Measured motion: searching for simplicity in spinal locomotor networks

Grillner, Sten; Jessell, Thomas M.

doi:10.1016/j.conb.2009.10.011

Cited by 355 publications

(312 citation statements)

References 118 publications

(157 reference statements)

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“…In many model systems, rhythmic locomotor activity is drug-induced. Although this approach has greatly facilitated investigation of CPG networks, their neuromodulation, and their development (1)(2)(3)(4), it also constrains the networks to operate over a relatively narrow range of possible output configurations, producing a single mode of operation dictated by the concentration and mixture of the drugs. This approach therefore precludes an appreciation of the complexity of naturally evoked and sustained motor network activity, which can operate like a rheostat over an almost infinitely wide range of frequencies and intensities.…”

Section: Discussionmentioning

confidence: 99%

“…During locomotion, sensory information interacts with central pattern generator (CPG) networks in the spinal cord, which in turn provide command signals to motorneurons (MNs) to sequence and guide movements appropriately (1). CPGs develop before locomotion is possible (2)(3)(4). Initially, however, the output of immature CPGs lacks the precision and flexibility that typifies adult locomotion.…”

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confidence: 99%

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Development of a spinal locomotor rheostat

Zhang

Issberner

Sillar

2011

Proc. Natl. Acad. Sci. U.S.A.

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Locomotion in immature animals is often inflexible, but gradually acquires versatility to enable animals to maneuver efficiently through their environment. Locomotor activity in adults is produced by complex spinal cord networks that develop from simpler precursors. How does complexity and plasticity emerge during development to bestow flexibility upon motor behavior? And how does this complexity map onto the peripheral innervation fields of motorneurons during development? We show in postembryonic Xenopus laevis frog tadpoles that swim motorneurons initially form a homogenous pool discharging single action potential per swim cycle and innervating most of the dorsoventral extent of the swimming muscles. However, during early larval life, in the prelude to a free-swimming existence, the innervation fields of motorneurons become restricted to a more limited sector of each muscle block, with individual motorneurons reaching predominantly ventral, medial, or dorsal regions. Larval motorneurons then can also discharge multiple action potentials in each cycle of swimming and differentiate in terms of their firing reliability during swimming into relatively high-, medium-, or low-probability members. Many motorneurons fall silent during swimming but can be recruited with increasing locomotor frequency and intensity. Each region of the myotome is served by motorneurons spanning the full range of firing probabilities. This unfolding developmental plan, which occurs in the absence of movement, probably equips the organism with the neuronal substrate to bend, pitch, roll, and accelerate during swimming in ways that will be important for survival during the period of free-swimming larval life that ensues.motor system | central pattern generator | ontogeny A dult vertebrates navigate through their environment with incredible agility and flexibility, a feature of locomotory behavior that is often critical for survival. During locomotion, sensory information interacts with central pattern generator (CPG) networks in the spinal cord, which in turn provide command signals to motorneurons (MNs) to sequence and guide movements appropriately (1). CPGs develop before locomotion is possible (2-4). Initially, however, the output of immature CPGs lacks the precision and flexibility that typifies adult locomotion. Therefore, postembryonic development must involve a period during which the central motor control circuitry is modified to accommodate the behavioral requirements of later stages. Much is known about the molecular mechanisms responsible for the differentiation of neuronal components of the motor system, motor axon trajectories, and innervation patterns (5-7). However, how this links to the functional development of these components has not been fully resolved, although there is ample evidence that activity itself is influential as a developmental signal (8, 9).Recent evidence has revealed a topographic recruitment order for dorsoventrally arranged spinal premotor interneurons and MNs during changes in swimming speed in larval ...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Development of a spinal locomotor rheostat

Zhang

Issberner

Sillar

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…Similarly, while walking on a narrow rocky path, stride length is modified constantly to optimize foot placement and avoid obstacles. Whether the input to achieve these modifications originates from the cortex or the peripheral afferents, the locomotor CPGs require a high degree of flexibility to integrate this information and generate smooth, task-dependent output (El Manira, 2014;Grillner and El Manira, 2015).…”

Section: Introductionmentioning

confidence: 99%

Delineating the Diversity of Spinal Interneurons in Locomotor Circuits

et al. 2017

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Locomotion is common to all animals and is essential for survival. Neural circuits located in the spinal cord have been shown to be necessary and sufficient for the generation and control of the basic locomotor rhythm by activating muscles on either side of the body in a specific sequence. Activity in these neural circuits determines the speed, gait pattern, and direction of movement, so the specific locomotor pattern generated relies on the diversity of the neurons within spinal locomotor circuits. Here, we review findings demonstrating that developmental genetics can be used to identify populations of neurons that comprise these circuits and focus on recent work indicating that many of these populations can be further subdivided into distinct subtypes, with each likely to play complementary functions during locomotion. Finally, we discuss data describing the manner in which these populations interact with each other to produce efficient, task-dependent locomotion.

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“…The mammalian locomotor networks have also been studied by using the adult cat where locomotor-like activity similarly can be induced pharmacologically or electrically (7)(8)(9). A general notion from these studies is that forelimb and hindlimb locomotion are controlled by independent limb-controlling circuits (10) and that rhythm-generating excitatory neurons, and pattern-generating neurons, interact to produce the coordinated motor output (11)(12)(13)(14). The network layout within these limb-controlling circuits has, however, been debated.…”

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Optogenetic dissection reveals multiple rhythmogenic modules underlying locomotion

Hägglund

Dougherty

Borgius

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

163

181

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Neural networks in the spinal cord known as central pattern generators produce the sequential activation of muscles needed for locomotion. The overall locomotor network architectures in limbed vertebrates have been much debated, and no consensus exists as to how they are structured. Here, we use optogenetics to dissect the excitatory and inhibitory neuronal populations and probe the organization of the mammalian central pattern generator. We find that locomotor-like rhythmic bursting can be induced unilaterally or independently in flexor or extensor networks. Furthermore, we show that individual flexor motor neuron pools can be recruited into bursting without any activity in other nearby flexor motor neuron pools. Our experiments differentiate among several proposed models for rhythm generation in the vertebrates and show that the basic structure underlying the locomotor network has a distributed organization with many intrinsically rhythmogenic modules.channelrhodopsin-2 | halorhodopsin | motor neurons | interneurons S pinal cord networks that drive and coordinate walking are, to a large extent, innate. Even in species that do not walk at birth, such as rodents and humans, the networks that generate walking are already present (1, 2). The early development of functional locomotor networks has been exploited and studied in the neonatal rodent spinal cord in vitro preparation in which locomotor-like activity can be induced pharmacologically or by electrical activation of descending or afferent fibers (3-6). The mammalian locomotor networks have also been studied by using the adult cat where locomotor-like activity similarly can be induced pharmacologically or electrically (7-9). A general notion from these studies is that forelimb and hindlimb locomotion are controlled by independent limb-controlling circuits (10) and that rhythm-generating excitatory neurons, and pattern-generating neurons, interact to produce the coordinated motor output (11)(12)(13)(14). The network layout within these limb-controlling circuits has, however, been debated. A number of conceptual models have been advanced. The classical half-center model asserts that flexor and extensor bursting is generated by two reciprocally coupled half-centers driving all flexors and extensors (8, 15). The flexor burst generator model is asymmetric and consists of a flexor burst generator that provides active excitation of flexor motor neurons and inhibition of extensor motor neurons that are otherwise tonically active (14,16,17). In response to evidence that the central pattern generator (CPG) could produce a more complex motor output than just a mere flexor-extensor alternation (9), the unit burst generator (UBG) model was proposed (18). According to this theory, separate modules can generate a rhythm in close muscle synergies and are distributed around each joint (18,19), or in the swimming network in each hemisegment (20). The UBGs therefore generate a local rhythmic activity that during locomotion will be recruited so that they form an interconnected n...

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Measured motion: searching for simplicity in spinal locomotor networks

Cited by 355 publications

References 118 publications

Development of a spinal locomotor rheostat

Development of a spinal locomotor rheostat

Delineating the Diversity of Spinal Interneurons in Locomotor Circuits

Optogenetic dissection reveals multiple rhythmogenic modules underlying locomotion

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