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.

scholarly journals Differential Modulation of Synaptic Strength and Timing Regulate Synaptic Efficacy in a Motor Network

2011 ◽  
Vol 105 (1) ◽  
pp. 293-304 ◽  
Author(s):  
Bruce R. Johnson ◽  
Jessica M. Brown ◽  
Mark D. Kvarta ◽  
Jay Y. J. Lu ◽  
Lauren R. Schneider ◽  
...  
Keyword(s):  
Synaptic Input ◽  
Synaptic Strength ◽  
Neuronal Firing ◽  
Cycle Period ◽  
Cycle Frequency ◽  
Pyloric Network ◽  
Motor Network ◽  
Pyloric Dilator ◽  
Network Output ◽  
Firing Properties

Neuromodulators modify network output by altering neuronal firing properties and synaptic strength at multiple sites; however, the functional importance of each site is often unclear. We determined the importance of monoamine modulation of a single synapse for regulation of network cycle frequency in the oscillatory pyloric network of the lobster. The pacemaker kernel of the pyloric network receives only one chemical synaptic feedback, an inhibitory synapse from the lateral pyloric (LP) neuron to the pyloric dilator (PD) neurons, which can limit cycle frequency. We measured the effects of dopamine (DA), octopamine (Oct), and serotonin (5HT) on the strength of the LP→PD synapse and the ability of the modified synapse to regulate pyloric cycle frequency. DA and Oct strengthened, whereas 5HT weakened, LP→PD inhibition. Surprisingly, the DA-strengthened LP→PD synapse lost its ability to slow the pyloric oscillations, whereas the 5HT-weakened LP→PD synapse gained a greater influence on the oscillations. These results are explained by monoamine modulation of factors that determine the firing phase of the LP neuron in each cycle. DA acts via multiple mechanisms to phase-advance the LP neuron into the pacemaker's refractory period, where the strengthened synapse has little effect. In contrast, 5HT phase-delays LP activity into a region of greater pacemaker sensitivity to LP synaptic input. Only Oct enhanced LP regulation of cycle period simply by enhancing LP→PD synaptic strength. These results show that modulation of the strength and timing of a synaptic input can differentially affect the synapse's efficacy in the network.

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 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.

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.

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.

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.

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.

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.

A mechanism for production of phase shifts in a pattern generator

1984 ◽  
Vol 51 (6) ◽  
pp. 1375-1393 ◽  
Author(s):  
J. S. Eisen ◽  
E. Marder
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Phase Relations ◽  
Significant Advance ◽  
Neuron Activity ◽  
Cycle Frequency ◽  
Bath Application ◽  
Pyloric Dilator ◽  
Wide Range ◽  
Post Synaptic Potential

During motor activity of the pyloric system of the lobster stomatogastric ganglion, there are rhythmic alternations between activity in the pyloric dilator (PD) and pyloric (PY) motor neurons. We studied the phase relations between PD motor neuron activity and PY motor neuron activity in preparations cycling at a wide range of frequencies and after altering the activity of the PD neurons. The PY neurons fall into two classes, early (PE) and late (PL) (21), distinguished by the different phases in the pyloric cycle at which they fire. The phase at which PE neurons fired and the phase at which PL neurons fired was independent of pyloric cycle frequency over a range of frequencies from 0.5 to 2.25 Hz. The anterior burster (AB) interneuron is electrically coupled to the PD motor neurons. Together the AB and PD neurons form the pacemaker for the pyloric system. Synchronous depolarization of the AB and PD neurons evokes a complex inhibitory post-synaptic potential (IPSP) in PY neurons. This IPSP has two components: an early, AB neuron-derived component and a late, PD neuron-derived component. Deletion of the PD neurons from the pyloric circuit by photoinactivation removed the PD-evoked component of the pacemaker-evoked IPSP. This resulted in a decrease in the duration of the IPSP evoked by pacemaker depolarization and a significant advance in the firing phase of PY neurons. Bath application of dopamine was used to hyperpolarize and inhibit the PD neurons (30), causing them to release less neurotransmitter. As a consequence, the duration of the IPSP evoked by pacemaker depolarization was decreased and the firing phase of the PY neurons was significantly advanced. Stimulation of the inferior ventricular nerve (IVN) produces a slow excitation of the PD neurons (30), causing them to release more neurotransmitter. Consequently, the duration of the IPSP evoked by pacemaker depolarization was increased and the firing phase of the PY neurons was significantly retarded for several cycles of pyloric activity following IVN stimulation. Thus, modulation of the strength of PD-evoked inhibition in PY neurons is responsible for altering the firing phase of the PY neurons with respect to the pyloric pacemaker. We suggest that frequency of the pyloric output and the phase relations of the elements within the pyloric cycle can be regulated independently. The potential implications of these data for modulation of synaptic efficacy in other preparations are discussed.

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