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The functional significance of velocity storage and its dependence on gravity

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Abstract

Research in the vestibular field has revealed the existence of a central process, called ‘velocity storage’, that is activated by both visual and vestibular rotation cues and is modified by gravity, but whose functional relevance during natural motion has often been questioned. In this review, we explore spatial orientation in the context of a Bayesian model of vestibular information processing. In this framework, deficiencies/ambiguities in the peripheral vestibular sensors are compensated for by central processing to more accurately estimate rotation velocity, orientation relative to gravity, and inertial motion. First, an inverse model of semicircular canal dynamics is used to reconstruct rotation velocity by integrating canal signals over time. However, its low-frequency bandwidth is limited to avoid accumulation of noise in the integrator. A second internal model uses this reconstructed rotation velocity to compute an internal estimate of tilt and inertial acceleration. The bandwidth of this second internal model is also restricted at low frequencies to avoid noise accumulation and drift of the tilt/translation estimator over time. As a result, low-frequency translation can be erroneously misinterpreted as tilt. The time constants of these two integrators (internal models) can be conceptualized as two Bayesian priors of zero rotation velocity and zero linear acceleration, respectively. The model replicates empirical observations like ‘velocity storage’ and ‘frequency segregation’ and explains spatial orientation (e.g., ‘somatogravic’) illusions. Importantly, the functional significance of this network, including velocity storage, is found during short-lasting, natural head movements, rather than at low frequencies with which it has been traditionally studied.

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Notes

  1. It is so because the acceleration of the endolymph in space is due to the friction between the endolymph and the canals. This friction is proportional to the difference in velocity between the canal and the endolymph, which is what is reported by the canal. Therefore, a perfect integration of the sensory signal of the canals yields a signal which is proportional to endolymph velocity in space.

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Acknowledgments

This work was supported by NIH grant EY12814

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  1. Department of Anatomy and Neurobiology, Washington University School of Medicine, 660 South Euclid Avenue, Box 8108, St. Louis, MO, 63110, USA

    Jean Laurens & Dora E. Angelaki

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  1. Jean Laurens
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  2. Dora E. Angelaki
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Correspondence to Dora E. Angelaki.

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Laurens, J., Angelaki, D.E. The functional significance of velocity storage and its dependence on gravity. Exp Brain Res 210, 407–422 (2011). https://doi.org/10.1007/s00221-011-2568-4

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