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.

Distributed amine modulation of graded chemical transmission in the pyloric network of the lobster stomatogastric ganglion

1995 ◽  
Vol 74 (1) ◽  
pp. 437-452 ◽  
Author(s):  
B. R. Johnson ◽  
J. H. Peck ◽  
R. M. Harris-Warrick
Keyword(s):  
Motor Pattern ◽  
Input Resistance ◽  
Synaptic Strength ◽  
Stomatogastric Ganglion ◽  
The Other ◽  
Chemical Synapse ◽  
Synaptic Organization ◽  
Resistance Change ◽  
Pyloric Network ◽  
Chemical Synapses

1. In the pyloric network of the lobster stomatogastric ganglion, graded synapses organize the network output. The amines dopamine (DA), serotonin, and octopamine each elicit a distinctive motor pattern from a quiescent pyloric network. We have examined the effects of these amines on the graded synaptic strengths between the six major types of neurons of this network to understand how amine modulation of synaptic strength contributes to the amine-induced motor patterns. Here we tested amine affects at 10 different graded chemical synapses of the pyloric network. We show that each amine has a statistically different spectrum of distributed effects across the network synapses. 2. Under our control conditions (isolated pairs of neurons, removal of modulatory input), most of the graded chemical synapses were weak and some synapses were nonfunctional. The output synapses of the ventricular dilator (VD) neuron were significantly stronger than the other synapses. 3. DA altered the synaptic strength of every graded chemical synapse. This amine strengthened the weak chemical output synapses of the anterior burster (AB), lateral pyloric (LP), and pyloric constrictor (PY) neurons and weakened (and in some cases abolished) the strong chemical output synapses of the VD neuron. The AB-->inferior cardiac neuron (IC) and PY-->IC graded chemical synapses were nonfunctional under our control conditions; DA activated these silent synapses. 4. Serotonin enhanced the AB's output chemical synapses but weakened all the other graded chemical synapses examined. Octopamine's effects were much weaker than those of the other two amines. It enhanced the AB-->LP synapse and the LP's output synapses and weakly strengthened the AB-->PY, VD-->LP, and VD-->PY synapses. 5. The amines alter the input resistance of many of the pyloric neurons, and this could contribute to the observed changes in synaptic strength by altering passive current flow between input and output sites in the cells. However, the input resistance changes were relatively small compared with the changes in synaptic strength and cannot alone account for the synaptic modulation. In some cases the sign of the input resistance change was inconsistent with the change in synaptic strength. Thus the amines appear to modify synaptic transmission directly in this system. 6. This study completes our description of amine effects on all the graded synapses of the pyloric network. We summarize our present and earlier work to show that modulators can reconfigure the entire synaptic organization of a neural network by acting at many distributed synaptic sites.(ABSTRACT TRUNCATED AT 400 WORDS)

Control of Central Pattern Generators by an Identified Neurone in Crustacea: Activation of the Gastric Mill Motor Pattern by a Neurone Known to Modulate the Pyloric Network

1988 ◽  
Vol 136 (1) ◽  
pp. 53-87
Author(s):  
PATSY S. DICKINSON ◽  
FRÉDÉRIC NAGY ◽  
MAURICE MOULINS
Keyword(s):  
Central Pattern Generator ◽  
Motor Pattern ◽  
Central Pattern Generators ◽  
Rhythmic Activity ◽  
Pattern Generator ◽  
Gastric Mill ◽  
Pyloric Network ◽  
Single Burst ◽  
Pattern Generators ◽  
Synaptic Drive

In the red lobster (Palinurus vulgaris), an identified neurone, the anterior pyloric modulator neurone (APM), which has previously been shown to modulate the output of the pyloric central pattern generator, was shown to modulate the output of the gastric mill central pattern generator. APM activity induced a rhythm when the network was silent and increased rhythmic activity when the network was already active. Rhythmic activity was induced whether APM fired in single bursts, tonically or in repetitive bursts. A single burst in APM induced a rhythm which considerably outlasted the burst, whereas repetitive bursts effectively entrained the gastric oscillator. These modulations involved two major mechanisms. (1) APM induced or enhanced plateau properties in some of the gastric mill neurones. (2) APM activated the extrinsic inputs to the network, thus increasing the excitatory synaptic drive to most of the neurones of the network. As a result, when APM was active, all the neurones of the pattern generator actively participated in the rhythmic activity. By its actions on two separate but behaviourally related neural networks, the APM neurone may be able to control an entire concert of related types of behaviour.

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.

Target-Specific Short-Term Dynamics Are Important for the Function of Synapses in an Oscillatory Neural Network

2005 ◽  
Vol 94 (4) ◽  
pp. 2590-2602 ◽  
Author(s):  
Akira Mamiya ◽  
Farzan Nadim
Keyword(s):  
Spiny Lobster ◽  
Synaptic Depression ◽  
The Other ◽  
Cycle Period ◽  
Main Function ◽  
Short Term ◽  
Presynaptic Neuron ◽  
Pyloric Network ◽  
Pyloric Dilator ◽  
Oscillatory Neural Network

Short-term dynamics such as facilitation and depression are present in most synapses and are often target-specific even for synapses from the same type of neuron. We examine the dynamics and possible functions of two synapses from the same presynaptic neuron in the rhythmically active pyloric network of the spiny lobster. Using simultaneous recordings, we show that the synapses from the lateral pyloric (LP) neuron to the pyloric dilator (PD; a member of the pyloric pacemaker ensemble) and the pyloric constrictor (PY) neurons both show short-term depression. However, the postsynaptic potentials produced by the LP-to-PD synapse are larger in amplitude, depress less, and recover faster than those produced by the LP-to-PY synapse. The main function of the LP-to-PD synapse is to slow down the pyloric rhythm. However, in some cases, it slows down the rhythm only when it is fast and has no effect or to speeds up when it is slow. In contrast, the LP-to-PY synapse functions to delay the activity of the PY neuron; this delay increases as the cycle period becomes longer. Using a computational model, we show that the short-term dynamics of synaptic depression observed for each of these synapses are tailored to their individual functions and that replacing the dynamics of either synapse with the other would disrupt these functions. Together, the experimental and modeling results suggest that the target-specific features of short-term synaptic depression are functionally important for synapses efferent from the same presynaptic neuron.

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.

Dopamine Modulates Two Potassium Currents and Inhibits the Intrinsic Firing Properties of an Identified Motor Neuron in a Central Pattern Generator Network

1999 ◽  
Vol 81 (1) ◽  
pp. 29-38 ◽  
Author(s):  
Peter Kloppenburg ◽  
Robert M. Levini ◽  
Ronald M. Harris-Warrick
Keyword(s):  
Action Potential ◽  
Motor Neuron ◽  
Central Pattern Generator ◽  
Action Potentials ◽  
Potassium Current ◽  
Potassium Currents ◽  
Pattern Generator ◽  
Pyloric Network ◽  
Firing Properties ◽  
Intrinsic Firing

Kloppenburg, Peter, Robert M. Levini, and Ronald M. Harris-Warrick. Dopamine modulates two potassium currents and inhibits the intrinsic firing properties of an identified motor neuron in a central pattern generator network. J. Neurophysiol. 81: 29–38, 1999. The two pyloric dilator (PD) neurons are components [along with the anterior burster (AB) neuron] of the pacemaker group of the pyloric network in the stomatogastric ganglion of the spiny lobster Panulirus interruptus. Dopamine (DA) modifies the motor pattern generated by the pyloric network, in part by exciting or inhibiting different neurons. DA inhibits the PD neuron by hyperpolarizing it and reducing its rate of firing action potentials, which leads to a phase delay of PD relative to the electrically coupled AB and a reduction in the pyloric cycle frequency. In synaptically isolated PD neurons, DA slows the rate of recovery to spike after hyperpolarization. The latency from a hyperpolarizing prestep to the first action potential is increased, and the action potential frequency as well as the total number of action potentials are decreased. When a brief (1 s) puff of DA is applied to a synaptically isolated, voltage-clamped PD neuron, a small voltage-dependent outward current is evoked, accompanied by an increase in membrane conductance. These responses are occluded by the combined presence of the potassium channel blockers 4-aminopyridine and tetraethylammonium. In voltage-clamped PD neurons, DA enhances the maximal conductance of a voltage-sensitive transient potassium current ( I A) and shifts its V act to more negative potentials without affecting its V inact. This enlarges the “window current” between the voltage activation and inactivation curves, increasing the tonically active I A near the resting potential and causing the cell to hyperpolarize. Thus DA's effect is to enhance both the transient and resting K+ currents by modulating the same channels. In addition, DA enhances the amplitude of a calcium-dependent potassium current ( I O(Ca)), but has no effect on a sustained potassium current ( I K( V)). These results suggest that DA hyperpolarizes and phase delays the activity of the PD neurons at least in part by modulating their intrinsic postinhibitory recovery properties. This modulation appears to be mediated in part by an increase of I A and I O(Ca). I A appears to be a common target of DA action in the pyloric network, but it can be enhanced or decreased in different ways by DA in different neurons.

Fast Synaptic Connections From CBIs to Pattern-Generating Neurons in Aplysia: Initiation and Modification of Motor Programs

2003 ◽  
Vol 89 (4) ◽  
pp. 2120-2136 ◽  
Author(s):  
Itay Hurwitz ◽  
Irving Kupfermann ◽  
Klaudiusz R. Weiss
Keyword(s):  
Central Pattern Generator ◽  
Motor Pattern ◽  
Aplysia Californica ◽  
Pattern Generator ◽  
Synaptic Connections ◽  
Motor Patterns ◽  
Motor Programs ◽  
Postsynaptic Potentials ◽  
Buccal Ganglia ◽  
Very High

Consummatory feeding movements in Aplysia californica are organized by a central pattern generator (CPG) in the buccal ganglia. Buccal motor programs similar to those organized by the CPG are also initiated and controlled by the cerebro-buccal interneurons (CBIs), interneurons projecting from the cerebral to the buccal ganglia. To examine the mechanisms by which CBIs affect buccal motor programs, we have explored systematically the synaptic connections from three of the CBIs (CBI-1, CBI-2, CBI-3) to key buccal ganglia CPG neurons (B31/B32, B34, and B63). The CBIs were found to produce monosynaptic excitatory postsynaptic potentials (EPSPs) with both fast and slow components. In this report, we have characterized only the fast component. CBI-2 monosynaptically excites neurons B31/B32, B34, and B63, all of which can initiate motor programs when they are sufficiently stimulated. However, the ability of CBI-2 to initiate a program stems primarily from the excitation of B63. In B31/B32, the size of the EPSPs was relatively small and the threshold for excitation was very high. In addition, preventing firing in either B34 or B63 showed that only a block in B63 firing prevented CBI-2 from initiating programs in response to a brief stimulus. The connections from CBI-2 to the buccal ganglia neurons showed a prominent facilitation. The facilitation contributed to the ability of CBI-2 to initiate a BMP and also led to a change in the form of the BMP. The cholinergic blocker hexamethonium blocked the fast EPSPs induced by CBI-2 in buccal ganglia neurons and also blocked the EPSPs between a number of key CPG neurons within the buccal ganglia. CBI-2 and B63 were able to initiate motor patterns in hexamethonium, although the form of a motor pattern was changed, indicating that non-hexamethonium-sensitive receptors contribute to the ability of these cells to initiate bursts. By contrast to CBI-2, CBI-1 excited B63 but inhibited B34. CBI-3 excited B34 and not B63. The data indicate that CBI-1, -2, and -3 are components of a system that initiates and selects between buccal motor programs. Their behavioral function is likely to depend on which combination of CBIs and CPG elements are activated.

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.

Evolution of air-breathing and central CO(2)/H(+) respiratory chemosensitivity: new insights from an old fish?

2000 ◽  
Vol 203 (22) ◽  
pp. 3505-3512 ◽  
Author(s):  
R.J. Wilson ◽  
M.B. Harris ◽  
J.E. Remmers ◽  
S.F. Perry
Keyword(s):  
Central Pattern Generator ◽  
Motor Pattern ◽  
Lung Ventilation ◽  
Pattern Generator ◽  
Motor Patterns ◽  
Air Breathing ◽  
Longnose Gar ◽  
Isolated Brainstem

While little is known of the origin of air-breathing in vertebrates, primitive air breathers can be found among extant lobe-finned (Sarcopterygii) and ray-finned (Actinopterygii) fish. The descendents of Sarcopterygii, the tetrapods, generate lung ventilation using a central pattern generator, the activity of which is modulated by central and peripheral CO(2)/H(+) chemoreception. Air-breathing in Actinopterygii, in contrast, has been considered a ‘reflexive’ behaviour with little evidence for central CO(2)/H(+) respiratory chemoreceptors. Here, we describe experiments using an in vitro brainstem preparation of a primitive air-breathing actinopterygian, the longnose gar Lepisosteus osseus. Our data suggest (i) that gill and air-breathing motor patterns can be produced autonomously by the isolated brainstem, and (ii) that the frequency of the air-breathing motor pattern is increased by hypercarbia. These results are the first evidence consistent with the presence of an air-breathing central pattern generator with central CO(2)/H(+) respiratory chemosensitivity in any primitive actinopterygian fish. We speculate that the origin of the central neuronal controller for air-breathing preceded the divergence of the sarcopterygian and actinopterygian lineages and dates back to a common air-breathing ancestor.

scholarly journals The central pattern generator underlying swimming in Dendronotus iris: a simple half-center network oscillator with a twist

2016 ◽  
Vol 116 (4) ◽  
pp. 1728-1742 ◽  
Author(s):  
Akira Sakurai ◽  
Paul S. Katz
Keyword(s):  
Central Pattern Generator ◽  
Body Wall ◽  
Impulse Activity ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Excitatory Synapse ◽  
Dynamic Clamp ◽  
Motor Patterns ◽  
The Brain ◽  
Excitatory Drive

The nudibranch mollusc, Dendronotus iris, swims by rhythmically flexing its body from left to right. We identified a bilaterally represented interneuron, Si3, that provides strong excitatory drive to the previously identified Si2, forming a half-center oscillator, which functions as the central pattern generator (CPG) underlying swimming. As with Si2, Si3 inhibited its contralateral counterpart and exhibited rhythmic bursts in left-right alternation during the swim motor pattern. Si3 burst almost synchronously with the contralateral Si2 and was coactive with the efferent impulse activity in the contralateral body wall nerve. Perturbation of bursting in either Si3 or Si2 by current injection halted or phase-shifted the swim motor pattern, suggesting that they are both critical CPG members. Neither Si2 nor Si3 exhibited endogenous bursting properties when activated alone; activation of all four neurons was necessary to initiate and maintain the swim motor pattern. Si3 made a strong excitatory synapse onto the contralateral Si2 to which it is also electrically coupled. When Si3 was firing tonically but not exhibiting bursting, artificial enhancement of the Si3-to-Si2 synapse using dynamic clamp caused all four neurons to burst. In contrast, negation of the Si3-to-Si2 synapse by dynamic clamp blocked ongoing swim motor patterns. Together, these results suggest that the Dendronotus swim CPG is organized as a “twisted” half-center oscillator in which each “half” is composed of two excitatory-coupled neurons from both sides of the brain, each of which inhibits its contralateral counterpart. Consisting of only four neurons, this is perhaps the simplest known network oscillator for locomotion.

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