Abstract

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.

Highlights

  • THE BUILDING BLOCKS OF THE...LOCOMOTION IN HUMANS AND...SELECTION OF BEHAVIOR: ROLE OF...THE LOCOMOTOR COMMAND SYSTEMS... 281DOWNSTREAM PROJECTIONS FROM... 282TRANSITION FROM STANDING TO...THE SPINAL COORDINATION OF...CENTRAL PATTERN GENERATION

  • This review summarizes the logics of the neural control of motion extending from the basal ganglia mechanisms responsible for selection of behavior and cortex for precision walking to the cellular and molecular design of the central pattern generator networks in the brain stem-spinal cord

  • Specific neural circuits are dedicated to serve each of these functions, often referred to as central pattern generator circuits (CPGs) or motor programs

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Summary

INTRODUCTION

“To move things is all that mankind can do, and for this the sole executant is a muscle, whether it be whispering a syllable or felling a forest.” This quote from Charles S. CPG circuits in the spinal cord are essential for the propulsive aspect of locomotor movements as they produce the complex motor pattern corresponding to swimming, flying, or walking [201] They act as a processing interface to integrate sensory feedback and instructive signals from the brain to optimize the execution of locomotor movements [393]. The analyses of the organization and function of locomotor circuits have traditionally relied mostly on electrophysiological and anatomical approaches to define sets of interneurons essential for generating the motor pattern and map their connectivity In this regard, accessible vertebrate preparations such as the lamprey and Xenopus tadpole have unraveled many of the fundamental principles of organization at the spinal level with ipsilateral excitatory drive combined with reciprocal inhibition [70, 387] that represents the backbone of the spinal locomotor circuits in all vertebrates. Clearly of critical importance, we will only marginally include biomechanical aspects [94, 160, 163, 202, 213, 354, 451] and only very briefly the area of spinal cord injury

THE BUILDING BLOCKS OF THE LOCOMOTOR SYSTEM
The Basic Propulsive Synergy
Initiation of Locomotion from Locomotor Command Areas
The Goal-Directed Aspect of the Locomotor System and Precision Walking
Intersegmental and Interlimb Coordination in Vertebrate Locomotion
LOCOMOTION IN HUMANS AND TETRAPODS
Months
SELECTION OF BEHAVIOR
Role of Motor Cortex for Precision Walking and Steering
A Locomotion with accurate positioning of limbs
Role of Basal Ganglia and Related Structures
The basal ganglia “indirect pathway” reduces locomotor activity
Basal ganglia in evolution: a conserved structure
Lamprey and Lower Vertebrates
Glutamatergic reticulospinal neurons drive the spinal CPGs
Modulator action via the 5-HT system contributes to spinal locomotor control
Conclusion
TRANSITION FROM STANDING TO LOCOMOTION AND BACK
Stop Cells Control the Termination of Locomotor Episodes
Spinal Tetrapods Can Generate WellCoordinated Locomotor Movements
Plasticity of the Spinal CPG
Spinal Coordination of Undulatory Locomotion
Spinal Cord Injury
Historical Account
The Complex Motor Pattern Retained After Deafferentation
Alternating Activity in Swimming
Concepts Regarding the Overall Organization of the Limb Control in Mammals
THE INTRINSIC FUNCTION OF CPGs
CPG for Rhythm and Coordination?
Identification of the Interneurons Generating Locomotion
Rhythm generation
Coordination of swimming at the segmental level
Undulatory locomotion through intersegmental coordination
Fine-tuning of the locomotor network through metabotropic receptors
Zebrafish
Modular organization
Neuronal diversity and task-specific circuit architecture
Interneurons involved in coordination
Motoneurons are bona fide members of the CPG: evidence from zebrafish
Mouse Circuit Organization
Flexor-extensor coordination
Left-right coordination
Coordination along the body
Sensory Interaction with the Spinal CPG
B Mechanism of entrainment
Role of Sensory Signals Reporting Hip Position
Support phase and transition to swing: lift off
Swing phase and the transition to support: touch down
Contribution of Muscle Spindles and Cutaneous Input
Rapid Corrections During the Support Phase
Vestibular Stabilization During Swimming
The Control of Body Orientation in Tetrapods During Standing and Locomotion
STEERING OF LOCOMOTOR MOVEMENTS
ROLE OF CEREBELLUM
Cerebellar Learning and Locomotor Coordination
In Conclusion
Findings
CONCLUDING REMARKS
Full Text
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