A rhythmic modulatory gating system in the stomatogastric nervous system of Homarus gammarus. I. Pyloric-related neurons in the commissural ganglia

1994 ◽  
Vol 71 (6) ◽  
pp. 2477-2489 ◽  
Author(s):  
F. Nagy ◽  
P. Cardi ◽  
I. Cournil
Keyword(s):  
Lucifer Yellow ◽  
Spiny Lobster ◽  
Electrical Coupling ◽  
Firing Frequency ◽  
Gamma Aminobutyric Acid ◽  
Stomatogastric Nervous System ◽  
Panulirus Interruptus ◽  
Homarus Gammarus ◽  
Commissural Neurons ◽  
Pyloric Network

1. Operation of the pyloric neural network in the crustacean stomatogastric ganglion (STG) depends on constant firing of modulatory inputs from anterior ganglia. We have identified two bilaterally symmetrical pairs of these inputs in the commissural ganglia (COGs) of the European rock lobster Homarus gammarus. During operation of the pyloric CPG, they fired in pyloric time, out of phase with the pyloric pacemakers. 2. One of the pair was the commissural pyloric (CP) neuron and the other was homologous to the P neuron described in the spiny lobster Panulirus interruptus. We describe their morphology and location in the COG. The CP neuron projected to the STG via the superior esophageal nerve (son) and the stomatogastric nerve (stn), whereas the P neuron projected via the inferior esophageal nerve (ion) and stn. 3. To determine the total number of commissural neurons projecting to the STG, we used cobalt and Lucifer yellow backfilling from their cut axons in the stn. With the ion cut, there were between 8 to 12 labeled somata in each COG including CP cell body, whereas only 2 somata (including P) were labeled with the son cut. Among these neurons, CP and P appeared to be the only commissural neurons that fired in pyloric time and projected in the STG on the pyloric network. 4. The CP neuron produced monosynaptic excitatory postsynaptic potentials (EPSPs) on the pyloric dilator (PD), lateral pyloric (LP), and inferior cardiac (IC) neurons, whereas the P neuron produced monosynaptic EPSPs on all pyloric motoneurons but IC. The P neuron was gamma-aminobutyric acid immunoreactive, and the P-derived EPSPs in pyloric neurons were reversibly blocked by bicuculline, picrotoxin, and D-tubocurarine. 5. The CP and P neurons were electrically coupled, and modification of membrane potential in either one of them appreciably changed the firing frequency of the coupled neuron. 6. A negative-feedback loop from the pyloric anterior burster (AB) interneuron provoked simultaneous rhythmic inhibitions in the P and CP neurons. Together with the electrical coupling, the rhythmic inhibition contributed to synchronize firing of the two commissural neurons. 7. The following papers in the series of describe the modulatory and rhythmic control exerted by the P and CP neurons over the pyloric pattern generator.

A rhythmic modulatory gating system in the stomatogastric nervous system of Homarus gammarus. II. Modulatory control of the pyloric CPG

1994 ◽  
Vol 71 (6) ◽  
pp. 2490-2502 ◽  
Author(s):  
F. Nagy ◽  
P. Cardi
Keyword(s):  
Activity Patterns ◽  
Firing Frequency ◽  
Network Activity ◽  
Stomatogastric Nervous System ◽  
Homarus Gammarus ◽  
Commissural Neurons ◽  
Pyloric Network ◽  
State Dependent ◽  
Pyloric Dilator ◽  
Network Operation

1. In the European rock lobster, Homarus gammarus, two bilaterally symmetrical pairs of commissural neurons, P and commissural pyloric (CP), evoke excitatory postsynaptic potentials in the neurons of the pyloric motor network. The present paper shows that the two commissural neurons also exert a modulatory control over the pyloric network. 2. The P and CP neurons were active during ongoing pyloric rhythms. Ongoing pyloric activity was terminated when the neurons were hyperpolarized to inhibit their firing. 3. When the pyloric network was quiescent, depolarizing either the P or CP neuron induced a robust pyloric rhythm. 4. We studied the actions of the P and CP neurons on individual pyloric neurons isolated in situ from network interactions by a photoinactivation techniques. The P neuron induced oscillatory properties in the pacemaker pyloric dilator (PD) neurons and the motor neuron, ventricular dilator (VD), whereas the CP neuron induced rhythmogenic properties in all the network neurons but VD. Together, the P-CP neurons modulated the entire pyloric network. The modulatory effects of the P-CP neurons did not outlast the duration of their discharge. 5. The P and CP neurons also controlled the firing frequency of all the pyloric neurons. They may, in addition, control phasing of the constrictor neurons discharges, but this effect was state-dependent and occurred only when the pyloric central pattern generator was functioning weakly. Their role in providing flexibility to the network operation appeared relatively limited. 6. We conclude that the P and CP neurons are good candidates for insuring long-term maintenance of pyloric network activity patterns.

A rhythmic modulatory gating system in the stomatogastric nervous system of Homarus gammarus. III. Rhythmic control of the pyloric CPG

1994 ◽  
Vol 71 (6) ◽  
pp. 2503-2516 ◽  
Author(s):  
P. Cardi ◽  
F. Nagy
Keyword(s):  
Differential Sensitivity ◽  
Excitatory Postsynaptic Potential ◽  
Rhythmic Pattern ◽  
Stomatogastric Nervous System ◽  
Pacemaker Neurons ◽  
Homarus Gammarus ◽  
Commissural Neurons ◽  
Pyloric Network ◽  
F Cells ◽  
Discrete Values

1. Two modulatory neurons, P and commissural pyloric (CP), known to be involved in the long-term maintenance of pyloric central pattern generator operation in the rock lobster Homarus gammarus, are members of the commissural pyloric oscillator (CPO), a higher-order oscillator influencing the pyloric network. 2. The CP neuron was endogenously oscillating in approximately 30% of the preparations in which its cell body was impaled. Rhythmic inhibitory feedback from the pyloric pacemaker anterior burster (AB) neuron stabilized the CP neuron's endogenous rhythm. 3. The organization of the CPO is described. Follower commissural neurons, the F cells, and the CP neuron receive a common excitatory postsynaptic potential from another commissural neuron, the large exciter (LE). When in oscillatory state, CP in turn excites the LE neuron. This positive feedback may maintain long episodes of CP oscillations. 4. The pyloric pacemaker neurons follow the CPO rhythm with variable coordination modes (i.e., 1:1, 1:2) and switch among these modes when their membrane potential is modified. The CPO inputs strongly constrain the pyloric period, which as a result may adopt only a few discrete values. This effect is based on mechanisms of entrainment between the CPO and the pyloric oscillator. 5. Pyloric constrictor neurons show differential sensitivity from the pyloric pacemaker neurons with respect to the CPO inputs. Consequently, their bursting period can be a shorter harmonic of the bursting period of the pyloric pacemakers neurons. 6. The CPO neurons seem to be the first example of modulatory gating neurons that also give timing cues to a rhythmic pattern generating network.

scholarly journals Roles for electrical coupling in neural circuits as revealed by selective neuronal deletions

1984 ◽  
Vol 112 (1) ◽  
pp. 147-167 ◽  
Author(s):  
E. Marder
Keyword(s):  
Neural Circuits ◽  
Neural Circuit ◽  
Lucifer Yellow ◽  
Electrical Coupling ◽  
Separate Analysis ◽  
Panulirus Interruptus ◽  
Pyloric Network ◽  
Synaptic Interactions ◽  
Pyloric Dilator ◽  
The Individual

Understanding fully the operation of a neural circuit requires both a description of the individual neurones within the circuit as well as the characterization of their synaptic interactions. These aims are often particularly difficult to achieve in neural circuits containing electrically-coupled neurones. In recent years two new methods (photoinactivation after Lucifer Yellow injection and intracellular injection of pronase) have been employed to delete selectively single neurones or small groups of neurones from neural circuits. These techniques have been successfully used in the analysis of circuits containing electrically-coupled neurones. In several systems new roles for electrical synapses in the integrative function of neural circuits have been proposed. In the nervous systems of both the leech and lobster it is now thought that synaptic interactions previously thought to be direct are mediated through an interposed, electrically-coupled neurone. In the pyloric system of the stomatogastric ganglion of the lobster, Panulirus interruptus, the Lucifer Yellow photoinactivation technique has permitted a separate analysis of the properties of several electrically-coupled neurones previously thought quite similar. We now know that the Anterior Burster (AB) interneurone and the Pyloric Dilator (PD) motor neurones, which together act as the pacemaker ensemble for the pyloric network, differ in many regards including their intrinsic ability to generate bursting pacemaker potentials, their neurotransmitters, their sensitivity to some neurotransmitters and hormones, the neural inputs they receive and their pattern of synaptic connectivity. These results will be discussed in the context of the role of electrical coupling in neuronal integration.

Electrically coupled pacemaker neurons respond differently to same physiological inputs and neurotransmitters

1984 ◽  
Vol 51 (6) ◽  
pp. 1362-1374 ◽  
Author(s):  
E. Marder ◽  
J. S. Eisen
Keyword(s):  
Motor Neurons ◽  
Slow Wave ◽  
Lucifer Yellow ◽  
Electrical Coupling ◽  
Excitatory Postsynaptic Potential ◽  
Panulirus Interruptus ◽  
Bursting Neuron ◽  
Postsynaptic Potential ◽  
Pyloric Dilator ◽  
Muscarinic Cholinergic

The two pyloric dilator (PD) motor neurons and the single anterior burster (AB) interneuron are electrically coupled and together comprise the pacemaker for the pyloric central pattern generator of the stomatogastric ganglion of the lobster, Panulirus interruptus. Previous work (31) has shown that the AB neuron is an endogenously bursting neuron, while the PD neuron is a conditional burster. In this paper the effects of physiological inputs and neurotransmitters on isolated PD neurons and AB neurons were studied using the lucifer yellow photoinactivation technique (33). Stimulation of the inferior ventricular nerve (IVN) fibers at high frequencies elicits a triphasic response in AB and PD neurons: a rapid excitatory postsynaptic potential (EPSP) followed by a slow inhibitory postsynaptic potential (IPSP), followed by an enhancement of the pacemaker slow-wave depolarizations. Photoinactivation experiments indicate that the enhancement of the slow wave is due primarily to actions of the IVN fibers on the PD neurons but not on the AB neuron. Bath-applied dopamine dramatically alters the motor output of the pyloric system. Photoinactivation experiments show that 10(-4) M dopamine increases the amplitude and frequency of the slow-wave depolarizations recorded in the AB neurons but hyperpolarizes and inhibits the PD neurons. Bath-applied serotonin increases the frequency and amplitude of the slow-wave depolarizations in the AB neuron but has no effect on PD neurons. Pilocarpine, a muscarinic cholinergic agonist, stimulates slow-wave depolarization production in both PD neurons and the AB neuron, but the waveform and frequency of the slow waves elicited are quite different. These results show that although the electrically coupled PD and AB neurons always depolarize synchronously and act together as the pacemaker for the pyloric system, they respond differently to a neuronal input and to several putative neuromodulators. Thus, despite electrical coupling sufficient to ensure synchronous activity, the PD and AB neurons can be modulated independently.

Serotonin Transduction Cascades Mediate Variable Changes in Pyloric Network Cycle Frequency in Response to the Same Modulatory Challenge

2008 ◽  
Vol 99 (6) ◽  
pp. 2844-2863 ◽  
Author(s):  
Nadja Spitzer ◽  
Gennady Cymbalyuk ◽  
Hongmei Zhang ◽  
Donald H. Edwards ◽  
Deborah J. Baro
Keyword(s):  
Steady State ◽  
Spiny Lobster ◽  
Cycle Frequency ◽  
Panulirus Interruptus ◽  
Response System ◽  
Pyloric Network ◽  
Bath Application ◽  
The Mean ◽  
Circuit Output ◽  
Sustained Increase

A fundamental question in systems biology addresses the issue of how flexibility is built into modulatory networks such that they can produce context-dependent responses. Here we examine flexibility in the serotonin (5-HT) response system that modulates the cycle frequency (cf) of a rhythmic motor output. We found that depending on the preparation, the same 5-min bath application of 5-HT to the pyloric network of the California spiny lobster, Panulirus interruptus, could produce a significant increase, decrease, or no change in steady-state cf relative to baseline. Interestingly, the mean circuit output was not significantly different among preparations prior to 5-HT application. We developed pharmacological tools to examine the preparation-to-preparation variability in the components of the 5-HT response system. We found that the 5-HT response system consisted of at least three separable components: a 5-HT2βPan-like component mediated a rapid decrease followed by a sustained increase in cf; a 5-HT1αPan-like component produced a small and usually gradual increase in cf; at least one other component associated with an unknown receptor mediated a sustained decrease in cf. The magnitude of the change in cf produced by each component was highly variable, so that when summed they could produce either a net increase, decrease, or no change in cf depending on the preparation. Overall, our research demonstrates that the balance of opposing components of the 5-HT response system determines the direction and magnitude of 5-HT–induced change in steady-state cf relative to baseline.

scholarly journals Dopamine-induced oscillations of the pyloric pacemaker neuron rely on release of calcium from intracellular stores

2011 ◽  
Vol 106 (3) ◽  
pp. 1288-1298 ◽  
Author(s):  
Lolahon R. Kadiri ◽  
Alex C. Kwan ◽  
Watt W. Webb ◽  
Ronald M. Harris-Warrick
Keyword(s):  
Spiny Lobster ◽  
Ionic Currents ◽  
Calcium Currents ◽  
Cycle Frequency ◽  
Panulirus Interruptus ◽  
Two Photon Microscopy ◽  
Two Photon ◽  
Pyloric Network ◽  
Nervous System Function ◽  
External Calcium

Endogenously bursting neurons play central roles in many aspects of nervous system function, ranging from motor control to perception. The properties and bursting patterns generated by these neurons are subject to neuromodulation, which can alter cycle frequency and amplitude by modifying the properties of the neuron's ionic currents. In the stomatogastric ganglion (STG) of the spiny lobster, Panulirus interruptus, the anterior burster (AB) neuron is a conditional oscillator in the presence of dopamine (DA) and other neuromodulators and serves as the pacemaker to drive rhythmic output from the pyloric network. We analyzed the mechanisms by which DA evokes bursting in the AB neuron. Previous work showed that DA-evoked bursting is critically dependent on external calcium (Harris-Warrick RM, Flamm RE. J Neurosci 7: 2113–2128, 1987). Using two-photon microscopy and calcium imaging, we show that DA evokes the release of calcium from intracellular stores well before the emergence of voltage oscillations. When this release from intracellular stores is blocked by antagonists of ryanodine or inositol trisphosphate (IP3) receptor channels, DA fails to evoke AB bursting. We further demonstrate that DA enhances the calcium-activated inward current, ICAN, despite the fact that it significantly reduces voltage-activated calcium currents. This suggests that DA-induced release of calcium from intracellular stores activates ICAN, which provides a depolarizing ramp current that underlies endogenous bursting in the AB neuron.

Dopamine Modulates Graded and Spike-Evoked Synaptic Inhibition Independently at Single Synapses in Pyloric Network of Lobster

1998 ◽  
Vol 79 (4) ◽  
pp. 2063-2069 ◽  
Author(s):  
Amir Ayali ◽  
Bruce R. Johnson ◽  
Ronald M. Harris-Warrick
Keyword(s):  
Action Potential ◽  
Spiny Lobster ◽  
Motor Pattern ◽  
Input Resistance ◽  
Stomatogastric Ganglion ◽  
Synaptic Inhibition ◽  
Panulirus Interruptus ◽  
Pyloric Network ◽  
Bath Application ◽  
Postsynaptic Cell

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.

Follower Neurons in Lobster (Panulirus interruptus) Pyloric Network Regulate Pacemaker Period in Complementary Ways

2003 ◽  
Vol 89 (3) ◽  
pp. 1327-1338 ◽  
Author(s):  
Adam L. Weaver ◽  
Scott L. Hooper
Keyword(s):  
Neural Networks ◽  
Electrical Coupling ◽  
Network Activity ◽  
Cycle Period ◽  
Period Range ◽  
Panulirus Interruptus ◽  
Pyloric Network ◽  
Baseline Activity ◽  
Insight Into

Distributed neural networks (ones characterized by high levels of interconnectivity among network neurons) are not well understood. Increased insight into these systems can be obtained by perturbing network activity so as to study the functions of specific neurons not only in the network's “baseline” activity but across a range of network activities. We applied this technique to study cycle period control in the rhythmic pyloric network of the lobster, Panulirus interruptus. Pyloric rhythmicity is driven by an endogenous oscillator, the Anterior Burster (AB) neuron. Two network neurons feed back onto the pacemaker, the Lateral Pyloric (LP) neuron by inhibition and the Ventricular Dilator (VD) neuron by electrical coupling. LP and VD neuron effects on pyloric cycle period can be studied across a range of periods by altering period by injecting current into the AB neuron and functionally removing (by hyperpolarization) the LP and VD neurons from the network at each period. Within a range of pacemaker periods, the LP and VD neurons regulate period in complementary ways. LP neuron removal speeds the network and VD neuron removal slows it. Outside this range, network activity is disrupted because the LP neuron cannot follow slow periods, and the VD neuron cannot follow fast periods. These neurons thus also limit, in complementary ways, normal pyloric activity to a certain period range. These data show that follower neurons in pacemaker networks can play central roles in controlling pacemaker period and suggest that in some cases specific functions can be assigned to individual network neurons.

Aminergic modulation in lobster stomatogastric ganglion. II. Target neurons of dopamine, octopamine, and serotonin within the pyloric circuit

1986 ◽  
Vol 55 (5) ◽  
pp. 866-881 ◽  
Author(s):  
R. E. Flamm ◽  
R. M. Harris-Warrick
Keyword(s):  
Neural Circuit ◽  
Lucifer Yellow ◽  
Spiny Lobster ◽  
Motor Pattern ◽  
Preceding Paper ◽  
Cell Types ◽  
Stomatogastric Ganglion ◽  
Synaptic Organization ◽  
Potential Oscillations ◽  
Panulirus Interruptus

In the preceding paper, we describe how dopamine, octopamine, and serotonin modulate the neural circuit generating a well-described motor pattern, the pyloric rhythm of the stomatogastric ganglion in the spiny lobster, Panulirus interruptus. In this paper, we identify the neurons within the pyloric circuit that are directly affected by each amine. We accomplished this by isolating each pyloric neuron from all known synaptic input, using a combination of Lucifer yellow photoinactivation of presynaptic neurons and pharmacological blockade by pyloric neurotransmitters. Dopamine, octopamine, and serotonin were bath applied to the preparation, and the responses of synaptically isolated neurons were recorded. Each amine had a unique constellation of effects on the neurons of the pyloric circuit. Almost every neuron in the circuit was directly affected by each amine. Dopamine and octopamine modulated every neuron, whereas serotonin affected four of the six cell types. Each amine had multiple effects among pyloric neurons including the induction of endogenous rhythmic bursting activity, initiation or enhancement of tonic firing activity, and inhibition accompanied by hyperpolarization. All three amines induced rhythmic bursting in one neuron (the AB neuron), but the form of the underlying slow-wave membrane-potential oscillations was different with octopamine than with dopamine and serotonin. Our knowledge of the effects of each amine on each pyloric neuron, combined with the extensive knowledge of the synaptic organization of the pyloric circuit, has allowed us to explain qualitatively the major aspects of the unique variants of the pyloric motor rhythm that each amine produces in the synaptically intact circuit.

Sensory alteration of motor patterns in the stomatogastric nervous system of the spiny lobster Panulirus interruptus

1982 ◽  
Vol 97 (1) ◽  
pp. 137-152
Author(s):  
K. A. Sigvardt ◽  
B. Mulloney
Keyword(s):  
Spiny Lobster ◽  
Sensory Nerves ◽  
Stomatogastric Nervous System ◽  
Impulse Frequency ◽  
Motor Patterns ◽  
Panulirus Interruptus ◽  
Sensory Axons ◽  
Lateral Posterior ◽  
Different Parts ◽  
Stimulation Of

1. Stretching the pyloric region of the lobster's stomach in a manner that resembles pyloric dilation triggers a prolonged burst of impulses in two interneurones with axons in the inferior ventricular nerve (IVN). The burst is activated in the oesophageal ganglion by sensory axons that traverse the lateral ventricular nerves, the dorsal ventricular nerve and the stomatogastric nerve. These sensory axons do not appear to make synaptic contacts in the stomatogastric ganglion. 2. Electrical stimulation of sensory branches of the pyloric nerve triggers similar bursts in the IVN interneurones. 3. The burst of impulses in the IVN interneurones lasts from 2 to 30 s and the impulse frequency ranges from 10 to 80 Hz in different parts of the burst. Once triggered, burst structure and burst duration are independent of the intensity or duration of stimuli applied to the sensory nerves. 4. These bursts alter both the gastric and pyloric motor patterns. The IVN interneurones make a complex pattern of synapses with stomatogastric neurones. These are: pyloric dilators (PD) - excitation and slow inhibition; ventricular dilator (VD) - excitation; gastric mill (GM) neurones - inhibition; lateral posterior gastric neurones (LPGN) - inhibition; and Interneurone I (Int I) - excitation and slow inhibition. The size of the p.s.p.s at each of these synapses depends on the duration and impulse-frequency of the burst in the presynaptic neurones, which in turn alters the firing patterns of the stomatogastric neurones in various ways.

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