Endogenous and Network Properties of LymnaeaFeeding Central Pattern Generator Interneurons

2002 ◽  
Vol 88 (4) ◽  
pp. 1569-1583 ◽  
Author(s):  
Volko A. Straub ◽  
Kevin Staras ◽  
György Kemenes ◽  
Paul R. Benjamin
Keyword(s):  
Central Pattern Generator ◽  
Activity Patterns ◽  
Pattern Generator ◽  
Pattern Generation ◽  
Detailed Knowledge ◽  
Rhythm Generation ◽  
Cell Type ◽  
Intrinsic Properties ◽  
Plateau Potential ◽  
Network Properties

Understanding central pattern generator (CPG) circuits requires a detailed knowledge of the intrinsic cellular properties of the constituent neurons. These properties are poorly understood in most CPGs because of the complexity resulting from interactions with other neurons of the circuit. This is also the case in the feeding network of the snail, Lymnaea, one of the best-characterized CPG networks. We addressed this problem by isolating the interneurons comprising the feeding CPG in cell culture, which enabled us to study their basic intrinsic electrical and pharmacological cellular properties without interference from other network components. These results were then related to the activity patterns of the neurons in the intact feeding network. The most striking finding was the intrinsic generation of plateau potentials by medial N1 (N1M) interneurons. This property is probably critical for rhythm generation in the whole feeding circuit because the N1M interneurons are known to play a pivotal role in the initiation of feeding cycles in response to food. Plateau potential generation in another cell type, the ventral N2 (N2v), appeared to be conditional on the presence of acetylcholine. Examination of the other isolated feeding CPG interneurons [lateral N1 (N1L), dorsal N2 (N2d), phasic N3 (N3p)] and the modulatory slow oscillator (SO) revealed no significant intrinsic properties in relation to pattern generation. Instead, their firing patterns in the circuit appear to be determined largely by cholinergic and glutamatergic synaptic inputs from other CPG interneurons, which were mimicked in culture by application of these transmitters. This is an example of a CPG system where the initiation of each cycle appears to be determined by the intrinsic properties of a key interneuron, N1M, but most other features of the rhythm are probably determined by network interactions.

Glutamatergic N2v Cells Are Central Pattern Generator Interneurons of the Lymnaea Feeding System: New Model for Rhythm Generation

1997 ◽  
Vol 78 (6) ◽  
pp. 3396-3407 ◽  
Author(s):  
M. J. Brierley ◽  
M. S. Yeoman ◽  
P. R. Benjamin
Keyword(s):  
Central Pattern Generator ◽  
Synaptic Connection ◽  
Giant Cells ◽  
Pattern Generator ◽  
Synaptic Connections ◽  
Rhythm Generation ◽  
Feeding System ◽  
New Model ◽  
Feeding Cycle ◽  
Protraction Phase

Brierley, M. J., M. S. Yeoman, and P. R. Benjamin. Glutamatergic N2v cells are central pattern generator interneurons of the Lymnaea feeding system: new model for rhythm generation. J. Neurophysiol. 78: 3396–3407, 1997. We aimed to show that the paired N2v (N2 ventral) plateauing cells of the buccal ganglia are important central pattern generator (CPG) interneurons of the Lymnaea feeding system. N2v plateauing is phase-locked to the rest of the CPG network in a slow oscillator (SO)-driven fictive feeding rhythm. The phase of the rhythm is reset by artificially evoked N2v bursts, a characteristic of CPG neurons. N2v cells have extensive input and output synaptic connections with the rest of the CPG network and the modulatory SO cell and cerebral giant cells (CGCs). Synaptic input from the protraction phase interneurons N1M (excitatory), N1L (inhibitory), and SO (inhibitory-excitatory) are likely to contribute to a ramp-shaped prepotential that triggers the N2v plateau. The prepotential has a highly complex waveform due to progressive changes in the amplitude of the component synaptic potentials. Most significant is the facilitation of the excitatory component of the SO → N2v monosynaptic connection. None of the other CPG interneurons has the appropriate input synaptic connections to terminate the N2v plateaus. The modulatory function of acetylcholine (ACh), the transmitter of the SO and N1M/N1Ls, was examined. Focal application of ACh (50-ms pulses) onto the N2v cells reproduced the SO → N2v biphasic synaptic response but also induced long-term plateauing (20–60 s). N2d cells show no endogenous ability to plateau, but this can be induced by focal applications of ACh. The N2v cells inhibit the N3 tonic (N3t) but not the N3 phasic (N3p) CPG interneurons. The N2v → N3t inhibitory synaptic connection is important in timing N3t activity. The N3t cells recover from this inhibition and fire during the swallow phase of the feeding pattern. Feedback N2v inhibition to the SO, N1L protraction phase interneurons prevents them firing during the retraction phase of the feeding cycle. The N2v → N1M synaptic connection was weak and only found in 50% of preparations. A weak N2v → CGC inhibitory connection prevents the CGCs firing during the rasp (N2) phase of the feeding cycle. These data allowed a new model for the Lymnaea feeding CPG to be proposed. This emphasizes that each of the six types of CPG interneuron has a unique set of synaptic connections, all of which contribute to the generation of a full CPG pattern.

Plateau potentials in motor neurons in the ventilatory system of the crab

1997 ◽  
Vol 200 (12) ◽  
pp. 1725-1736
Author(s):  
R Dicaprio
Keyword(s):  
Central Pattern Generator ◽  
Motor Neurons ◽  
Large Amplitude ◽  
Action Potentials ◽  
Experimental Tests ◽  
Pattern Generator ◽  
Plateau Potentials ◽  
Plateau Potential

The motor neurons in the crab ventilatory system have previously been considered to be passive output elements in that the generation of bursts of action potentials in these neurons during ventilation was thought to be due to cyclic inhibition and excitation from the interneurons in the ventilatory central pattern generator. This study demonstrates that the large-amplitude depolarization that underlies bursts of action potentials in ventilatory motor neurons is produced by a plateau potential. These motor neurons satisfy a number of the experimental tests that have been proposed for plateau potentials, such as triggering of the burst by a brief depolarization, termination of the burst by a hyperpolarizing input, and an all-or-none suppression of the depolarizing potential by the injection of hyperpolarizing current.

scholarly journals Using a Model to Assess the Role of the Spatiotemporal Pattern of Inhibitory Input and Intrasegmental Electrical Coupling in the Intersegmental and Side-to-Side Coordination of Motor Neurons by the Leech Heartbeat Central Pattern Generator

2008 ◽  
Vol 100 (3) ◽  
pp. 1354-1371 ◽  
Author(s):  
Paul S. García ◽  
Terrence M. Wright ◽  
Ian R. Cunningham ◽  
Ronald L. Calabrese
Keyword(s):  
Motor Neuron ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Electrical Coupling ◽  
Pattern Generator ◽  
Living System ◽  
Phase Relations ◽  
Spatiotemporal Pattern ◽  
Intrinsic Properties ◽  
Synaptic Inputs

Previously we presented a quantitative description of the spatiotemporal pattern of inhibitory synaptic input from the heartbeat central pattern generator (CPG) to segmental motor neurons that drive heartbeat in the medicinal leech and the resultant coordination of CPG interneurons and motor neurons. To begin elucidating the mechanisms of coordination, we explore intersegmental and side-to-side coordination in an ensemble model of all heart motor neurons and their known synaptic inputs and electrical coupling. Model motor neuron intrinsic properties were kept simple, enabling us to determine the extent to which input and electrical coupling acting together can account for observed coordination in the living system in the absence of a substantive contribution from the motor neurons themselves. The living system produces an asymmetric motor pattern: motor neurons on one side fire nearly in synchrony (synchronous), whereas on the other they fire in a rear-to-front progression (peristaltic). The model reproduces the general trends of intersegmental and side-to-side phase relations among motor neurons, but the match with the living system is not quantitatively accurate. Thus realistic (experimentally determined) inputs do not produce similarly realistic output in our model, suggesting that motor neuron intrinsic properties may contribute to their coordination. By varying parameters that determine electrical coupling, conduction delays, intraburst synaptic plasticity, and motor neuron excitability, we show that the most important determinant of intersegmental and side-to-side phase relations in the model was the spatiotemporal pattern of synaptic inputs, although phasing was influenced significantly by electrical coupling.

Modeling the gastric mill central pattern generator of the lobster with a relaxation-oscillator network

1993 ◽  
Vol 70 (3) ◽  
pp. 1030-1053 ◽  
Author(s):  
P. F. Rowat ◽  
A. I. Selverston
Keyword(s):  
Central Pattern Generator ◽  
Model Neuron ◽  
Relaxation Oscillator ◽  
Reciprocal Inhibition ◽  
Pattern Generator ◽  
Pattern Generation ◽  
Gastric Mill ◽  
Plateau Potentials ◽  
Isolated Cells ◽  
Current Parameter

1. The gastric mill central pattern generator (CPG) controls the chewing movements of teeth in the gastric mill of the lobster. This CPG has been extensively studied, but the precise mechanism underlying pattern generation is not well understood. The goal of this research was to develop a simplified model that captures the principle, biologically significant features of this CPG. We introduce a simplified neuron model that embodies approximations of well-known membrane currents, and is able to reproduce several global characteristics of gastric mill neurons. A network built with these neurons, using graded synaptic transmission and having the synaptic connections of the biological circuit, is sufficient to explain much of the network's behavior. 2. The cell model is a generalization and extension of the Van der Pol relaxation oscillator equations. It is described by two differential equations, one for current conservation and one for slow current activation. The model has a fast current that may, by adjusting one parameter, have a region of negative resistance in its current-voltage (I-V) curve. It also has a slow current with a single gain parameter that can be regarded as the combination of slow inward and outward currents. 3. For suitable values of the fast current parameter and the slow current parameter, the isolated model neuron exhibits several different behaviors: plateau potentials, postinhibitory rebound, postburst hyperpolarization, and endogenous oscillations. When the slow current is separated into inward and outward fractions with separately adjustable gain parameters, the model neuron can fire tonically, be quiescent, or generate spontaneous voltage oscillations with varying amounts of depolarization or hyperpolarization. 4. The most common form of synaptic interaction in the gastric CPG is reciprocal inhibition. A pair of identical model cells, connected with reciprocal inhibition, oscillates in antiphase if either the isolated cells are endogenous oscillators, or they are quiescent without plateau potentials, or they have plateau potentials but the synaptic strengths are below a critical level. If the isolated cells have widely differing frequencies (or would have if the cells were made to oscillate by adjusting the fast currents), reciprocal inhibition entrains the cells to oscillate with the same frequency but with phases that are advanced or retarded relative to the phases seen when the cells have the same frequency. The frequency of the entrained pair of cells lies between the frequencies of the original cells. The relative phases can also be modified by using very unequal synaptic strengths.(ABSTRACT TRUNCATED AT 400 WORDS)

Identification and characterization of cerebral ganglion neurons that induce swimming and modulate swim-related pedal ganglion neurons in Aplysia brasiliana

1995 ◽  
Vol 74 (4) ◽  
pp. 1444-1462 ◽  
Author(s):  
G. N. Gamkrelidze ◽  
P. J. Laurienti ◽  
J. E. Blankenship
Keyword(s):  
Central Pattern Generator ◽  
Motor Neurons ◽  
Cerebral Ganglion ◽  
Motor Program ◽  
Pattern Generator ◽  
Pedal Ganglion ◽  
Cell Type ◽  
Command Neurons ◽  
Sensory Stimuli ◽  
Ganglion Neurons

1. We have identified and characterized a family of several pairs of neurons in the cerebral ganglion of Aplysia brasiliana that are capable of inducing, maintaining, or modulating a motor program that underlies swim locomotion in this marine mollusk. We have operationally defined these cells as command neurons (CNs) for swimming. 2. The command cells occur in bilateral pairs in the cerebral ganglion and make direct and indirect outputs to neurons in the pedal ganglia, including motor neurons, a central pattern generator circuit, and modulatory neurons that enhance muscle contractions during swimming. Several of the CNs are sufficient individually to induce the swim motor program (SMP), all receive sensory feedback from the periphery, and several interconnect with other swim-related CNs. 3. Tonic discharges of approximately 10 Hz in CN types 1-3 (CN1-CN3) are capable of eliciting the oscillatory, phasic SMP as recorded in peripheral nerves that innervate the swim appendages, the parapodia. CN1, CN2, and CN3 make monosynaptic excitatory connections onto ipsilateral, contralateral, and bilateral pedal swim-modulatory neurons [parapodial opener-phase (POP) cells], respectively; and each command cell type activates the pedal central pattern generator (CPG), leading to sustained phasic output of motor neurons and POP cells. 4. Tonic firing of CN4 causes weak activation of the SMP contralaterally. These neurons occur as two pairs of neurons in each cerebral hemiganglion, with mutual electrical and chemical synaptic interconnections. CN4 cells also excite CN1 and CN2 cells. Thus CN4 is classified as a higher-order swim command cell type. 5. Command cells classified as types 5-8 (CN5-CN8), although not capable of inducing the SMP individually, nonetheless have strong synaptic connections with pedal POP cells and/or with other command neurons. These command cells may excite or inhibit follower cells on the same or opposite sides of the preparation and modulate the swim output. 6. All the command cells tested received strong input from mechanical stimulation, either stretch or pinching, of either parapodium. Mechanosensory input from the parapodia was shown to depend on the presence of the pedal ganglion, but not the pleural. Sensory stimulation activated command cells and motor neurons, but POP cells received input from sensory stimuli only through the cerebral ganglion, probably via command cells. The effects of applied mechanosensory stimuli could be entirely mimicked by motor neuron-induced contractions of the parapodia.

Mechanisms of gastric rhythm generation in the isolated stomatogastric ganglion of spiny lobsters: bursting pacemaker potentials, synaptic interactions, and muscarinic modulation

1992 ◽  
Vol 68 (3) ◽  
pp. 890-907 ◽  
Author(s):  
R. C. Elson ◽  
A. I. Selverston
Keyword(s):  
Building Blocks ◽  
Pattern Generator ◽  
Stomatogastric Ganglion ◽  
Pattern Generation ◽  
Cooperative Interaction ◽  
Membrane Properties ◽  
Muscarinic Agonist ◽  
Rhythm Generation ◽  
Pacemaker Potentials ◽  
Muscarinic Modulation

1. The gastric central pattern generator (CPG), located in the stomatogastric ganglion (STG) of the spiny lobster (Panulirus interruptus), is nonrhythmic when deprived of neuromodulatory inputs from anterior ganglia. Leaving these inputs intact in vitro can sustain a gastric rhythm but also introduces numerous, uncontrolled and largely unknown modulatory and synaptic influences that greatly complicate analysis of this CPG. 2. Here we induced gastric rhythms in the isolated STG, by superfusing a specific modulator, the muscarinic agonist, pilocarpine. Muscarinic agents sustain vigorous gastric rhythms in the isolated STG. Our aim was to analyze the pattern-generating functions of the restricted gastric circuit, free of complicating influences from other ganglia, and under specific (muscarinic) modulation. 3. We used combinations of multiple cell hyperpolarizations, photodeletions, and synaptic blockade by picrotoxin to assess the pattern-generating role of individual gastric neurons and to study the activity of subcircuits. 4. Four identified gastric neurons [lateral gastric (LG), dorsal gastric (DG), 2 electrically coupled lateral posterior gastric (2LPGs)] acted as pattern-generating cells. They showed bursting pacemaker potentials (BPPs), i.e., plateau (or driver) potentials that underlay bursts of axonal spikes and slow, interburst depolarizing potentials that underlay repetitive burst activity. LG and DG, at least, became conditional bursters, able to burst repetitively because of intrinsic oscillations. The other gastric neurons behaved mainly as follower cells and derived their rhythmic bursting from synaptic coupling to the pattern-generator cells and from their own intrinsic (but nonoscillatory) properties. 5. The pattern-generating neurons form a novel “kernel” circuit that works by the cooperative interaction of cellular properties and synaptic connectivity. 6. This study constitutes the first complete and fully consistent analysis of pattern generation in the gastric network of the isolated STG. These mechanisms pertain to muscarinic rhythms in particular but also, we suggest, to gastric rhythm generation and CPG function in general. We suggest that 1) rhythmicity normally depends on the induction of bursty membrane properties in at least some component neurons; 2) different subcircuits can produce rhythmic patterns and may be activated by different modulators; and 3) the gastric network shares several important “building blocks” with CPGs that have been analyzed in other systems. 7. Muscarinic inputs are implicated as an important gastric regulator. We compare these responses with the reported modulatory actions of the anterior pyloric modulator (AMP), an identified, putatively cholinergic input interneuron that may act via muscarinic mechanisms.

scholarly journals Eupnea, tachypnea, and autoresuscitation in a closed-loop respiratory control model

2017 ◽  
Vol 118 (4) ◽  
pp. 2194-2215 ◽  
Author(s):  
Casey O. Diekman ◽  
Peter J. Thomas ◽  
Christopher G. Wilson
Keyword(s):  
Central Pattern Generator ◽  
Closed Loop ◽  
Minute Ventilation ◽  
Respiratory Control ◽  
Pattern Generator ◽  
Control Model ◽  
Open Loop ◽  
Blood Oxygen ◽  
Rhythm Generation ◽  
Metabolic Demand

How sensory information influences the dynamics of rhythm generation varies across systems, and general principles for understanding this aspect of motor control are lacking. Determining the origin of respiratory rhythm generation is challenging because the mechanisms in a central circuit considered in isolation may be different from those in the intact organism. We analyze a closed-loop respiratory control model incorporating a central pattern generator (CPG), the Butera-Rinzel-Smith (BRS) model, together with lung mechanics, oxygen handling, and chemosensory components. We show that 1) embedding the BRS model neuron in a control loop creates a bistable system; 2) although closed-loop and open-loop (isolated) CPG systems both support eupnea-like bursting activity, they do so via distinct mechanisms; 3) chemosensory feedback in the closed loop improves robustness to variable metabolic demand; 4) the BRS model conductances provide an autoresuscitation mechanism for recovery from transient interruption of chemosensory feedback; and 5) the in vitro brain stem CPG slice responds to hypoxia with transient bursting that is qualitatively similar to in silico autoresuscitation. Bistability of bursting and tonic spiking in the closed-loop system corresponds to coexistence of eupnea-like breathing, with normal minute ventilation and blood oxygen level and a tachypnea-like state, with pathologically reduced minute ventilation and critically low blood oxygen. Disruption of the normal breathing rhythm, through either imposition of hypoxia or interruption of chemosensory feedback, can push the system from the eupneic state into the tachypneic state. We use geometric singular perturbation theory to analyze the system dynamics at the boundary separating eupnea-like and tachypnea-like outcomes. NEW & NOTEWORTHY A common challenge facing rhythmic biological processes is the adaptive regulation of central pattern generator (CPG) activity in response to sensory feedback. We apply dynamical systems tools to understand several properties of a closed-loop respiratory control model, including the coexistence of normal and pathological breathing, robustness to changes in metabolic demand, spontaneous autoresuscitation in response to hypoxia, and the distinct mechanisms that underlie rhythmogenesis in the intact control circuit vs. the isolated, open-loop CPG.

Brain Stem Control of Swallowing: Neuronal Network and Cellular Mechanisms

2001 ◽  
Vol 81 (2) ◽  
pp. 929-969 ◽  
Author(s):  
André Jean
Keyword(s):  
Brain Stem ◽  
Central Pattern Generator ◽  
Pattern Generator ◽  
Pattern Generation ◽  
Ventrolateral Medulla ◽  
Cellular Mechanisms ◽  
Neuronal Circuitry ◽  
Microelectrode Recordings ◽  
The Brain ◽  
Dorsal Medulla

Swallowing movements are produced by a central pattern generator located in the medulla oblongata. It has been established on the basis of microelectrode recordings that the swallowing network includes two main groups of neurons. One group is located within the dorsal medulla and contains the generator neurons involved in triggering, shaping, and timing the sequential or rhythmic swallowing pattern. Interestingly, these generator neurons are situated within a primary sensory relay, that is, the nucleus tractus solitarii. The second group is located in the ventrolateral medulla and contains switching neurons, which distribute the swallowing drive to the various pools of motoneurons involved in swallowing. This review focuses on the brain stem mechanisms underlying the generation of sequential and rhythmic swallowing movements. It analyzes the neuronal circuitry, the cellular properties of neurons, and the neurotransmitters possibly involved, as well as the peripheral and central inputs which shape the output of the network appropriately so that the swallowing movements correspond to the bolus to be swallowed. The mechanisms possibly involved in pattern generation and the possible flexibility of the swallowing central pattern generator are discussed.

scholarly journals Biological data questions the support of the self inhibition required for pattern generation in the half center model

2019 ◽  
Author(s):  
Matthias Kohler ◽  
Philipp Stratmann ◽  
Florian Röhrbein ◽  
Alois Knoll ◽  
Alin Albu-Schäffer ◽  
...  
Keyword(s):  
Spinal Cord ◽  
Central Pattern Generator ◽  
Pattern Generator ◽  
Pattern Generation ◽  
Biological Data ◽  
The Self ◽  
Published Data ◽  
Functional Evaluation ◽  
Inhibitory Mechanism ◽  
Locomotion Control

AbstractLocomotion control in mammals has been hypothesized to be governed by a central pattern generator (CPG) located in the circuitry of the spinal cord. The most common model of the CPG is the half center model, where two pools of neurons generate alternating, oscillatory activity. In this model, the pools reciprocally inhibit each other ensuring alternating activity. There is experimental support for reciprocal inhibition. However another crucial part of the half center model is a self inhibitory mechanism which prevents the neurons of each individual pool from infinite firing. Self-inhibition is hence necessary to obtain alternating activity. But critical parts of the experimental bases for the proposed mechanisms for self-inhibition were obtained in vitro, in preparations of juvenile animals. The commonly used adaptation of spike firing does not appear to be present in adult animals in vivo. We therefore modeled several possible self inhibitory mechanisms for locomotor control. Based on currently published data, previously proposed hypotheses of the self inhibitory mechanism, necessary to support the CPG hypothesis, seems to be put into question by functional evaluation tests or by in vivo data. This opens for alternative explanations of how locomotion activity patterns in the adult mammal could be generated.Author summaryLocomotion control in animals is hypothesized to be controlled through an intrinsic central pattern generator in the spinal cord. This was proposed over a hundred years ago and has subsequently been formed into a consistent theory, through experimentation and computer modeling. However, critical data that support the neuronal circuitry mechanisms underpinning this theory has been obtained in experiments that greatly differ from intact animals. We propose, after trying to fill in this critical part, that new ideas are required to explain locomotion of intact animals.

Sign in / Sign up

Export Citation Format

Share Document