scholarly journals The differential contribution of pacemaker neurons to synaptic transmission in the pyloric network of the Jonah crab, Cancer borealis

2019 ◽  
Vol 122 (4) ◽  
pp. 1623-1633
Author(s):  
Diana Martinez ◽  
Joseph M. Santin ◽  
David Schulz ◽  
Farzan Nadim
Keyword(s):  
Single Cell ◽  
Glutamate Transporter ◽  
Cholinergic Neurons ◽  
Synaptic Action ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Pacemaker Neurons ◽  
Pyloric Network ◽  
Single Cell Pcr ◽  
Pyloric Dilator

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.

scholarly journals The differential contribution of pacemaker neurons to synaptic transmission in the pyloric network of the Jonah crab, Cancer borealis

2019 ◽  
Author(s):  
Diana Martinez ◽  
Joseph M. Santin ◽  
David Schulz ◽  
Farzan Nadim
Keyword(s):  
Glutamate Transporter ◽  
Cholinergic Neurons ◽  
Synaptic Action ◽  
Cancer Borealis ◽  
Pacemaker Neurons ◽  
Pyloric Network ◽  
Pyloric Dilator ◽  
Mrna Analysis ◽  
Differential Contribution ◽  
Stomatogastric System

AbstractMany 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. Although the stomatogastric system of the crab Cancer borealis has become a preferred model system for exploration of cellular and synaptic basis of circuit dynamics, in this species, the identity of the PD neuron neurotransmitter and its contribution to the total pacemaker group synaptic output remain unexplored. We examined the synaptic properties of the crab PD neuron 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. Conversely, the AB neuron does not express either of these cholinergic markers, and expresses high levels of vesicular glutamate transporter mRNA, consistent with a glutamatergic phenotype. Notably, in the combined synapses to the LP and PY neurons, the major contribution is from the glutamatergic AB neuron and only between 25-30% of the synaptic strength is due to the PD neuron. However, there was no difference between the short-term synaptic plasticity in the total pacemaker synapse compared to that of the PD neuron alone. 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.

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.

scholarly journals Distinct Synaptic Dynamics of Heterogeneous Pacemaker Neurons in an Oscillatory Network

2007 ◽  
Vol 97 (3) ◽  
pp. 2239-2253 ◽  
Author(s):  
Pascale Rabbah ◽  
Farzan Nadim
Keyword(s):  
Temporal Dynamics ◽  
Neuron Type ◽  
Presynaptic Neuron ◽  
Cycle Frequency ◽  
Pacemaker Neurons ◽  
Synaptic Inputs ◽  
Pyloric Network ◽  
Pyloric Dilator ◽  
Network Output ◽  
Synaptic Dynamics

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.

Synaptic Modulation of the Interspike Interval Signatures of Bursting Pyloric 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
Keyword(s):  
Interspike Interval ◽  
Synaptic Connectivity ◽  
Stomatogastric Nervous System ◽  
Firing Patterns ◽  
Synaptic Modulation ◽  
Pyloric Network ◽  
Synaptic Interactions ◽  
Pyloric Dilator ◽  
Temporal Structures ◽  
Spike Patterns

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.

Sensory input induces long-lasting changes in the output of the lobster pyloric network

1990 ◽  
Vol 64 (5) ◽  
pp. 1555-1573 ◽  
Author(s):  
S. L. Hooper ◽  
M. Moulins ◽  
L. Nonnotte
Keyword(s):  
Neural Network ◽  
Sensory Input ◽  
Nervous Activity ◽  
Low Frequency ◽  
Neuron Activity ◽  
Stomatogastric Nervous System ◽  
Cycle Frequency ◽  
Pyloric Network ◽  
Pyloric Dilator ◽  
Stimulation Of

1. A long-lasting restructuring of the pyloric neural network of the lobster stomatogastric nervous system (STS) by a multisynaptic sensory afferent is described. This restructuring can be obtained either by mechanical stimulation of the pyloric region of the stomach or by brief high-frequency electrical stimulation of a nerve that innervates this region, the lateral posterolateral nerve (lpln). Electron microscopy shows that this nerve contains several thousand very small fibers (approximately 0.3 microns diam), the activation of some subset of which is responsible for the effects of lpln stimulation. 2. These stimulation paradigms result in both short-duration changes in pyloric activity and modulatory effects long outlasting the stimulus end. The long-lasting changes include the cessation of rhythmic ventricular dilator (VD) and lateral pyloric (LP) neuron activity, and thus result in a reduced pyloric pattern in which only the pyloric dilator (PD), inferior cardiac (IC), anterior burster (AB), and pyloric (PY) neurons are active. 3. Tonic low-frequency lpln stimulation, alternatively, results in the VD neuron rhythmically firing long spike bursts with a cycle frequency much slower than that of the pyloric network while an otherwise complete pyloric pattern continues. In this new bursting pattern the VD neuron fires exclusively with another STS neural network, the cardiac sac (CS) network, and thus functionally "switches" from the pyloric to the CS network. This switch of the VD neuron from the pyloric to the CS network also occurs when the CS network is spontaneously active. 4. Our results thus demonstrate that sensory input can provoke a long-lasting modification of the functional configuration of a rhythmic neural network. They further extend the concept of flexibility in nervous systems by showing that individual neurons can belong to more than one neural network, "switching" from one to another in response to sensory input or spontaneous central nervous activity.

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 Phase maintenance in a rhythmic motor pattern during temperature changes in vivo

2014 ◽  
Vol 111 (12) ◽  
pp. 2603-2613 ◽  
Author(s):  
Wafa Soofi ◽  
Marie L. Goeritz ◽  
Tilman J. Kispersky ◽  
Astrid A. Prinz ◽  
Eve Marder ◽  
...  
Keyword(s):  
Motor Pattern ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Environmental Perturbations ◽  
Phase Maintenance ◽  
Pyloric Dilator ◽  
Similar Temperature ◽  
Intact Crab

Central-pattern-generating neural circuits function reliably throughout an animal's life, despite constant molecular turnover and environmental perturbations. Fluctuations in temperature pose a problem to the nervous systems of poikilotherms because their body temperature follows the ambient temperature, thus affecting the temperature-dependent dynamics of various subcellular components that constitute neuronal circuits. In the crustacean stomatogastric nervous system, the pyloric circuit produces a triphasic rhythm comprising the output of the pyloric dilator, lateral pyloric, and pyloric constrictor neurons. In vitro, the phase relationships of these neurons are maintained over a fourfold change in pyloric frequency as temperature increases from 7°C to 23°C. To determine whether these temperature effects are also found in intact crabs, in the presence of sensory feedback and neuromodulator-rich environments, we measured the temperature dependence of the pyloric frequency and phases in vivo by implanting extracellular electrodes into Cancer borealis and Cancer pagurus and shifting tank water temperature from 11°C to 26°C. Pyloric frequency in the intact crab increased significantly with temperature (Q10 = 2–2.5), while pyloric phases were generally conserved. For a subset of the C. borealis experiments, animals were subsequently dissected and the stomatogastric ganglion subjected to a similar temperature ramp in vitro. We found that the maximal frequency attained at high temperatures in vivo is lower than it is under in vitro conditions. Our results demonstrate that, over a wide temperature range, the phases of the pyloric rhythm in vivo are generally preserved, but that the frequency range is more restricted than it is in vitro.

scholarly journals A Neuronal Role For a Crustacean Red Pigment Concentrating Hormone-Like Peptide: Neuromodulation of the Pyloric Rhythm in the Crab, Cancer Borealis

1988 ◽  
Vol 135 (1) ◽  
pp. 165-181 ◽  
Author(s):  
MICHAEL P. NUSBAUM ◽  
EVE MARDER
Keyword(s):  
Nervous System ◽  
Physiological Data ◽  
Red Pigment ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Cycle Frequency ◽  
Pyloric Dilator ◽  
Whole Mount ◽  
Motor Neurones ◽  
Pyloric Rhythm

The distribution of red pigment concentrating hormone (RPCH)-like immunoreactivity (RPLI) in the stomatogastric nervous system of the crab, Cancer borealis, was studied using whole-mount immunocytochemistry. RPLI was seen in neuropilar processes in the stomatogastric ganglion (STG), and in somata in the oesophageal ganglion and commissural ganglia. Staining was blocked by preincubating the antiserum with RPCH, as well as with a number of adipokinetic hormones (AKHs) and related peptides. Synthetic RPCH had strong actions on the pyloric rhythm of the isolated STG. Bath applications of RPCH (10−9-10−6moll−1) increased the cycle frequency in preparations displaying slow pyloric rhythms, and initiated rhythmic pyloric activity in silent preparations. In the presence of tetrodotoxin (TTX), RPCH evoked rhythmic non-impulse-mediated alternations in membrane potential in the lateral pyloric and pyloric dilator motor neurones. The effects of RPCH were compared to those of a series of AKHs which resemble RPCH structurally. The immunocytochemical and physiological data together suggest that RPCH or a similar molecule is a neurally released modulator of the STG.

Dopamine Modulation of Calcium Currents in Pyloric Neurons of the Lobster Stomatogastric Ganglion

2003 ◽  
Vol 90 (2) ◽  
pp. 631-643 ◽  
Author(s):  
Bruce R. Johnson ◽  
Peter Kloppenburg ◽  
Ronald M. Harris-Warrick
Keyword(s):  
Calcium Channel ◽  
Transmitter Release ◽  
Stomatogastric Ganglion ◽  
Calcium Currents ◽  
Voltage Gated ◽  
Pyloric Network ◽  
Pyloric Dilator ◽  
Voltage Dependent ◽  
Inward Currents ◽  
Dopamine Modulation

We examined the dopamine (DA) modulation of calcium currents (ICa) that could contribute to the plasticity of the pyloric network in the lobster stomatogastric ganglion. Pyloric somata were voltage-clamped under conditions designed to block voltage-gated Na+, K+, and H currents. Depolarizing steps from –60 mV generated voltage-dependent, inward currents that appeared to originate in electrotonically distal, imperfectly clamped regions of the cell. These currents were blocked by Cd2+ and enhanced by Ba2+ but unaffected by Ni2+. Dopamine enhanced the peak ICa in the pyloric constrictor (PY), lateral pyloric (LP), and inferior cardiac (IC) neurons and reduced peak ICa in the ventricular dilator (VD), pyloric dilator (PD), and anterior burster (AB) neurons. All of these effects, except for the AB, are consistent with DA's excitation or inhibition of firing in the pyloric neurons. Enhancement of ICa in PY and LP neurons and reduction of ICa in VD and PD neurons are also consistent with DA-induced synaptic strength changes via modulation of presynaptic ICa. However, the reduction of ICa in AB suggests that DA's enhancement of AB transmitter release is not directly mediated through presynaptic ICa. ICa in PY and PD neurons was more sensitive to nifedipine block than in AB neurons. In addition, nifedipine blocked DA's effects on ICa in the PY and PD neurons but not in the AB neuron. Thus the contribution of specific calcium channel subtypes carrying the total ICa may vary between pyloric neuron classes, and DA may act on different calcium channel subtypes in the different pyloric neurons.

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