivalence principle states that all linear accelerometers must measure both linear acceleration and gravity. Here we investigate whether the brain uses internal models, defined as neural systems that mimic physical principles, to help estimate linear acceleration and gravity2,3,4. Internal models may be used in motor control5,6,7, sensorimotor integration8,9,10 and sensory processing11,12,13,14, but direct experimental evidence for such models is limited. To determine how humans process ambiguous gravity and linear acceleration cues, subjects were tilted after being rotated at a constant velocity about an Earth-vertical axis. We show that the eye movements evoked by this post-rotational tilt include a response component that compensates for the estimated linear acceleration even when no actual linear acceleration occurs. These measured responses are consistent with our internal model predictions that the nervous system can develop a non-zero estimate of linear acceleration even when no true linear acceleration is present.

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Figure 1: During acceleration on Earth, gravity (G) minus linear acceleration (A) yields specific gravito-inertial force (GIF, F).
Figure 2: If the subject is oriented ‘nose-up’, a clockwise yaw rotational cue (ω̂) rotates the estimated gravity (Ĝ) toward the subject's right.
Figure 3: Post-rotational horizontal VOR.
Figure 4: Comparison of induced VOR to theoretical estimate of linear acceleration.

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Acknowledgements

We thank S. Clark-Donovan and J. Roth for assistance throughout and T. Inglis, G.McCollum, S. Oster, P. Roberts, C. Wall and the NSI sensorimotor journal club for comments on the manuscript. This work was supported by grants from the NIH/NIDCD (D.M.M.), ESA (L.Z.), and NIH/NASA (R.J.P.).

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Author notes

  1. Daniel M. Merfeld

    Present address: Vestibular Physiology Laboratory, Massachusetts Eye and Ear Infirmary, 243 Charles Street, Boston, MA, 02114, USA

  2. Daniel M. Merfeld and Lionel Zupan: These authors contributed equally to this work.

  3. Daniel M. Merfeld: Correspondence and requests for materials should be addressed to D.M.M.

Authors and Affiliations

  1. Neurological Sciences Institute, Oregon Health Sciences University, 1120 NW 20th Avenue, Portland, 97209, Oregon, USA

    Robert J. Peterka

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Correspondence to Daniel M. Merfeld.

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Merfeld, D., Zupan, L. & Peterka, R. Humans use internal models to estimate gravity and linear acceleration. Nature 398, 615–618 (1999). https://doi.org/10.1038/19303

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