Spinal microcircuits comprising dI3 interneurons are necessary for motor functional recovery following spinal cord transection

Bui, Tuan V.; Stifani, Nicolas; Akay, Turgay; Brownstone, Robert M.

doi:10.7554/elife.21715

Cited by 47 publications

(49 citation statements)

References 71 publications

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“…Kinematics were post‐processed using the motion analysis software Motus (Vicon Motion Systems, GBR) or custom‐made software written by Dr Nicolas Stifani with ImageJ (KinemaJ) and R (KinemaR) (Bui et al . ; Fiander et al . ).…”

Section: Methodsmentioning

confidence: 99%

“…Due to the large slippage of the skin above the knee joint, the knee values were calculated by triangulation using the hip and ankle coordinates together with the measured length of femur and tibia (Pearson et al 2005). Kinematics were post-processed using the motion analysis software Motus (Vicon Motion Systems, GBR) or custom-made software written by Dr Nicolas Stifani with ImageJ (KinemaJ) and R (KinemaR) (Bui et al 2016;Fiander et al 2017). None of the animals was trained for the experiments to avoid the possible complications of different learning capabilities.…”

Section: Emg and Kinematics Recordingsmentioning

confidence: 99%

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Modular organization of murine locomotor pattern in the presence and absence of sensory feedback from muscle spindles

Santuz

Akay

Mayer

et al. 2019

The Journal of Physiology

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Key points Locomotion on land and in water requires the coordination of a great number of muscle activations and joint movements. Constant feedback about the position of own body parts in relation to the surrounding environment and the body itself (proprioception) is required to maintain stability and avoid failure. The central nervous system may follow a modular type of organization by controlling muscles in orchestrated groups (muscle synergies) rather than individually. We used this concept on genetically modified mice lacking muscle spindles, one of the two main classes of proprioceptors. We provide evidence that proprioceptive feedback is required by the central nervous system to accurately tune the modular organization of locomotion. Abstract For exploiting terrestrial and aquatic locomotion, vertebrates must build their locomotor patterns based on an enormous amount of variables. The great number of muscles and joints, together with the constant need for sensory feedback information (e.g. proprioception), make the task of controlling movement a problem with overabundant degrees of freedom. It is widely accepted that the central nervous system may simplify the creation and control of movement by generating activation patterns common to muscle groups, rather than specific to individual muscles. These activation patterns, called muscle synergies, describe the modular organization of movement. We extracted synergies through electromyography from the hind limb muscle activities of wild‐type and genetically modified mice lacking sensory feedback from muscle spindles. Muscle spindle‐deficient mice underwent a modification of the temporal structure (motor primitives) of muscle synergies that resulted in diminished functionality during walking. In addition, both the temporal and spatial (motor modules) components of synergies were severely affected when external perturbations were introduced or when animals were immersed in water. These findings show that sensory feedback from group Ia/II muscle spindles regulates motor function in normal and perturbed walking. Moreover, when group Ib Golgi tendon organ feedback is lacking due to enhanced buoyancy, the modular organization of swimming is almost completely compromised.

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Section: Methodsmentioning

confidence: 99%

Section: Emg and Kinematics Recordingsmentioning

confidence: 99%

Modular organization of murine locomotor pattern in the presence and absence of sensory feedback from muscle spindles

Santuz

Akay

Mayer

et al. 2019

The Journal of Physiology

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“…Which interneurons are responsible for phasically gating the sensory transmission? One likely component is the dl3 interneurons that are activated by low-threshold cutaneous afferents and project to both motoneurons and the CPG (74,75). Moreover, they are rhythmically modulated by the CPG and would thus seem well suited to be part of this circuit.…”

Section: E Phase-dependent Reflex Reversals Help Correct For Obstaclmentioning

confidence: 99%

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Grillner

Manira

2020

Physiological Reviews

363

395

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The vertebrate control of locomotion involves all levels of the nervous system from cortex to the spinal cord. Here, we aim to cover all main aspects of this complex behavior, from the operation of the microcircuits in the spinal cord to the systems and behavioral levels and extend from mammalian locomotion to the basic undulatory movements of lamprey and fish. The cellular basis of propulsion represents the core of the control system, and it involves the spinal central pattern generator networks (CPGs) controlling the timing of different muscles, the sensory compensation for perturbations, and the brain stem command systems controlling the level of activity of the CPGs and the speed of locomotion. The forebrain and in particular the basal ganglia are involved in determining which motor programs should be recruited at a given point of time and can both initiate and stop locomotor activity. The propulsive control system needs to be integrated with the postural control system to maintain body orientation. Moreover, the locomotor movements need to be steered so that the subject approaches the goal of the locomotor episode, or avoids colliding with elements in the environment or simply escapes at high speed. These different aspects will all be covered in the review.

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“…Kinematics were post-processed using the motion analysis software Motus (Vicon Motion Systems, GBR) or a custom-made software written by Dr. Nicolas Stifani with ImageJ (KinemaJ) and R (KinemaR) (61,62). None of the animals were trained for the experiments to avoid the possible complications of different learning capabilities.…”

Section: Methodsmentioning

confidence: 99%

Modular organization of the murine locomotor pattern in presence and absence of sensory feedback from muscle spindles

Santuz

Akay

Mayer

et al. 2018

Preprint

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For exploiting terrestrial and aquatic locomotion, vertebrates must build their locomotor patterns based on an enormous amount of variables. The great number of muscles and joints, together with the constant need for sensory feedback information (e.g. proprioception), make the task of creating and controlling movement a problem with overabundant degrees of freedom. It is widely accepted that the central nervous system might simplify the creation and control of movement. This could happen through the generation of activation patterns, which are common to many different muscles, rather than specific to individual muscles. These activation patterns, called muscle synergies, can be extracted from electromyographic data and describe the modular organization of movement. We extracted muscle synergies from the hindlimb muscle activities of wild type and genetically modified mice, in which sensory feedback from muscle spindles is eliminated. Muscle spindle-deficient mice underwent a modification of the temporal structure (motor primitives) of muscle synergies that resulted in diminished functionality during walking. In addition, both the temporal and spatial components (motor modules) of muscle synergies were severely affected when external perturbations were introduced of when animals were immersed in water. These findings show that group Ia/II sensory feedback from muscle spindles regulates motor function in normal and perturbed walking. Moreover, when group Ib Golgi tendon organ feedback is lacking due to the reduction of gravitational load in conditions of enhanced buoyancy, the modular organization of swimming is almost completely compromised. Significance statementLocomotion on land and in water requires the coordination of a great number of muscle activations and joint movements. Moreover, constant feedback about the position of own body parts in relation to the surrounding environment and the body itself (proprioception) is required to maintain stability and avoid failure. The theory of muscle synergies states that the central nervous system might control muscles in orchestrated groups (synergies) rather than individually. We used this concept on genetically modified mice, lacking one of the two classes of proprioceptors. Our results provide evidence that proprioceptive feedback is required by the central nervous system to accurately tune the modular organization of locomotion. IntroductionIn order to move through different environments, vertebrates must coordinate an overwhelming number of muscles and joints. The complex task of generating and controlling movement is achieved by a fine interplay of muscle activations, originated from and tuned by the brain and spinal cord (i.e. the central nervous system, CNS). Sensory feedback to the CNS plays a significant role in influencing the control of movement patterns. For instance, the ability to sense the position of own body parts in relation to the surrounding environment and the body itself, called proprioception, is of clear importance (1). During locomotion, the ...

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Spinal microcircuits comprising dI3 interneurons are necessary for motor functional recovery following spinal cord transection

Cited by 47 publications

References 71 publications

Modular organization of murine locomotor pattern in the presence and absence of sensory feedback from muscle spindles

Modular organization of murine locomotor pattern in the presence and absence of sensory feedback from muscle spindles

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Modular organization of the murine locomotor pattern in presence and absence of sensory feedback from muscle spindles

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