Cited by 40Motor Control and AdaptationVestibular and auditory disordersNeurological disorders and treatments

Dysmetria and errors in predictions: the role of internal forward model

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Cabaraux, Pierre, Gandini, Jordi, Kakei, Shinji, Manto, Mario, Mitoma, Hiroshi, Tanaka, Hirokazu·2020·International Journal of Molecular Sciences

Abstract

The terminology of cerebellar dysmetria embraces a ubiquitous symptom in motor deficits, oculomotor symptoms, and cognitive/emotional symptoms occurring in cerebellar ataxias. Patients with episodic ataxia exhibit recurrent episodes of ataxia, including motor dysmetria. Despite the consensus that cerebellar dysmetria is a cardinal symptom, there is still no agreement on its pathophysiological mechanisms to date since its first clinical description by Babinski. We argue that impairment in the predictive computation for voluntary movements explains a range of characteristics accompanied by dysmetria. Within this framework, the cerebellum acquires and maintains an internal forward model, which predicts current and future states of the body by integrating an estimate of the previous state and a given efference copy of motor commands. Two of our recent studies experimentally support the internal-forward-model hypothesis of the cerebellar circuitry. First, the cerebellar outputs (firing rates of dentate nucleus cells) contain predictive information for the future cerebellar inputs (firing rates of mossy fibers). Second, a component of movement kinematics is predictive for target motions in control subjects. In cerebellar patients, the predictive component lags behind a target motion and is compensated with a feedback component. Furthermore, a clinical analysis has examined kinematic and electromyography (EMG) features using a task of elbow flexion goal-directed movements, which mimics the finger-to-nose test. Consistent with the hypothesis of the internal forward model, the predictive activations in the triceps muscles are impaired, and the impaired predictive activations result in hypermetria (overshoot). Dysmetria stems from deficits in the predictive computation of the internal forward model in the cerebellum. Errors in this fundamental mechanism result in undershoot (hypometria) and overshoot during voluntary motor actions. The predictive computation of the forward model affords error-based motor learning, coordination of multiple degrees of freedom, and adequate timing of muscle activities. Both the timing and synergy theory fit with the internal forward model, microzones being the elemental computational unit, and the anatomical organization of converging inputs to the Purkinje neurons providing them the unique property of a perceptron in the brain. We propose that motor dysmetria observed in attacks of ataxia occurs as a result of impaired predictive computation of the internal forward model in the cerebellum.

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  • The connectivity of the cerebellum is organized in a series of parallel loops with the cerebral cortex, the striatum, and the spinal cord, making the cerebellum a key sensorimotor interface: each region receives inputs from a specific region of the central nervous system and sends back projections to these same regions.

    “The connectivity of the cerebellum is organized in a series of parallel loops with the cerebral cortex, the striatum, and the spinal cord, which makes the cerebellum a key sensorimotor interface: each region of the cerebellum receives inputs from a specific region of the central nervous system, and sends back projections to these same regions (Sokolov et al., 2017; Diedrichsen et al., 2019; Cabar”

    From The Forward Model: A Unifying Theory for the Role of the Cerebellum in Motor Control and Sense of Agency (2021) · cites this paper as Cabaraux et al., 2020

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  • Some deficits observed in cerebellar patients could be explained by an impaired forward model resulting in increased dependence on delayed visual feedback.

    “Altogether, this suggests that some of the deficits observed in cerebellar patients could be explained by an impaired forward model resulting in increased dependence on delayed visual feedback (Kakei et al., 2019; Cabaraux et al., 2020; Tanaka et al., 2020; Zimmet et al., 2020).”
  • Patients with cerebellar lesions are impaired for on-line movement correction, with dysmetria and intention tremor as hallmarks of cerebellar ataxia.

    “Patients with cerebellar lesions are impaired for on-line movement correction: overshooting or undershooting the target (dysmetria) and oscillatory corrections (intention tremor) are the hallmarks of cerebellar ataxia, which can be broadly defined as inaccuracy and incoordination in limb movements and instability in posture, gait and ocular saccades (Holmes, 1939; Cabaraux et al., 2020).”

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Research works printed but not linked: 2

  1. [44]Manto M. Habas C. Le Cervelet, de L’anatomie et la Physiologie à la Clinique Humaine Springer-Verlag Paris, France 2013
  2. [54]Ito M. The Cerebellum Brain for an Implicit Self FT Press Upper Saddle River, NJ, USA 2012

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Authors
Cabaraux, P., Gandini, J., Kakei, S., Manto, M., Mitoma, H., & Tanaka, H.
Affiliations
  • HUmani - CHU Charleroi-Chimay (BE)
  • Tokyo Metropolitan Institute of Medical Science (JP)
  • University of Mons (BE)
  • Tokyo Medical University (JP)
  • Tokyo City University (JP)
Corresponding author
Mitoma, Hiroshi
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2020-09-20
Volume
21
Issue
18
Pages
6900
ISSN
1422-0067 (ISSN-L)
OpenAlex
W3087315882
Cited by
40
References
100
Citations by year
2026: 5 · 2025: 5 · 2024: 7 · 2023: 7 · 2022: 7 · 2021: 8 · 2020: 1
FWCI
0.78
Type
journal article
Language
en
Open access
Locations
  • International Journal of Molecular Sciences (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
  • Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
  • Health Sciences › Medicine › Neurology › Neurological disorders and treatments
Keywords
episodic ataxia, cerebellar ataxia, efference copy, dentate nucleus, mossy fibers, hypermetria, hypometria, finger-to-nose test, Purkinje cells, voluntary movement
MeSH terms
Cerebellar Ataxia, Cerebellum, Humans, Models, Neurological, Purkinje Cells

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