Neurotransmitter Interactions in the Stomatogastric System of the Spiny Lobster: One Peptide Alters the Response of a Central Pattern Generator to a Second Peptide

1997 ◽  
Vol 77 (2) ◽  
pp. 599-610 ◽  
Author(s):  
Patsy S. Dickinson ◽  
Wesley P. Fairfield ◽  
John R. Hetling ◽  
Jane Hauptman
Keyword(s):  
Central Pattern Generator ◽  
Motor Neurons ◽  
Spiny Lobster ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Stomatogastric Nervous System ◽  
Panulirus Interruptus ◽  
State Dependent ◽  
Bursting Activity ◽  
Stomatogastric System

Dickinson, Patsy S., Wesley P. Fairfield, John R. Hetling, and Jane Hauptman. Neurotransmitter interactions in the stomatogastric system of the spiny lobster: one peptide alters the response of a central pattern generator to a second peptide. J. Neurophysiol. 77: 599–610, 1997. Two of the peptides found in the stomatogastric nervous system of the spiny lobster, Panulirus interruptus, interacted to modulate the activity of the cardiac sac motor pattern. In the isolated stomatogastric ganglion, red-pigment-concentrating hormone (RPCH), but not proctolin, activated the bursting activity in the inferior ventricular (IV) neurons that drives the cardiac sac pattern. The cardiac sac pattern normally ceased within 15 min after the end of RPCH superfusion. However, when proctolin was applied within a few minutes of that time, it was likewise able to induce cardiac sac activity. Similarly, proctolin applied together with subthreshold RPCH induced cardiac sac bursting. The amplitude of the excitatory postsynaptic potentials from the IV neurons to the cardiac sac dilator neuron CD2 (1 of the 2 major motor neurons in the cardiac sac system) was potentiated in the presence of both proctolin and RPCH. The potentiation in RPCH was much greater than in proctolin alone. However, the potentiation inproctolin after RPCH was equivalent to that recorded in RPCH alone. Although we do not yet understand the mechanisms for these interactions of the two modulators, this study provides an example of one factor that can determine the “state” of the system that is critical in determining the effect of a modulator that is “state dependent,” and it provides evidence for yet another level of flexibility in the motor output of this system.

scholarly journals Output variability across animals and levels in a motor system

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Angela Wenning ◽  
Brian J Norris ◽  
Cengiz Günay ◽  
Daniel Kueh ◽  
Ronald L Calabrese
Keyword(s):  
Life History ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Motor System ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Phase Relations ◽  
The Other ◽  
Output Variability ◽  
Rhythmic Behaviors

Rhythmic behaviors vary across individuals. We investigated the sources of this output variability across a motor system, from the central pattern generator (CPG) to the motor plant. In the bilaterally symmetric leech heartbeat system, the CPG orchestrates two coordinations in the bilateral hearts with different intersegmental phase relations (Δϕ) and periodic side-to-side switches. Population variability is large. We show that the system is precise within a coordination, that differences in repetitions of a coordination contribute little to population output variability, but that differences between bilaterally homologous cells may contribute to some of this variability. Nevertheless, much output variability is likely associated with genetic and life history differences among individuals. Variability of Δϕ were coordination-specific: similar at all levels in one, but significantly lower for the motor pattern than the CPG pattern in the other. Mechanisms that transform CPG output to motor neurons may limit output variability in the motor pattern.

scholarly journals Feedback From Peripheral Musculature to Central Pattern Generator in the Neurogenic Heart of the Crab Callinectes sapidus: Role of Mechanosensitive Dendrites

2010 ◽  
Vol 103 (1) ◽  
pp. 83-96 ◽  
Author(s):  
Keyla García-Crescioni ◽  
Timothy J. Fort ◽  
Estee Stern ◽  
Vladimir Brezina ◽  
Mark W. Miller
Keyword(s):  
Motor Neuron ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Callinectes Sapidus ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Neuron Spike ◽  
Effector System ◽  
Spike Bursts

The neurogenic heart of decapod crustaceans is a very simple, self-contained, model central pattern generator (CPG)-effector system. The CPG, the nine-neuron cardiac ganglion (CG), is embedded in the myocardium itself; it generates bursts of spikes that are transmitted by the CG's five motor neurons to the periphery of the system, the myocardium, to produce its contractions. Considerable evidence suggests that a CPG-peripheral loop is completed by a return feedback pathway through which the contractions modify, in turn, the CG motor pattern. One likely pathway is provided by dendrites, presumably mechanosensitive, that the CG neurons project into the adjacent myocardial muscle. Here we have tested the role of this pathway in the heart of the blue crab, Callinectes sapidus . We performed “de-efferentation” experiments in which we cut the motor neuron axons to the myocardium and “de-afferentation” experiments in which we cut or ligated the dendrites. In the isolated CG, these manipulations had no effect on the CG motor pattern. When the CG remained embedded in the myocardium, however, these manipulations, interrupting either the efferent or afferent limb of the CPG-peripheral loop, decreased contraction amplitude, increased the frequency of the CG motor neuron spike bursts, and decreased the number of spikes per burst and burst duration. Finally, passive stretches of the myocardium likewise modulated the spike bursts, an effect that disappeared when the dendrites were cut. We conclude that feedback through the dendrites indeed operates in this system and suggest that it completes a loop through which the system self-regulates its activity.

scholarly journals Neuromodulator-evoked synaptic metaplasticity within a central pattern generator network

2012 ◽  
Vol 108 (10) ◽  
pp. 2846-2856 ◽  
Author(s):  
Mark D. Kvarta ◽  
Ronald M. Harris-Warrick ◽  
Bruce R. Johnson
Keyword(s):  
Central Pattern Generator ◽  
Spiny Lobster ◽  
Motor Pattern ◽  
Synaptic Depression ◽  
Pattern Generator ◽  
Chemical Synapse ◽  
Pyloric Network ◽  
Pyloric Dilator ◽  
Synaptic Dynamics ◽  
Chemical Synapses

Synapses show short-term activity-dependent dynamics that alter the strength of neuronal interactions. This synaptic plasticity can be tuned by neuromodulation as a form of metaplasticity. We examined neuromodulator-induced metaplasticity at a graded chemical synapse in a model central pattern generator (CPG), the pyloric network of the spiny lobster stomatogastric ganglion. Dopamine, serotonin, and octopamine each produce a unique motor pattern from the pyloric network, partially through their modulation of synaptic strength in the network. We characterized synaptic depression and its amine modulation at the graded synapse from the pyloric dilator neuron to the lateral pyloric neuron (PD→LP synapse), driving the PD neuron with both long square pulses and trains of realistic waveforms over a range of presynaptic voltages. We found that the three amines can differentially affect the amplitude of graded synaptic transmission independently of the synaptic dynamics. Low concentrations of dopamine had weak and variable effects on the strength of the graded inhibitory postsynaptic potentials (gIPSPs) but reliably accelerated the onset of synaptic depression and recovery from depression independently of gIPSP amplitude. Octopamine enhanced gIPSP amplitude but decreased the amount of synaptic depression; it slowed the onset of depression and accelerated its recovery during square pulse stimulation. Serotonin reduced gIPSP amplitude but increased the amount of synaptic depression and accelerated the onset of depression. These results suggest that amine-induced metaplasticity at graded chemical synapses can alter the parameters of synaptic dynamics in multiple and independent ways.

A Central Pattern Generator Producing Alternative Outputs: Temporal Pattern of Premotor Activity

2006 ◽  
Vol 96 (1) ◽  
pp. 309-326 ◽  
Author(s):  
Brian J. Norris ◽  
Adam L. Weaver ◽  
Lee G. Morris ◽  
Angela Wenning ◽  
Paul A. García ◽  
...  
Keyword(s):  
Central Pattern Generator ◽  
Motor Neurons ◽  
Coordination Mode ◽  
Motor Pattern ◽  
Quantitative Description ◽  
Extracellular Recording ◽  
Pattern Generator ◽  
Regular Feature ◽  
Phase Constancy ◽  
Activity State

The central pattern generator for heartbeat in medicinal leeches constitutes seven identified pairs of segmental heart interneurons. Four identified pairs of heart interneurons make a staggered pattern of inhibitory synaptic connections with segmental heart motor neurons. Using extracellular recording from multiple interneurons in the network in 56 isolated nerve cords, we show that this pattern generator produces a side-to-side asymmetric pattern of intersegmental coordination among ipsilateral premotor interneurons. This pattern corresponds to a similarly asymmetric fictive motor pattern in heart motor neurons and asymmetric constriction pattern of the two tubular hearts, synchronous and peristaltic. We provide a quantitative description of the firing pattern of all the premotor interneurons, including phase, duty cycle, and intraburst frequency of this premotor activity pattern. This analysis identifies two stereotypical coordination modes corresponding to synchronous and peristaltic, which show phase constancy over a broad range of periods as do the fictive motor pattern and the heart constriction pattern. Coordination mode is controlled through one segmental pair of heart interneurons (switch interneurons). Side-to-side switches in coordination mode are a regular feature of this pattern generator and occur with changes in activity state of these switch interneurons. Associated with synchronous coordination of premotor interneurons, the ipsilateral switch interneuron is in an active state, during which it produces rhythmic bursts, whereas associated with peristaltic coordination, the ipsilateral switch interneuron is largely silent. We argue that timing and pattern elaboration are separate functions produced by overlapping subnetworks in the heartbeat central pattern generator.

Plasticity in the multifunctional buccal central pattern generator of Helisoma illuminated by the identification of phase 3 interneurons

1996 ◽  
Vol 75 (2) ◽  
pp. 561-574 ◽  
Author(s):  
E. M. Quinlan ◽  
A. D. Murphy
Keyword(s):  
Motor Activity ◽  
Motor Neuron ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Neuron Activity ◽  
Phase 2 ◽  
Phase 3 ◽  
Standard Pattern

1. The mechanism for generating diverse patterns of buccal motor neuron activity was explored in the multifunctional central pattern generator (CPG) of Helisoma. The standard pattern of motor neuron activity, which results in typical feeding behavior, consists of three distinct phases of buccal motor neuron activity. We have previously identified CPG interneurons that control the motor neuron activity during phases 1 and 2 of the standard pattern. Here we identify a pair of interneurons responsible for buccal motor neuron activity during phase 3, and examine the variability in the interactions between this third subunit and other subunits of the CPG. 2. During the production of the standard pattern, phase 3 excitation in many buccal motor neurons follows a prominent phase 2 inhibitory postsynaptic potential. Therefore phase 3 excitation was previously attributed to postinhibitory rebound (PIR) in these motor neurons. Two classes of observations indicated that PIR was insufficient to account for phase 3 activity, necessitating phase 3 interneurons. 1) A subset of identified buccal neurons is inhibited during phase 3 by discrete synaptic input. 2) Other identified buccal neurons display discrete excitation during both phases 2 and 3. 3. A bilaterally symmetrical pair of CPG interneurons, named N3a, was identified and characterized as the source of phase 3 postsynaptic potentials in motor neurons. During phase 3 of the standard motor pattern, interneuron N3a generated bursts of action potentials. Stimulation of N3a, in quiescent preparations, evoked a depolarization in motor neurons that are excited during phase 3 and a hyperpolarization in motor neurons that are inhibited during phase 3. Hyperpolarization of N3a during patterned motor activity eliminated both phase 3 excitation and inhibition. Physiological and morphological characterization of interneuron N3a is provided to invite comparisons with possible homologues in other gastropod feeding CPGs. 4. These data support a model proposed for the organization of the tripartite buccal CPG. According to the model, each of the three phases of buccal motor neuron activity is controlled by discrete subsets of pattern-generating interneurons called subunit 1 (S1), subunit 2 (S2), and subunit 3 (S3). The standard pattern of buccal motor neuron activity underlying feeding is mediated by an S1-S2-S3 sequence of CPG subunit activity. However, a number of "nonstandard" patterns of buccal motor activity were observed. In particular, S2 and S3 activity can occur independently or be linked sequentially in rhythmic patterns other than the standard feeding pattern. Simultaneous recordings of S3 interneuron N3a with effector neurons indicated that N3a can account for phase-3-like postsynaptic potentials (PSPs) in nonstandard patterns. The variety of patterns of buccal motor neuron activity indicates that each CPG subunit can be active in the absence of, or in concert with, activity in any other subunit. 5. To explore how CPG activity may be regulated to generate a particular motor pattern from the CPG's full repertoire, we applied the neuromodulator serotonin. Serotonin initiated and sustained the production of an S2-S3 pattern of activity, in part by enhancing PIR in S3 interneuron N3a after the termination of phase 2 inhibition.

A Central Pattern Generator Producing Alternative Outputs: Pattern, Strength, and Dynamics of Premotor Synaptic Input to Leech Heart Motor Neurons

2007 ◽  
Vol 98 (5) ◽  
pp. 2992-3005 ◽  
Author(s):  
Brian J. Norris ◽  
Adam L. Weaver ◽  
Angela Wenning ◽  
Paul S. García ◽  
Ronald L. Calabrese
Keyword(s):  
Central Pattern Generator ◽  
Motor Neurons ◽  
Temporal Pattern ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Synaptic Connectivity ◽  
Neuron Activity ◽  
Coordination Modes ◽  
Asymmetric Pattern ◽  
Medicinal Leeches

The central pattern generator (CPG) for heartbeat in medicinal leeches consists of seven identified pairs of segmental heart interneurons and one unidentified pair. Four of the identified pairs and the unidentified pair of interneurons make inhibitory synaptic connections with segmental heart motor neurons. The CPG produces a side-to-side asymmetric pattern of intersegmental coordination among ipsilateral premotor interneurons corresponding to a similarly asymmetric fictive motor pattern in heart motor neurons, and asymmetric constriction pattern of the two tubular hearts, synchronous and peristaltic. Using extracellular recordings from premotor interneurons and voltage-clamp recordings of ipsilateral segmental motor neurons in 69 isolated nerve cords, we assessed the strength and dynamics of premotor inhibitory synaptic output onto the entire ensemble of heart motor neurons and the associated conduction delays in both coordination modes. We conclude that premotor interneurons establish a stereotypical pattern of intersegmental synaptic connectivity, strengths, and dynamics that is invariant across coordination modes, despite wide variations among preparations. These data coupled with a previous description of the temporal pattern of premotor interneuron activity and relative phasing of motor neuron activity in the two coordination modes enable a direct assessment of how premotor interneurons through their temporal pattern of activity and their spatial pattern of synaptic connectivity, strengths, and dynamics coordinate segmental motor neurons into a functional pattern of activity.

A Central Pattern Generator Producing Alternative Outputs: Phase Relations of Leech Heart Motor Neurons With Respect to Premotor Synaptic Input

2007 ◽  
Vol 98 (5) ◽  
pp. 2983-2991 ◽  
Author(s):  
Brian J. Norris ◽  
Adam L. Weaver ◽  
Angela Wenning ◽  
Paul S. García ◽  
Ronald L. Calabrese
Keyword(s):  
Motor Neuron ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Coordination Mode ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Neuron Activity ◽  
Intersegmental Coordination ◽  
Asymmetric Pattern ◽  
Neuron Ensemble

The central pattern generator (CPG) for heartbeat in leeches consists of seven identified pairs of segmental heart interneurons and one unidentified pair. Four of the identified pairs and the unidentified pair of interneurons make inhibitory synaptic connections with segmental heart motor neurons. The CPG produces a side-to-side asymmetric pattern of intersegmental coordination among ipsilateral premotor interneurons corresponding to a similarly asymmetric fictive motor pattern in heart motor neurons, and asymmetric constriction pattern of the two tubular hearts: synchronous and peristaltic. Using extracellular techniques, we recorded, in 61 isolated nerve cords, the activity of motor neurons in conjunction with the phase reference premotor heart interneuron, HN(4), and another premotor interneuron that allowed us to assess the coordination mode. These data were then coupled with a previous description of the temporal pattern of premotor interneuron activity in the two coordination modes to synthesize a global phase diagram for the known elements of the CPG and the entire motor neuron ensemble. These average data reveal the stereotypical side-to-side asymmetric patterns of intersegmental coordination among the motor neurons and show how this pattern meshes with the activity pattern of premotor interneurons. Analysis of animal-to-animal variability in this coordination indicates that the intersegmental phase progression of motor neuron activity in the midbody in the peristaltic coordination mode is the most stereotypical feature of the fictive motor pattern. Bilateral recordings from motor neurons corroborate the main features of the asymmetric motor pattern.

Synaptic regulation of cellular properties and burst oscillations of neurons in gastric mill system of spiny lobsters, Panulirus interruptus

1984 ◽  
Vol 52 (1) ◽  
pp. 54-73 ◽  
Author(s):  
D. F. Russell ◽  
D. K. Hartline
Keyword(s):  
Motor Neurons ◽  
Pattern Generator ◽  
Stomatogastric Ganglion ◽  
Gastric Mill ◽  
Panulirus Interruptus ◽  
Synaptic Regulation ◽  
Gastric Cells ◽  
Current Pulses ◽  
Regenerative Property ◽  
Stimulation Of

The properties of neurons in the stomatogastric ganglion (STG) participating in the pattern generator for the gastric mill rhythm were studied by intracellular current injection under several conditions: during ongoing gastric rhythms, in the nonrhythmic isolated STG, after stimulation of the nerve carrying central nervous system (CNS) inputs to the STG, or under Ba2+ or Sr2+. Slow regenerative depolarizations during ongoing rhythms were demonstrated in the anterior median, cardiopyloric, lateral cardiac, gastropyloric, and continuous inhibitor (AM, CP, LC, GP, and CI) neurons according to criteria such as voltage dependency, burst triggering, and termination by brief current pulses, etc. Experiments showed that regenerative-like behavior was not due to synaptic network interactions. The slow regenerative responses were abolished by isolating the stomatogastric ganglion but could be reestablished by stimulating the input nerve. This indicates that certain CNS inputs synaptically induce the regenerative property in specific gastric neurons. Slow regenerative depolarizations were not demonstrable in gastric mill (GM) motor neurons. Their burst oscillations and firing rate were instead proportional to injected current. CNS inputs evoked a prolonged depolarization in GM motor neurons, apparently by a nonregenerative mechanism. All the gastric cells showed prolonged regenerative potentials under 0.5-1.5 mM Ba2+. We conclude that the gastric neurons of the STG can be divided into three types according to their properties: those with a regenerative capability, a repetitively firing type, and a nonregenerative "proportional" type. The cells are strongly influenced by several types of CNS inputs, including "gastric command fibers."

Peptidergic modulation of a multioscillator system in the lobster. I. Activation of the cardiac sac motor pattern by the neuropeptides proctolin and red pigment-concentrating hormone

1989 ◽  
Vol 61 (4) ◽  
pp. 833-844 ◽  
Author(s):  
P. S. Dickinson ◽  
E. Marder
Keyword(s):  
Nervous System ◽  
Motor Neurons ◽  
Motor Pattern ◽  
Stomatogastric Ganglion ◽  
Red Pigment ◽  
Stomatogastric Nervous System ◽  
Two Phase ◽  
Motor Patterns ◽  
Neuronal Element

1. The cardiac sac motor pattern consists of slow and irregular impulse bursts in the motor neurons [cardiac sac dilator 1 and 2 (CD1 and CD2)] that innervate the dilator muscles of the cardiac sac region of the crustacean foregut. 2. The effects of the peptides, proctolin and red pigment-concentrating hormone (RPCH), on the cardiac sac motor patterns produced by in vitro preparations of the combined stomatogastric nervous system [the stomatogastric ganglion (STG), the paired commissural ganglia (CGs), and the oesophageal ganglion (OG)] were studied. 3. Bath applications of either RPCH or proctolin activated the cardiac sac motor pattern when this motor pattern was not already active and increased the frequency of the cardiac sac motor pattern in slowly active preparations. 4. The somata of CD1 and CD2 are located in the esophageal and stomatogastric ganglia, respectively. Both neurons project to all four of the ganglia of the stomatogastric nervous system. RPCH elicited cardiac sac motor patterns when applied to any region of the stomatogastric nervous system, suggesting a distributed pattern generating network with multiple sites of modulation. 5. The anterior median (AM) neuron innervates the constrictor muscles of the cardiac sac. The AM usually functions as a part of the gastric mill pattern generator. However, when the cardiac sac is activated by RPCH applied to the stomatogastric ganglion, the AM neuron becomes active in antiphase with the cardiac sac dilator bursts. This converts the cardiac sac motor pattern from a one-phase rhythm to a two-phase rhythm. 6. These data show that a neuropeptide can cause a neuronal element to switch from being solely a component of one neuronal circuit to functioning in a second one as well. This example shows that peptidergic "reconfiguration" of neuronal networks can produce substantial changes in the behavior of associated neurons.

Gating of Afferent Input by a Central Pattern Generator

1999 ◽  
Vol 81 (2) ◽  
pp. 950-953 ◽  
Author(s):  
Ralph A. DiCaprio
Keyword(s):  
Central Pattern Generator ◽  
Sensory Input ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Afferent Input ◽  
Inhibitory Input ◽  
Cycle Period ◽  
Intracellular Recordings ◽  
Afferent Fibers ◽  
Sufficient Magnitude

Gating of afferent input by a central pattern generator. Intracellular recordings from the sole proprioceptor (the oval organ) in the crab ventilatory system show that the nonspiking afferent fibers from this organ receive a cyclic hyperpolarizing inhibition in phase with the ventilatory motor pattern. Although depolarizing and hyperpolarizing current pulses injected into a single afferent will reset the ventilatory motor pattern, the inhibitory input is of sufficient magnitude to block afferent input to the ventilatory central pattern generator (CPG) for ∼50% of the cycle period. It is proposed that this inhibitory input serves to gate sensory input to the ventilatory CPG to provide an unambiguous input to the ventilatory CPG.

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