Modular organization of motor behavior in the frog's spinal cord (original) (raw)
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Journal of Neurophysiology, 2009
Spinal circuits may organize trajectories using pattern generators and synergies. In frogs, prior work supports fixed-duration pulses of fixed composition synergies, forming primitives. In wiping behaviors, spinal frogs adjust their motor activity according to the starting limb position and generate fairly straight and accurate isochronous trajectories across the workspace. To test whether a compact description using primitives modulated by proprioceptive feedback could reproduce such trajectory formation, we built a biomechanical model based on physiological data. We recorded from hindlimb muscle spindles to evaluate possible proprioceptive input. As movement was initiated, early skeletofusimotor activity enhanced many muscle spindles firing rates. Before movement began, a rapid estimate of the limb position from simple combinations of spindle rates was possible. Three primitives were used in the model with muscle compositions based on those observed in frogs. Our simulations showe...
Development and neuromodulation of spinal locomotor networks in the metamorphosing frog
Journal of Physiology-Paris, 2006
Metamorphosis in the anuran frog, Xenopus laevis, involves profound structural and functional transformations in most of the organism's physiological systems as it encounters a complete alteration in body plan, habitat, mode of respiration and diet. The metamorphic process also involves a transition in locomotory strategy from axial-based undulatory swimming using alternating contractions of left and right trunk muscles, to bilaterally-synchronous kicking of the newly developed hindlimbs in the young adult. At critical stages during this behavioural switch, functional larval and adult locomotor systems co-exist in the same animal, implying a progressive and dynamic reconfiguration of underlying spinal circuitry and neuronal properties as limbs are added and the tail regresses. To elucidate the neurobiological basis of this developmental
Modules in the brain stem and spinal cord underlying motor behaviors
Journal of Neurophysiology, 2011
Previous studies using intact and spinalized animals have suggested that coordinated movements can be generated by appropriate combinations of muscle synergies controlled by the central nervous system (CNS). However, which CNS regions are responsible for expressing muscle synergies remains an open question. We address whether the brain stem and spinal cord are involved in expressing muscle synergies used for executing a range of natural movements. We analyzed the electromyographic (EMG) data recorded from frog leg muscles before and after transection at different levels of the neuraxis—rostral midbrain (brain stem preparations), rostral medulla (medullary preparations), and the spinal-medullary junction (spinal preparations). Brain stem frogs could jump, swim, kick, and step, while medullary frogs could perform only a partial repertoire of movements. In spinal frogs, cutaneous reflexes could be elicited. Systematic EMG analysis found two different synergy types: 1) synergies shared ...
Modular Premotor Drives and Unit Bursts as Primitives for Frog Motor Behaviors
The Journal of Neuroscience, 2004
Spinal cord modularity impacts on our understanding of reflexes, development, descending systems in normal motor control, and recovery from injury. We used independent component analysis and best-basis or matching pursuit wavepacket analysis to extract the composition and temporal structure of bursts in hindlimb muscles of frogs. These techniques make minimala prioriassumptions about drive and motor pattern structure. We compared premotor drive and burst structures in spinal frogs with less reduced frogs with a fuller repertoire of locomotory, kicking, and scratching behaviors. Six multimuscle drives explain most of the variance of motor patterns (∼80%). Each extracted drive was activated with pulses at a single time scale or common duration (∼275 msec) burst structure. The data show that complex behaviors in brainstem frogs arise as a result of focusing drives to smaller core groups of muscles. Brainstem drives were subsets of the muscle groups from spinal frogs. The 275 msec burst...
Development and functional organization of spinal locomotor circuits
Current opinion in neurobiology, 2011
The coordination and timing of muscle activities during rhythmic movements, like walking and swimming, are generated by intrinsic spinal motor circuits. Such locomotor networks are operational early in development and are found in all vertebrates. This review outlines and compares recent advances that have revealed the developmental and functional organization of these fundamental spinal motor networks in limbed and non-limbed animals. The comparison will highlight common principles and divergence in the organization of the spinal locomotor network structure in these different species as well as point to unresolved issues regarding the assembly and functioning of these networks.
A Neural Basis for Motor Primitives in the Spinal Cord
The Journal of Neuroscience, 2010
Motor primitives and modularity may be important in biological movement control. However, their neural basis is not understood. To investigate this, we recorded 302 neurons, making multielectrode recordings in the spinal cord gray of spinalized frogs, at 400, 800, and 1200 μm depth, at the L2/L3 segment border. Simultaneous muscle activity recordings were used with independent components analysis to infer premotor drive patterns. Neurons were divided into groups based on motor pattern modulation and sensory responses, depth recorded, and behavior. The 187 motor pattern modulated neurons recorded comprised 14 cutaneous neurons and 28 proprioceptive neurons at 400 μm in the dorsal horn, 131 intermediate zone interneurons from ∼800 μm depth without sensory responses, and 14 motoneuron-like neurons at ∼1200 μm. We examined all such neurons during spinal behaviors. Mutual information measures showed that cutaneous neurons and intermediate zone neurons were related better to premotor driv...
Flexibility of the axial central pattern generator network for locomotion in the salamander.
Ryczko D, Knüsel J, Crespi A, Lamarque S, Mathou A, Ijspeert AJ, Cabelguen JM. Flexibility of the axial central pattern generator network for locomotion in the salamander. In tetrapods, limb and axial movements are coordinated during locomotion. It is well established that inter-and intralimb coordination show considerable variations during ongoing locomotion. Much less is known about the flexibility of the axial musculoskeletal system during locomotion and the neural mechanisms involved. Here we examined this issue in the salamander Pleurodeles waltlii, which is capable of locomotion in both aquatic and terrestrial environments. Kinematics of the trunk and electromyograms from the mid-trunk epaxial myotomes were recorded during four locomotor behaviors in freely moving animals. A similar approach was used during rhythmic struggling movements since this would give some insight into the flexibility of the axial motor system. Our results show that each of the forms of locomotion and the struggling behavior is characterized by a distinct combination of mid-trunk motor patterns and cycle durations. Using in vitro electrophysiological recordings in isolated spinal cords, we observed that the spinal networks activated with bath-applied N-methyl-D-aspartate could generate these axial motor patterns. In these isolated spinal cord preparations, the limb motor nerve activities were coordinated with each mid-trunk motor pattern. Furthermore, isolated mid-trunk spinal cords and hemicords could generate the mid-trunk motor patterns. This indicates that each side of the cord comprises a network able to generate coordinated axial motor activity. The roles of descending and sensory inputs in the behavior-related changes in axial motor coordination are discussed. axial system; central pattern generator; locomotor flexibility; salamander
Linear combinations of primitives in vertebrate motor control
Proceedings of the National Academy of Sciences, 1994
Recent investigations on the spinalized frog have provided evidence suggesting that the neural circuits in the spinal cord are organized into a number of distinct functional modules. We have investigated the rule that governs the coactivation of two such modules. To this end, we have developed an experimental paradigm that involves the simultaneous stimulation of two sites in the frog's spinal cord and the quantitative comparison of the resulting mechanical response with the summation of the responses obtained from the stimulation of each site. We found that the simultaneous stimulation of two sites leads to the vector summation of the endpoint forces generated by each site separately. This linear behavior is quite remarkable and provides strong support to the view that the central nervous system may generate a wide repertoire of motor behaviors through the vectorial superposition of a few motor primitives stored within the neural circuits in the spinal cord.