DS0401 - Une nouvelle représentation du vivant

Movement control and prediction in Earth’s gravitoinertial field – MOTION

We investigated how the G-I forces are used by the brain to control arm movements. There is growing evidence that corticospinal control differs between eccentric and concentric contractions. Using transcranial magnetic and peripheral neural stimulations, we will test the hypothesis that the control of these contractions depends on G-related cues, but recruits differently the primary motor cortex and spinal cord circuits. MOTION will study the neural and functional mechanisms underlying the vestibular-based control of arm movements (testing healthy and vestibular-defective individuals). By means of EMG and EEG, we will test the prediction that the excitability to vestibular input increases when planning movements subjected to G force. Thanks to the plasticity of the motor system, one can adapt to new G-I fields. With experiments performed in OG- and 2G, we will test whether the newly updated internal model can also be used by the brain to control ongoing movements. We will make the first investigation with a view to assessing the possibility of using macaques as a non-human primate model for studying the integration of G in the arm motor commands. This will be done by investigating the potential role of G-related otolith signals for controlling limb movements in healthy and labyrinthectomized macaques. MOTION project will also exploit the mental simulation technique to investigate predictive mechanisms related G-I forces. We will use fMRI to determine whether brain regions that are known to host internal representation of G (e.g., insula) are recruited during mental simulation of movements subjected to G. We will also test whether the mental training of movements exposed to G-I forces (e.g., reaching for a target while sitting on a rotating platform) could lead to sensorimotor adaptation and decrease the detrimental effect of the forces acting on the arm when the movements are really performed during rotations.

1. We found a modulation of movement kinematics with the direction of the movement and, consequently, according to the gravitational torque applied to the arm. These observations show the fundamental role of gravity in the planning of motion in three-dimensional space. Publications eLife and Journal of Neurophysilogy.
2. We found an activation of the insular cortex (vestibular cortex) during vertical but not horizontal movements. These results indicate that an internal representation of the gravity, whose neural site is in the insular cortex, is engaged during the execution of the vertical movements. Publication Neuroscience.
3. The activation of the insular cortex is also present during the mental simulation of the movement, i.e., when no interaction with the environment takes place. An article is being written.
4. We found that the cortico-spinal control of an eccentric action (gravity-aided movement) is different from the control of an eccentric action (movement in the direction of gravity). An article is being written.
5. We have revealed the existence of 2 cortical networks capable of planning arm movements from vestibular information. A sensorimotor-type frontal network that transforms vestibular information relatively directly into motor commands, and a more complex parieto-frontal network that would allow the planning of movements based on visuospatial representations constructed from vestibular information.
6. We found that the vestibular system provided the necessary information to the motor system for optimization of movement. An article is being written.

With our proposal, we wish to uncover for the first time the cortical processes associated with the gravito-inertial control of arm movements. Information that we will gain from healthy and impaired (vestibularly, proprioceptively) humans and monkeys is likely to be of (in)valuable values for defining effective therapeutic strategies for people with vestibular lesions. Importantly, we will test the possibility of using macaque as a non-human primate model for investigating vestibular-induced arm movements.
Our results are promising and open interesting issues fir further research on this topic. The partners are very happy of their collaboration and results and plan to collaborate again in the future. For instance, a new proposal, on the influence of gravity force on motion perception and control, has been submitted to NIH by the partner 3 (Angelaki) with the partner 1 (Papaxanthis) as collaborator. The partners 1 (Papaxanthis) & 2 (Blouin) plan to submit soon new proposals (ANR, Europe) upon the influence of gravito-inertial forces on motor learning and adaptation.

1. Rousseau C, Papaxanthis C, Gaveau J, Pozzo T, White O. (2016) Initial information prior to movement onset influences kinematics of upward arm pointing movements. J Neurophysiol. 1;116(4):1673-1683.
2. Rousseau C, Fautrelle L, Papaxanthis C, Fadiga L, Pozzo T, White O (2016) Direction-dependent activation of the insular cortex during vertical and horizontal hand movements. Neuroscience 14;325:10-9.
3. Bock O, Schott N, Papaxanthis C (2015) Motor imagery: lessons learned in movement science might be applicable for spaceflight. Front Syst Neurosci.18;9:75.
4. Rousseau C, Fautrelle L, Papaxanthis C, Pozzo T, White O (2015) The insular cortex integrates proprioceptive information sensitive to gravity. ESMRMB. Edimburgh, UK.
5. Lebon F, Traverse E, Fadiga L, Pozzo T, Papaxanthis C (2015) The integration of gravity of implicit and explicit motor representation.Society for Neuroscience Conference. Chicago, IL, USA.
6. Blouin J, Saradjian AH, Pialasse J-P, Manson G, Mouchnino L, Simoneau M (2017) Two neural circuits to point home position after body displacement. Neural Control of Movement, Dublin
7. C. Papaxanthis La gravité Incarnée (2016). 50ème Congrès de la Société Internationale d'Otoneurologie (France). Invité par le président de la Société.
8. C. Papaxanthis Optimal integration of gravity cues (2016). Laboratoire Euromove, Montpellier (France).
9. Blouin, J (2017) Contrôle de la motricité des membres supérieurs: une fonction oubliée du système vestibulaire. GDR Vertige, Marseille (invité)

Submission summary

Because our body is permanently exposed to the Earth's gravity (G), the way that the CNS deals with -and represents- gravito-inertial (G-I) forces is an important issue in motor and cognitive neuroscience. Indeed, the CNS must finely tune the motor commands according to the G-I force field in order to produce coordinated arm movements and preserve autonomy. Surprisingly, most of the investigations in the field of motor control have ignored two important aspects of arm movements: i) they are under the constraints imposed by the Earth’s G and ii) they are often produced simultaneously with whole-body motion that creates additional forces on the arm (e.g., Coriolis). This constitutes a severe limitation in understanding how the CNS plans and controls motor actions. In light of this, we built the theory-driven MOTION project which is based on contemporary motor control models proposing that motor commands are produced according to an internal model of the environment and task dynamics (internal model theory). The aim of this project, presented by our consortium of two French and one American (with relative NIH grant) Partners, is to investigate how the internal representations of G-I forces are developed and used by the brain to control arm movements. There is growing evidence that corticospinal control differs between eccentric contraction (i.e., the muscle is lengthening, due to G) and concentric contraction (i.e., the muscle is shortening). Using transcranial magnetic and peripheral neural stimulations, we will test the hypothesis that the control of eccentric and concentric contractions depends on G-related cues, but recruits differently the primary motor cortex and spinal cord circuits. To build up an internal model of G-I forces, the brain strongly relies upon vestibular information. A challenging objective of MOTION project is to uncover the neural and functional mechanisms underlying the vestibular-based control of arm movements (testing healthy and vestibular-defective individuals). By means of EMG and EEG, we will test the prediction that the excitability to vestibular input increases when planning movements subjected to G force. Thanks to the plasticity of the sensorimotor system, one can adapt to new G-I fields and show accurate movements after short exposure periods. With experiments performed in micro- and hypergravity, we will test whether the newly updated internal model, which is thought to be critical for movement planning, can also be used by the brain to control ongoing movements (e.g., when the spatial goal suddenly changes during the movements). We will make the first investigation with a view to assessing the possibility of using macaques as a non-human primate model for studying the integration of G in the arm motor commands. This will be done by investigating the potential role of G-related otolith signals for controlling limb movements in healthy and labyrinthectomized macaques. The last axis of MOTION project will exploit the mental simulation technique to investigate predictive mechanisms related G-I forces. We will use fMRI to determine whether brain regions that are known to host internal representation of G (e.g., insula) are recruited during mental simulation of movements subjected to G. We will also test whether the mental training of movements exposed to G-I forces (e.g., reaching for a target while sitting on a rotating platform) could lead to sensorimotor adaptation and decrease the detrimental effect of the forces acting on the arm when the movements are really performed during rotations. We will give a high priority to the training of highly qualified personnel and to the dissemination and exploitation of the results throughout the Motion project. Opportunity will be provided to graduate students and postdoctoral fellows to acquire theoretical and technical backgrounds related to the cognitive and motor issues developed in our project in the form of internships in both French Partners' institutes.

Project coordination

Charalambos PAPAXANTHIS (CAPS (Cognition, Action et Plasticité Sensorimotrice), UMR INSERM 1093)

The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.

Partner

Baylor College of Medicine Department of Psychology and Electrical and Computer Engineering
CNRS DR12_LNC Centre National de la Recherche Scientifique Délégation Provence et Corse_Laboratoire de Neurosciences Cognitives
Université de Bourgogne CAPS (Cognition, Action et Plasticité Sensorimotrice), UMR INSERM 1093

Help of the ANR 229,559 euros
Beginning and duration of the scientific project: September 2014 - 36 Months

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