scholarly journals Suppressive control of the crustacean pyloric network by a pair of identified interneurons. I. Modulation of the motor pattern

1990 ◽  
Vol 10 (2) ◽  
pp. 448-457 ◽  
Author(s):  
JR Cazalets ◽  
F Nagy ◽  
M Moulins
1982 ◽  
Vol 48 (4) ◽  
pp. 914-937 ◽  
Author(s):  
D. F. Russell ◽  
D. K. Hartline

1. Neurons in the central pattern generator for the "pyloric" motor rhythm of the lobster stomatogastric ganglion were investigated for the possible involvement of regenerative membrane properties in their membrane-potential oscillations and bursting output patterns. 2. Evidence was found that each class of pyloric-system neurons can possess a capability for generating prolonged regenerative depolarizations by a voltage-dependent membrane mechanism. Such responses have been termed plateau potentials. 3. Several tests were applied to determine whether a given cell possessed a plateau capability. First among these was the ability to trigger all-or-none bursts of nerve impulses by brief depolarizing current pulses and to terminate bursts in an all-or-none fashion with brief hyperpolarizing current pulses. Tests were made under conditions of a high level of activity in the pyloric generator, often in conjunction with the use of hyperpolarizing offsets to the cell under test to suppress ongoing bursting. 4. For each class, the network of synaptic interconnections among the pyloric-system neurons was shown to not be the cause of the regenerative responses observed. 5. Plateau potentials are viewed as a driving force for axon spiking during bursts and as interacting with the synaptic network in the formation of the pyloric motor pattern.


1998 ◽  
Vol 79 (3) ◽  
pp. 1396-1408 ◽  
Author(s):  
Stefan Clemens ◽  
Denis Combes ◽  
Pierre Meyrand ◽  
John Simmers

Clemens, Stefan, Denis Combes, Pierre Meyrand, and John Simmers. Long-term expression of two interacting motor pattern-generating networks in the stomatogastric system of freely behaving lobster. J. Neurophysiol. 79: 1396–1408, 1998. Rhythmic movements of the gastric mill and pyloric regions of the crustacean foregut are controlled by two stomatogastric neuronal networks that have been intensively studied in vitro. By using electromyographic recordings from the European lobster, Homarus gammarus, we have monitored simultaneously the motor activity of pyloric and gastric mill muscles for ≤3 mo in intact and freely behaving animals. Both pyloric and gastric mill networks are almost continuously active in vivo regardless of the presence of food. In unfed resting animals kept under “natural-like” conditions, the pyloric network expresses the typical triphasic pattern seen in vitro but at considerably slower cycle periods (2.5–3.5 s instead of 1–1.5 s). Gastric mill activity occurs at mean cycle periods of 20–50 s compared with 5–10 s in vitro but may suddenly stop for up to tens of minutes, then restart without any apparent behavioral reason. When conjointly active, the two networks express a strict coupling that involves certain but not all motor neurons of the pyloric network. The posterior pyloric constrictor muscles, innervated by a total of 8 pyloric (PY) motor neurons, are influenced by the onset of each gastric mill medial gastric/lateral gastric(MG/LG) neuron powerstroke burst, and for one cycle, PY neuron bursts may attain >300% of their mean duration. However, the duration of activity in the lateral pyloric constrictor muscle, innervated by the unique lateral pyloric (LP) motor neuron, remains unaffected by this perturbation. During this period after gastric perturbation, LP neuron and PY neurons thus express opposite burst-to-period relationships in that LP neuron burst duration is independent of the ongoing cycle period, whereas PY neuron burst duration changes with period length. In vitro the same type of gastro-pyloric interaction is observed, indicating that it is not dependent on sensory inputs. Moreover, this interaction is intrinsic to the stomatogastric ganglion itself because the relationship between the two networks persists after suppression of descending inputs to the ganglion. Intracellular recordings reveal that thisgastro-pyloric interaction originates from the gastric MG and LG neurons of the gastric network, which inhibit the pyloric pacemaker ensemble. As a consequence, the pyloric PY neurons, which are inhibited by the pyloric dilator (PD) neurons of the pyloric pacemaker group, extend their activity during the time that PD neuron is held silent. Moreover, there is evidence for a pyloro-gastric interaction, apparently rectifying, from the pyloric pacemakers back to the gastric MG/LG neuron group.


2010 ◽  
Vol 104 (2) ◽  
pp. 873-884 ◽  
Author(s):  
Hongmei Zhang ◽  
Edmund W. Rodgers ◽  
Wulf-Dieter C. Krenz ◽  
Merry C. Clark ◽  
Deborah J. Baro

Dopamine (DA) modifies the motor pattern generated by the pyloric network in the stomatogastric ganglion (STG) of the spiny lobster, Panulirus interruptus , by directly acting on each of the circuit neurons. The 14 pyloric neurons fall into six cell types, and DA actions are cell type specific. The transient potassium current mediated by shal channels ( IA) is a common target of DA modulation in most cell types. DA shifts the voltage dependence of IA in opposing directions in pyloric dilator (PD) versus lateral pyloric (LP) neurons. The mechanism(s) underpinning cell-type specific DA modulation of IA is unknown. DA receptors (DARs) can be classified as type 1 (D1R) or type 2 (D2R). D1Rs and D2Rs are known to increase and decrease intracellular cAMP concentrations, respectively. We hypothesized that the opposing DA effects on PD and LP IA were due to differences in DAR expression patterns. In the present study, we found that LP expressed somatodendritic D1Rs that were concentrated near synapses but did not express D2Rs. Consistently, DA modulation of LP IA was mediated by a Gs-adenylyl cyclase-cAMP-protein kinase A pathway. Additionally, we defined antagonists for lobster D1Rs (flupenthixol) and D2Rs (metoclopramide) in a heterologous expression system and showed that DA modulation of LP IA was blocked by flupenthixol but not by metoclopramide. We previously showed that PD neurons express D2Rs, but not D1Rs, thus supporting the idea that cell specific effects of DA on IA are due to differences in receptor expression.


2012 ◽  
Vol 108 (10) ◽  
pp. 2846-2856 ◽  
Author(s):  
Mark D. Kvarta ◽  
Ronald M. Harris-Warrick ◽  
Bruce R. Johnson

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.


1998 ◽  
Vol 79 (4) ◽  
pp. 2063-2069 ◽  
Author(s):  
Amir Ayali ◽  
Bruce R. Johnson ◽  
Ronald M. Harris-Warrick

Ayali, Amir, Bruce R. Johnson, and Ronald M. Harris-Warrick. Dopamine modulates graded and spike-evoked synaptic inhibition independently at single synapses in pyloric network of lobster. J. Neurophysiol. 79: 2063–2069, 1998. Bath application of dopamine (DA) modifies the rhythmic motor pattern generated by the pyloric network in the stomatogastric ganglion of the spiny lobster, Panulirus interruptus. Synaptic transmission between network members is an important target of DA action. All pyloric neurons employ both graded transmitter release and action-potential–mediated synaptic inhibition. DA was previously shown to alter the graded synaptic strength of every pyloric synapse. In this study, we compared DA's effects on action-potential–mediated and graded synaptic inhibition at output synapses of the lateral pyloric (LP) neuron. At each synapse the postsynaptic cell tested was isolated from other descending and pyloric synaptic inputs. DA caused a reduction in the size of the LP spike-evoked inhibitory postsynaptic potentials (IPSPs) in the pyloric dilator (PD) neuron. The change in IPSP size was significantly and linearly correlated with DA-induced reduction in the input resistance of the postsynaptic PD neuron. In contrast, graded inhibition, tested in the same preparations after superfusing the stomatogastric ganglion (STG) with tetrodotoxin (TTX), was consistently enhanced by DA. DA shifted the amplitude of spike-evoked IPSPs in the same direction as the alteration of the postsynaptic cell input resistance at two additional synapses tested: DA weakened the LP spike-mediated inhibition of the ventricular dilator (VD) and reduced the VD input resistance, while strengthening the LP → pyloric constrictor (PY) synapse and increasing PY input resistance. As previously reported, graded inhibition was enhanced at these two LP output synapses. We conclude that DA can differentially modulate the spike-evoked and graded components of synapses between members of a central pattern generator network. At the synapses we studied, actions on the presynaptic cell predominate in the modulation of graded transmission, whereas effects on postsynaptic cells predominate in the regulation of spike-evoked IPSPs.


2002 ◽  
Vol 88 (6) ◽  
pp. 2942-2953 ◽  
Author(s):  
Muriel Thoby-Brisson ◽  
John Simmers

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-dependent properties of the neurons themselves. Whereas pyloric neurons, including the PD, lateral pyloric, and pyloric cell types, are unable to generate burst-producing membrane potential oscillations in the short-term absence of extrinsic modulatory inputs, in long-term decentralized ganglia, the same cells are able to oscillate spontaneously, even after experimental isolation in situ from all other elements in the pyloric network. In PD neurons this reacquisition of rhythmicity is associated with a net reduction in outward tetraethylammonium-sensitive ionic currents that include a delayed-rectifier type potassium current ( I Kd) and a calcium-dependent K+ current, I KCa. By contrast, long-term STG decentralization caused enhancement of a hyperpolarization-activated inward current that resembles I h. These results are consistent with the hypothesis that modulatory inputs sustain the modulation-dependent rhythmogenic character of the pyloric network by continuously regulating the balance of membrane conductances that underlie neuronal oscillation.


1997 ◽  
Vol 78 (6) ◽  
pp. 3210-3221 ◽  
Author(s):  
Bruce R. Johnson ◽  
Ronald M. Harris-Warrick

Johnson, Bruce R. and Ronald M. Harris-Warrick. Amine modulation of glutamate responses from pyloric motor neurons in lobster stomatogastric ganglion. J. Neurophysiol. 78: 3210–3221, 1997. The amines dopamine (DA), serotonin (5-HT), and octopamine (Oct) each elicit a distinctive motor pattern from a quiescent pyloric network in the lobster stomatogastric ganglion (STG). We previously have demonstrated that these amines alter the synaptic strength at multiple, distributed sites within the pyloric network that could contribute to the amine-induced motor patterns. Here, we examined the postsynaptic contribution to these changes in synaptic strength by determining how the amines modify responses of pyloric motor neurons to glutamate (Glu), one of the network transmitters, applied iontophoretically into the STG neuropil. Dopamine reduced the Glu responses of the pyloric dilator (PD), ventricular dilator (VD), and inferior cardiac (IC) neurons and enhanced the Glu responses of the lateral pyloric (LP) and pyloric constrictor (PY) neurons. The only effect of 5-HT was to reduce the Glu response of the VD neuron. Oct enhanced the Glu responses of the LP and PY neurons but did not affect the PD, VD, and IC responses. We also examined amine effects on the depolarizing responses to iontophoresed acetylcholine (ACh) in the PD and VD and found that they paralleled the amine effects on Glu responses in these neurons. This suggests that amine modulation of PD and VD responses to Glu and ACh may be explained by general changes in the ionic conductance of these neurons. We compare our results with our earlier work describing amine effects on synaptic strength and input resistance to show that amines act at both pre- and postsynaptic sites to modify graded synaptic transmission in the pyloric network.


1995 ◽  
Vol 74 (1) ◽  
pp. 437-452 ◽  
Author(s):  
B. R. Johnson ◽  
J. H. Peck ◽  
R. M. Harris-Warrick

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)


2001 ◽  
Vol 85 (4) ◽  
pp. 1424-1435 ◽  
Author(s):  
Patsy S. Dickinson ◽  
Jane Hauptman ◽  
John Hetling ◽  
Anand Mahadevan

The neuropeptide red pigment concentrating hormone (RPCH), which we have previously shown to activate the cardiac sac motor pattern and lead to a conjoint gastric mill-cardiac sac pattern in the spiny lobster Panulirus, also activates and modulates the pyloric pattern. Like the activity of gastric mill neurons in RPCH, the pattern of activity in the pyloric neurons is considerably more complex than that seen in control saline. This reflects the influence of the cardiac sac motor pattern, and particularly the upstream inferior ventricular (IV) neurons, on many of the pyloric neurons. RPCH intensifies this interaction by increasing the strength of the synaptic connections between the IV neurons and their targets in the stomatogastric ganglion. At the same time, RPCH enhances postinhibitory rebound in the lateral pyloric (LP) neuron. Taken together, these factors largely explain the complex pyloric pattern recorded in RPCH in Panulirus.


1988 ◽  
Vol 136 (1) ◽  
pp. 53-87
Author(s):  
PATSY S. DICKINSON ◽  
FRÉDÉRIC NAGY ◽  
MAURICE MOULINS

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.


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