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Cited by 106Vestibular and auditory disordersMotor Control and AdaptationMultisensory perception and integration

Multimodal Integration in Rostral Fastigial Nucleus Provides an Estimate of Body Movement

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Brooks, Jessica X., Cullen, Kathleen E.·2009·The Journal of Neuroscience
DOI 10.1523/jneurosci.1937-09.2009PMC PMC3311469
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Abstract

The ability to accurately control posture and perceive self-motion and spatial orientation requires knowledge of the motion of both the head and body. However, whereas the vestibular sensors and nuclei directly encode head motion, no sensors directly encode body motion. Instead, the convergence of vestibular and neck proprioceptive inputs during self-motion is generally believed to underlie the ability to compute body motion. Here, we provide evidence that the brain explicitly computes an internal estimate of body motion at the level of single cerebellar neurons. Neuronal responses were recorded from the rostral fastigial nucleus, the most medial of the deep cerebellar nuclei, during whole-body, body-under-head, and head-on-body rotations. We found that approximately half of the neurons encoded the motion of the body in space, whereas the other half encoded the motion of the head in space in a manner similar to neurons in the vestibular nuclei. Notably, neurons encoding body motion responded to both vestibular and proprioceptive stimulation (accordingly termed bimodal neurons). In contrast, neurons encoding head motion were sensitive only to vestibular inputs (accordingly termed unimodal neurons). Comparison of the proprioceptive and vestibular responses of bimodal neurons further revealed similar tuning in response to changes in head-on-body position. We propose that the similarity in nonlinear processing of vestibular and proprioceptive signals underlies the accurate computation of body motion. Furthermore, the same neurons that encode body motion (i.e., bimodal neurons) most likely encode vestibular signals in a body-referenced coordinate frame, since the integration of proprioceptive and vestibular information is required for both computations.

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  • Recent work by Cullen and colleagues has shown an important relationship between corollary discharge signals and reafferent signals associated with the resulting movement of the head or body.

    “Recent work by Cullen and colleagues on the cerebellar and vestibular mechanisms related to the control and appreciation of head and body movements has shown the important relationship between corollary discharge signals and reafferent signals associated with the resulting movement of the head or body.”

    From Motion sickness: more than nausea and vomiting (2014) · cites this paper as Brooks and Cullen 2009

    The Discussion section on voluntary movements (page unavailable) reports that vestibular neurons respond differently to active and passive movement, supporting the claim’s connection to movement-related sensory signals. But the paper says its own experiments used only passive movements and proposes efference copy as a possibility requiring further study; it does not show a relationship between corollary discharge and reafference during resulting head or body movement. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Any discrepancy between expected and reafferent signals represents a sensory conflict that potentially could be provocative.

    “Any discrepancy between the expected and reafferent signals represents a sensory conflict that potentially could be provocative (Brooks and Cullen 2009, 2013; Cullen 2012; Cullen et al. 2009; Saab and Willis 2001; Serra et al. 1998).”

    From Motion sickness: more than nausea and vomiting (2014) · cites this paper as Brooks and Cullen 2009

    The Results section on simultaneous proprioceptive and vestibular stimulation reports that those inputs can cancel during head-on-body motion. The passages do not address a discrepancy between expected and reafferent signals, or whether such a discrepancy constitutes a potentially provocative sensory conflict (searched: reafference, sensory prediction, sensory conflict, motion sickness). Page numbers were not available in our copy. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

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  1. Hayes AVRB Optican LM A UNIX-based multiple process system for real-time data acquisition and control Western Electronic Show and Conference Proceedings 1982 2 1 10

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Related

Authors
Brooks, J. X., & Cullen, K. E.
Affiliations
McGill University (CA)
ORCID
Cullen, Kathleen E.
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2009-08-26
Volume
29
Issue
34
Pages
10499-10511
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.1937-09.2009
PMC
PMC3311469
OpenAlex
W2083680074
Cited by
106
References
56
Citations by year
2026: 2 · 2025: 9 · 2024: 6 · 2023: 7 · 2022: 1 · 2021: 10 · 2020: 7 · 2019: 6 · 2018: 4 · 2017: 6 · 2016: 6 · 2015: 3 · 2014: 17 · 2013: 8 · 2012: 3
FWCI
2.98
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Canadian Institutes of Health Research
  • National Institute on Deafness and Other Communication Disorders (R01DC002390)
Topics
  • Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
Keywords
neck proprioception, bimodal neurons, self-motion perception, deep cerebellar nuclei, vestibular nuclei
MeSH terms
Action Potentials, Animals, Macaca mulatta, Models, Neurological, Motion, Movement, Neck, Neurons, Orientation, Physical Stimulation, Posture, Predictive Value of Tests, Proprioception, Vestibule, Labyrinth, Vestibular Nuclei, Head Movements

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