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

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.

1994 ◽  
Vol 71 (6) ◽  
pp. 2490-2502 ◽  
Author(s):  
F. Nagy ◽  
P. Cardi

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.


1994 ◽  
Vol 71 (6) ◽  
pp. 2477-2489 ◽  
Author(s):  
F. Nagy ◽  
P. Cardi ◽  
I. Cournil

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.


2019 ◽  
Vol 122 (4) ◽  
pp. 1623-1633
Author(s):  
Diana Martinez ◽  
Joseph M. Santin ◽  
David Schulz ◽  
Farzan Nadim

Many neurons receive synchronous input from heterogeneous presynaptic neurons with distinct properties. An instructive example is the crustacean stomatogastric pyloric circuit pacemaker group, consisting of the anterior burster (AB) and pyloric dilator (PD) neurons, which are active synchronously and exert a combined synaptic action on most pyloric follower neurons. Previous studies in lobster have indicated that AB is glutamatergic, whereas PD is cholinergic. However, although the stomatogastric system of the crab Cancer borealis has become a preferred system for exploration of cellular and synaptic basis of circuit dynamics, the pacemaker synaptic output has not been carefully analyzed in this species. We examined the synaptic properties of these neurons using a combination of single-cell mRNA analysis, electrophysiology, and pharmacology. The crab PD neuron expresses high levels of choline acetyltransferase and the vesicular acetylcholine transporter mRNAs, hallmarks of cholinergic neurons. In contrast, the AB neuron expresses neither cholinergic marker but expresses high levels of vesicular glutamate transporter mRNA, consistent with a glutamatergic phenotype. Notably, in the combined synapses to follower neurons, 70–75% of the total current was blocked by putative glutamatergic blockers, but short-term synaptic plasticity remained unchanged, and although the total pacemaker current in two follower neuron types was different, this difference did not contribute to the phasing of the follower neurons. These findings provide a guide for similar explorations of heterogeneous synaptic connections in other systems and a baseline in this system for the exploration of the differential influence of neuromodulators. NEW & NOTEWORTHY The pacemaker-driven pyloric circuit of the Jonah crab stomatogastric nervous system is a well-studied model system for exploring circuit dynamics and neuromodulation, yet the understanding of the synaptic properties of the two pacemaker neuron types is based on older analyses in other species. We use single-cell PCR and electrophysiology to explore the neurotransmitters used by the pacemaker neurons and their distinct contribution to the combined synaptic potentials.


1990 ◽  
Vol 64 (5) ◽  
pp. 1574-1589 ◽  
Author(s):  
S. L. Hooper ◽  
M. Moulins

1. In the lobster Palinurus vulgaris a sensory input in the lateral posterolateral nerve (lpln) of the stomatogastric nervous system (STS) is able to turn on the cardiac sac (CS) network and to induce dramatic long-lasting alterations in the output of the pyloric network. This long-lasting alteration of pyloric network output consists primarily of changes in the activity of the two neurons that innervate the muscles of the cardiopyloric valve of the stomach, with the dilator neuron (the ventricular dilator, VD) transferring from the pyloric network to the CS network and the constrictor neuron (the inferior cardiac, IC) shifting to fire earlier in the pyloric pattern. 2. The inferior ventricular (IV) neurons of the CS network make complex multiaction synaptic connections onto several pyloric neurons in a related species, Panulirus interruptus. We show that many of the short-term alterations in pyloric activity observed during CS network bursts in Palinurus are due to similar IV neuron synaptic connections. However, the long-lasting effects of lpln stimulation on pyloric output are not due to this synaptic input, because 1) direct activation of the IV neurons does not induce long-lasting changes in pyloric activity and 2) pharmacologic disconnection of this synaptic input does not abolish lpln stimulation's long-lasting effects. Lpln stimulation therefore activates two different neuronal inputs to the pyloric network. 3. The transfer of the VD neuron from the pyloric to the CS network is the result of the concerted actions of these two inputs. Lpln stimulation turns on the CS network, and the IV neurons of the CS network excite the VD neuron and ensure it fires with the CS network. The second neuronal input (that not involving known CS network neurons) abolishes in a long-lasting fashion the VD neuron regenerative (plateau) properties, and thus suppresses the ability of the VD neuron to participate in the pyloric rhythmic pattern between CS network bursts. 4. Experimental manipulation of VD neuron activity can both mimic and reverse the effects of lpln stimulation on the IC neuron. The changes in IC neuron activity are therefore not due to direct lpln-activated synaptic input onto the IC neuron, but instead are indirect "network" effects arising from the changes in VD neuron activity.


2019 ◽  
Author(s):  
Erick Olivares ◽  
Eduardo J. Izquierdo ◽  
Randall D. Beer

AbstractMultiple mechanisms contribute to the generation, propagation, and coordination of the rhythmic patterns necessary for locomotion in Caenorhabditis elegans. Current experiments have focused on two possibilities: pacemaker neurons and stretch-receptor feedback. Here, we focus on whether it is possible that a chain of multiple network rhythmic pattern generators in the ventral nerve cord also contribute to locomotion. We use a simulation model to search for electrophysiological parameters of the anatomically constrained ventral nerve cord circuit that, when embodied and situated, can drive forward locomotion on agar, in the absence of pacemaker neurons or stretch-receptor feedback. Systematic exploration of the space of possible solutions reveals that there are multiple configurations that result in locomotion that is consistent with certain aspects of the kinematics of worm locomotion on agar. Analysis of the best solutions reveals that gap junctions between different classes of motorneurons in the ventral nerve cord can play key roles in coordinating the multiple rhythmic pattern generators.


1969 ◽  
Vol 54 (2) ◽  
pp. 212-231 ◽  
Author(s):  
Akira Watanabe ◽  
Shosaku Obara ◽  
Toyohiro Akiyama

The pacemaker neurons of the heart ganglion are innervated from the CNS through two pairs of acceleratory nerves. The effect of acceleratory nerve stimulation was examined with intracellular electrodes from the pacemaker cells. The major effects on the pacemaker potential were an increase in the rate of rise of the spontaneous depolarization and in the duration of the plateau. The aftereffect of stimulation could last for minutes. No clear excitatory postsynaptic potential (EPSP) was observed, however. On high frequency stimulation, a small depolarizing response (the initial response) was sometimes observed, but the major postsynaptic event was the following slow depolarization, or the enhancement of the pacemaker potential (the late response). With hyperpolarization the initial response did not significantly change its amplitude, but the late response disappeared, showing that the latter has the property of the local response. The membrane conductance did not increase with acceleratory stimulation. The injection of depolarizing current increased the rate of rise of the spontaneous depolarization, but only slightly in comparison with acceleratory stimulation, and did not increase the burst duration. It is concluded that the acceleratory effect is not mediated by the EPSP but is due to a direct action of the transmitter on the pacemaker membrane.


2002 ◽  
Vol 205 (18) ◽  
pp. 2825-2832 ◽  
Author(s):  
Amir Ayali ◽  
Yael Zilberstein ◽  
Netta Cohen

SUMMARYThe frontal ganglion (FG) is part of the insect stomatogastric nervous system and is found in most insect orders. Previous work has shown that in the desert locust, Schistocerca gregaria, the FG constitutes a major source of innervation to the foregut. In an in vitro preparation,isolated from all descending and sensory inputs, the FG spontaneously generated rhythmic multi-unit bursts of action potentials that could be recorded from all its efferent nerves. The consistent endogenous FG rhythmic pattern indicates the presence of a central pattern generator network. We found the appearance of in vitro rhythmic activity to be strongly correlated with the physiological state of the donor locust. A robust pattern emerged only after a period of saline superfusion, if the locust had a very full foregut and crop, or if the animal was close to ecdysis. Accordingly,haemolymph collected at these stages inhibited an ongoing rhythmic pattern when applied onto the ganglion. We present this novel central pattern generating system as a basis for future work on the neural network characterisation and its role in generating and controlling behaviour.


1993 ◽  
Vol 69 (5) ◽  
pp. 1475-1483 ◽  
Author(s):  
P. S. Dickinson ◽  
C. Mecsas ◽  
J. Hetling ◽  
K. Terio

1. The cardiac sac network, which controls the rhythmic contractions of the cardiac sac in the foregut of crustaceans, is distributed throughout the stomatogastric nervous system, including the oesophageal ganglion (OG), the commissural ganglia (CGs), and the stomatogastric ganglion (STG). A red pigment-concentrating hormone (RPCH)-like peptide is likewise widely distributed. 2. The effects that bath application of the neuropeptide RPCH to the different ganglia has on the cardiac sac pattern were studied. 3. RPCH applied to the STG, the OG, or the CGs elicited bursting activity in all the known components of the cardiac sac pattern, including the two motor neurons, cardiac sac dilators 1 and 2 (CD1 and CD2), and the inferior ventricular nerve (ivn) fibers. 4. A cardiac sac pattern was also elicited when RPCH was applied to either the STG, the OG, or the CGs after synapses in that ganglion had been blocked by low Ca2+ saline containing 20 mM Co2+. 5. These data suggest that the ivn fibers are sensitive to RPCH and respond to it by generating bursting activity at or near their terminals in all four ganglia. 6. Application of RPCH to either the STG or the OG also caused an increase in the amplitude of the postsynaptic potential (PSP) from the ivn fibers to both CD1 and CD2. The increase was largest in the ganglion to which the RPCH was applied. 7. Repeated stimulation of the ivn, mimicking the bursts that occur during cardiac sac activity, also caused an increase in PSP amplitude, and so facilitation resulting from activation of ivn bursting could account for a portion of the increased amplitude seen in RPCH.(ABSTRACT TRUNCATED AT 250 WORDS)


2007 ◽  
Vol 97 (3) ◽  
pp. 2239-2253 ◽  
Author(s):  
Pascale Rabbah ◽  
Farzan Nadim

Many rhythmically active networks involve heterogeneous populations of pacemaker neurons with potentially distinct synaptic outputs that can be differentially targeted by extrinsic inputs or neuromodulators, thereby increasing possible network output patterns. To understand the roles of heterogeneous pacemaker neurons, we characterized differences in synaptic output from the anterior burster (AB) and pyloric dilator (PD) neurons in the lobster pyloric network. These intrinsically distinct neurons are strongly electrically coupled, coactive, and constitute the pyloric pacemaker ensemble. During pyloric oscillations, the pacemaker neurons produce compound inhibitory synaptic connections to the follower lateral pyloric (LP) and pyloric constrictor (PY) neurons, which fire out of phase with AB/PD and with different delay times. Using pharmacological blockers, we separated the synapses originating from the AB and PD neurons and investigated their temporal dynamics. These synapses exhibited distinct short-term dynamics, depending on the presynaptic neuron type, and had different relative contributions to the total synaptic output depending on waveform shape and cycle frequency. However, paired comparisons revealed that the amplitude or dynamics of synapses from either the AB or PD neuron did not depend on the postsynaptic neuron type, LP or PY. To address the functional implications of these findings, we examined the correlation between synaptic inputs from the pacemakers and the burst onset phase of the LP and PY neurons in the ongoing pyloric rhythm. These comparisons showed that the activity of the LP and PY neurons is influenced by the peak phase and amplitude of the synaptic inputs from the pacemaker neurons.


2003 ◽  
Vol 89 (3) ◽  
pp. 1363-1377 ◽  
Author(s):  
Attila Szűcs ◽  
Reynaldo D. Pinto ◽  
Michail I. Rabinovich ◽  
Henry D. I. Abarbanel ◽  
Allen I. Selverston

The pyloric network of the lobster stomatogastric nervous system is one of the best described assemblies of oscillatory neurons producing bursts of action potentials. While the temporal patterns of bursts have been investigated in detail, those of spikes have received less attention. Here we analyze the intraburst firing patterns of pyloric neurons and the synaptic interactions shaping their dynamics in millisecond time scales not performed before. We find that different pyloric neurons express characteristic, cell-specific firing patterns in their bursts. Nonlinear analysis of the interspike intervals (ISIs) reveals distinctive temporal structures (‘interspike interval signatures’), which are found to depend on the synaptic connectivity of the network. We compare ISI patterns of the pyloric dilator (PD), lateral pyloric (LP), and ventricular dilator (VD) neurons in 1) normal conditions, 2) after blocking glutamatergic synaptic connections, and 3) in various functional configurations of the three neurons. Manipulation of the synaptic connectivity results in characteristic changes in the ISI signatures of the postsynaptic neurons. The intraburst firing pattern of the PD neuron is regularized by the inhibitory synaptic connection from the LP neuron as revealed in current-clamp experiments and also as reconstructed with a dynamic clamp. On the other hand, mutual inhibition between the LP and VD neurons tend to produce more irregular bursts with increased spike jitter. The results show that synaptic interactions fine-tune the output of pyloric neurons. The present data also suggest a way of processing of synaptic information: bursting neurons are capable of encoding incoming signals by altering the fine structure of their intraburst spike patterns.


Sign in / Sign up

Export Citation Format

Share Document