Special cellular and synaptic mechanisms in motor pattern generation (original) (raw)
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Simple cellular and network control principles govern complex patterns of motor behavior
Proceedings of the National Academy of Sciences, 2009
The vertebrate central nervous system is organized in modules that independently execute sophisticated tasks. Such modules are flexibly controlled and operate with a considerable degree of autonomy. One example is locomotion generated by spinal central pattern generator networks (CPGs) that shape the detailed motor output. The level of activity is controlled from brainstem locomotor command centers, which in turn, are under the control of the basal ganglia. By using a biophysically detailed, full-scale computational model of the lamprey CPG (10,000 neurons) and its brainstem/forebrain control, we demonstrate general control principles that can adapt the network to different demands. Forward or backward locomotion and steering can be flexibly controlled by local synaptic effects limited to only the very rostral part of the network. Variability in response properties within each neuronal population is an essential feature and assures a constant phase delay along the cord for different locomotor speeds.
Neuronal morphologies built for reliable physiology in a rhythmic motor circuit
eLife, 2019
It is often assumed that highly-branched neuronal structures perform compartmentalized computations. However, previously we showed that the Gastric Mill (GM) neuron in the crustacean stomatogastric ganglion (STG) operates like a single electrotonic compartment, despite having thousands of branch points and total cable length >10 mm (Otopalik et al., 2017a; 2017b). Here we show that compact electrotonic architecture is generalizable to other STG neuron types, and that these neurons present direction-insensitive, linear voltage integration, suggesting they pool synaptic inputs across their neuronal structures. We also show, using simulations of 720 cable models spanning a broad range of geometries and passive properties, that compact electrotonus, linear integration, and directional insensitivity in STG neurons arise from their neurite geometries (diameters tapering from 10-20 µm to < 2 µm at their terminal tips). A broad parameter search reveals multiple morphological and bioph...
Motor pattern specification by dual descending pathways to a lobster rhythm-generating network
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1999
In the European lobster Homarus gammarus, rhythmic masticatory movements of the three foregut gastric mill teeth are generated by antagonistic sets of striated muscles that are driven by a neural network in the stomatogastric ganglion. In vitro, this circuit can spontaneously generate a single (type I) motor program, unlike in vivo in which gastric mill patterns with different phase relationships are found. By using paired intrasomatic recordings, all elements of the gastric mill network, which consists mainly of motoneurons, have been identified and their synaptic relationships established. The gastric mill circuit of Homarus is similar to that of other decapod crustaceans, although some differences in neuron number and synaptic connectivity were found. Moreover, specific members of the lobster network receive input from two identified interneurons, one excitatory and one inhibitory, that project from each rostral commissural ganglion. Integration of input from these projection ele...
{R}egulation of motor patterns by the central spike-initiation zone of a sensory neuron
Sensory feedback from muscles and peripheral sensors acts to initiate, tune or reshape motor activity according to the state of the body. Yet, sensory neurons often show low levels of activity even in the absence of sensory input. Here we examine the functional role of spontaneous low-frequency activity of such a sensory neuron. The anterior gastric receptor (AGR) is a muscle-tendon organ in the crab stomatogastric nervous system whose phasic activity shapes the well-characterized gastric mill (chewing) and pyloric (filtering) motor rhythms. Phasic activity is driven by a spike-initiation zone near the innervated muscle. We demonstrate that AGR possesses a second spike-initiation zone, which is located spatially distant from the innervated muscle in a central section of the axon. This initiation zone generates tonic activity and is responsible for the spontaneous activity of AGR in vivo, but does not code sensory information. Rather, it is sensitive to the neuromodulator octopamine. A computational model indicates that the activity at this initiation zone is not caused by excitatory input from another neuron, but generated intrinsically. This tonic activity is functionally relevant, because it modifies the activity state of the gastric mill motor circuit and changes the pyloric rhythm. The sensory function of AGR is not impaired as phasic activity suppresses spiking at the central initiation zone. Our results thus demonstrate that sensory neurons are not mere reporters of sensory signals. Neuromodulators can elicit non-sensory coding activity in these neurons that shapes the state of the motor system.
Journal of Neurophysiology, 2002
Rhythm generation by the pyloric motor network in the stomatogastric ganglion (STG) of the spiny lobster requires permissive neuromodulatory inputs from other central ganglia. When these inputs to the STG are suppressed by cutting the single, mainly afferent stomatogastric nerve (stn), pyloric neurons cease to burst and the network falls silent. However, as shown previously, if such a decentralized quiescent ganglion is maintained in organ culture, pyloric network rhythmicity returns after 3–4 days and, although slower, is similar to the motor pattern expressed when the stn is intact. Here we use current- and voltage-clamp, primarily of identified pyloric dilator (PD) neurons, to investigate changes in synaptic and cellular properties that underlie this transition in network behavior. Although the efficacy of chemical synapses between pyloric neurons decreases significantly (by ≤50%) after STG decentralization, the fundamental change leading to rhythm recovery occurs in the voltage-...
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1988
Recordings from the lateral gastric (LG) neuron, which forms part of the gastric mill central pattern generator in the red lobster, Palinurus vulgaris, indicate that regenerative membrane properties (plateau properties) and synaptic inputs interact sequentially rather than simultaneously to determine its discharge pattern. LG thus presents a composite discharge, consisting of 2 separate segments of firing and one silent period. The first firing segment depends on regenerative membrane properties; this is the endogenous component, or segment, of LG's discharge. The second firing segment is the result of extrinsic synaptic input, forming the synaptic component of LG's discharge. The relative importance of these 2 components can vary, and thus LG's discharge ranges from one in which LG fires only as a result of its endogenous component to one in which its endogenous component is entirely absent and only the synaptic component underlies action potentials. Activity in an iden...