Identification, Localization, and Modulation of Neural Networks for Walking in the Mudpuppy (Necturus Maculatus) Spinal Cord

Abstract

We tested the hypothesis that the neural networks for walking in the mudpuppy can be divided into a flexor and an extensor center, each of which contains collections of interneurons localized in the vicinity of their motoneuron pools. Combining a battery of techniques, we identified and localized the elbow flexor center and its motoneuron pool in the C2 segment and the elbow extensor center and its motoneuron pool in the C3 segment. Rhythmic flexion or extension of the limb in isolation could be induced by continuous trains of current pulses of the C2 or C3 segments, respectively. Independent activation could also occur after application of glutamate receptor agonist NMDA. Part of segment C2 in isolation generated rhythmic elbow flexor bursts, whereas part of segment C3 in isolation generated rhythmic elbow extensor bursts. An isolated region spanning the C3 roots generated both flexor and extensor bursts. The step cycle was modulated in a phase-dependent manner by stimulation of the dorsal roots, the ventral roots, or either of the two centers. The effects of ventral root stimulation were removed by deafferentation to block reafferent input attributable to muscle contraction induced by the stimulation. We conclude that the neural networks for walking contain at least a flexor and an extensor generator that are localized in close apposition to the motoneuron pools, that the two centers can work independently despite the fact that there are reciprocal inhibitory interconnections between them, and that sensory input interacts with the spinal neural networks to reset the ongoing walking rhythm in a phase-dependent manner.

Predictions of Phase-Locking in Excitatory Hybrid Networks: Excitation Does Not Promote Phase-Locking in Pattern-Generating Networks as Reliably as Inhibition

“…For example, although it has been shown that patterned activity in the lamprey hemicord is supported by a population of excitatory neurons without any inhibition, the full system appears to be dominated by inhibition because coordination of left-right activity in the segmental half-center oscillators is lost when inhibition is blocked (Cangiano and Grillner 2005). In salamander (Cheng et al 1998) and mammalian spinal cord (McCrea and Rybak 2008), synchronized activity of flexor and extensor motor neurons has been observed in reciprocally coupled excitatory networks when inhibitory synaptic transmission was blocked. However, biologically relevant CPG coordination was again found to rely on one or several levels of half-center oscillators that organize alternating flexor-extensor motor neuron activation.…”

“…Leech heartbeat (Calabrese and Peterson 1983), pyloric and gastric networks of the STG (Marder and Calabrese 1996), lamprey swimming (Cangiano and Grillner 2005), salamander locomotor (Cheng et al 1998), and mammalian locomotor (McCrea and Rybak 2008) CPGs are all functionally dominated by inhibitory synapses, as evidenced by the lack of a single identified excitatory synapse in the first two systems listed. We present experimental and theoretical data showing that a CPG dominated by typical excitatory synapses would need to be carefully tuned to function and in many configurations would be highly sensitive to noise.…”

Simulation and Robotics Studies of Salamander Locomotion: Applying Neurobiological Principles to the Control of Locomotion in Robots

“…1, left) for the forelimbs and within the thoracic segments 14 to 18 for the hindlimbs (Székely and Czéh, 1976;Wheatley, 1992;Cheng et al, 1998). Evidence from spinal sections (Székely and Czéh, 1976) show that these regions can be decomposed into left and right neural centers, which independently coordinate with each limb.…”

Split-Belt Treadmill Stepping in Infants Suggests Autonomous Pattern Generators for the Left and Right Leg in Humans

“…Although the constituents of a module are unclear, we know that groups of neurons, such as neurons from each side of the spinal cord (Kudo and Yamada, 1987;Soffe, 1989) or neurons controlling a set of muscles (Cheng et al, 1998;Stein andDanielsMcQueen, 2002, 2004), have considerable rhythmogenic and autonomous ability. Behaviorally, the independence of each hemispinal cord can be reflected in the coordination of leg movements on a split-belt treadmill, in which the belts are run at different speeds.…”