A topographic map of recruitment in spinal cord

McLean, David L.; Fan, Jingyi; Higashijima, Shin‐ichi; Hale, Melina E.; Fetcho, Joseph R.

doi:10.1038/nature05588

Cited by 344 publications

(470 citation statements)

References 27 publications

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“…Having identified which neurons control particular motor patterns, we can now ask how their activity is decoded in the spinal cord to produce the associated behavior. Substantial progress has been made recently in understanding the organization and function of specific cell types and circuits in the zebrafish spinal cord [38][39][40] , encouraging the hope that a connection between descending motor commands and the resulting motor patterns is within reach. More obscure, however, is the upstream circuitry that leads to the selective activation of these descending control neurons.…”

Section: Discussionmentioning

confidence: 99%

Control of visually guided behavior by distinct populations of spinal projection neurons

et al. 2008

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A basic question in the field of motor control is how different actions are represented by activity in spinal projection neurons. We used a new behavioral assay to identify visual stimuli that specifically drive basic motor patterns in zebrafish. These stimuli evoked consistent patterns of neural activity in the neurons projecting to the spinal cord, which we could map throughout the entire population using in vivo two-photon calcium imaging. We found that stimuli that drive distinct behaviors activated distinct subsets of projection neurons, consisting, in some cases, of just a few cells. This stands in contrast to the distributed activation seen for more complex behaviors. Furthermore, targeted cell by cell ablations of the neurons associated with evoked turns abolished the corresponding behavioral response. This description of the functional organization of the zebrafish motor system provides a framework for identifying the complete circuit underlying a vertebrate behavior.In a behaving animal, the brain communicates its intentions to muscles via the pattern of activity in descending projection neurons 1 . In vertebrates, these cells respond to the detection and processing of sensory stimuli and transmit their motor command to the local networks of the spinal cord, which in turn initiate and coordinate muscle contraction 2 . A fundamental question in neuroscience is how the commands that initiate behaviors are encoded in the activation of these projection neurons 3-5 .The spinal projection system of fish provides an excellent model for studying this code 6 . A diverse range of swimming behaviors can be seen in 6-d-old zebrafish 7-9 that are mediated by a descending projection to the spinal cord consisting of fewer than 300 neurons 10,11 . These neurons are easily labeled with fluorescent indicators 12 , optically accessible with modern imaging techniques and arranged in a stereotyped pattern such that the same cells or groups of cells can easily be identified from one fish to the next 13 . These neurons are morphologically diverse, with distinct dendritic fields and axonal projection patterns 13,14 , suggesting that they serve different behavioral functions. Nevertheless, determining how differing patterns of activity in these spinal projection neurons produce different motor outputs has proved to be difficult. 23,24 , the actual command is encoded in distributed activity throughout the population of control neurons 2 .The swimming behaviors of zebrafish, including the complex sequence of turns and swims that make up the escape response, can be broken down into basic kinematic elements 8 . It is possible that the motor commands for these basic behaviors originate from distinct populations of neurons, which when combined would appear as a `distributed command'. We found that whole-field visual motion, with the direction dynamically locked to the fish's body axis, is able to selectively evoke some of these basic swim patterns. Calcium imaging of stimulus-evoked responses in the complete population of n...

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Section: Discussionmentioning

confidence: 99%

Control of visually guided behavior by distinct populations of spinal projection neurons

et al. 2008

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“…2D). In normal development (and presumably also in the absence of activity), MNs become functionally differentiated such that, by stage 42, they (i) can fire multiple impulses in each cycle of swimming; (ii) may " drop out" of the rhythm as it slows down and weakens, but become available if swimming speeds up and intensifies; and (iii) form a more heterogeneous pool comprising members with distinct electrical properties and synaptic drive, similar to zebrafish (10,26). This combination of changes provides the larval rhythm with increased flexibility because the intensity and frequency of rhythmic activation of the muscles can change dramatically on a cycle-by-cycle basis.…”

Section: Discussionmentioning

confidence: 99%

“…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. Two simpler model systems, the zebrafish and the Xenopus frog tadpole, generate fictive locomotion in the absence of drugs, which allows investigations of neuronal networks during near-normal operation and affords an opportunity to study how these networks emerge during development (3,10,13,14). We focused on changes in MNs controlling the swimming behavior of postembryonic Xenopus frog tadpoles.…”

Section: Discussionmentioning

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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“…These segments contain multiple classes of muscle fibers, including slow, fast, and intermediate types, with distinct mechanical and metabolic properties that constitute a "gearing" system adjustable to a wide range of speeds. The activity of a given segment is mostly independent of the others, and when, which, and how many fibers will be activated are determined by a neural network in the spinal cord (1)(2)(3). This neural mechanism by which contraction magnitude is varied is based on the logic for recruiting motor neurons into the active population, called the size principle (1)(2)(3)(4).…”

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confidence: 99%

A mechanism for graded motor control encoded in the channel properties of the muscle ACh receptor

Nishino

Baba

Okamura

2011

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

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The larva of the invertebrate chordate Ciona intestinalis possesses only 36 striated muscle cells and lacks body segmentation. It can swim, however, like a vertebrate tadpole, and how its simple body achieves such sophisticated motor control remains puzzling. We found that muscle contractions in Ciona larvae are variable and can be changed by sensory stimuli, so that neuromuscular transmission can convert the variable neural inputs into graded muscle activity. We characterized the molecular nature of the nicotinic acetylcholine receptor (nAChR) at neuromuscular synapses. When heterologously expressed in Xenopus oocytes, this nAChR channel exhibited two biophysical features resembling vertebrate neuronal nAChRs rather than the muscle type: inward rectification and high Ca 2+ permeability. Both of these properties were abolished by a simple mutation at the channel pore in one of the non-α subunits, called BGDE3, so as to adopt the sequence of related subunits in vertebrates, γ and ε. In vivo exchange of native BGDE3 with this mutant severely disrupted graded motor control, producing instead sporadic all-or-none-like flexions. The graded nature of excitation-contraction (E-C) coupling in this organism is based on the traits of the nAChR channel pore, which confer fine controllability on such a coarse motor architecture.ascidian larva | muscle physiology | locomotion | neuromuscular junction I n tailed aquatic vertebrates such as fish and amphibian tadpoles, swimming undulations are generated by sequential activation of the myotomal segments. These segments contain multiple classes of muscle fibers, including slow, fast, and intermediate types, with distinct mechanical and metabolic properties that constitute a "gearing" system adjustable to a wide range of speeds. The activity of a given segment is mostly independent of the others, and when, which, and how many fibers will be activated are determined by a neural network in the spinal cord (1-3). This neural mechanism by which contraction magnitude is varied is based on the logic for recruiting motor neurons into the active population, called the size principle (1-4). This control system for compound muscle fibers is likely a key innovation in vertebrates, but how far this basis can be traced back in invertebrate systems is poorly understood.Ascidians are marine invertebrates that constitute a sister clade of the vertebrates (5, 6). The larva of the ascidian Ciona intestinalis (L) is tadpole shaped and possesses bilateral muscle bands, a dorsal neural tube supported by an axial notochord, and sensory organs including a photoreceptive ocellus (Fig. 1A and Fig. S1A). Despite this suite of organs, the body of the Ciona larva is quite simple. The muscle band on each side lacks a segmental plan and is composed of only 18 cells arranged in a single layer (Fig. 1A and Fig. S1). The 4-5 pairs of cholinergic motor neurons located in the motor ganglion (or the visceral ganglion) have accounted for the swimming behavior (Fig. S1) (7-10). These cholinergic neurons project axons...

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A topographic map of recruitment in spinal cord

Cited by 344 publications

References 27 publications

Control of visually guided behavior by distinct populations of spinal projection neurons

Control of visually guided behavior by distinct populations of spinal projection neurons

Development of a spinal locomotor rheostat

A mechanism for graded motor control encoded in the channel properties of the muscle ACh receptor

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