Long-Term Neuromodulatory Regulation of a Motor Pattern–Generating Network: Maintenance of Synaptic Efficacy and Oscillatory Properties

2002 ◽  
Vol 88 (6) ◽  
pp. 2942-2953 ◽  
Author(s):  
Muriel Thoby-Brisson ◽  
John Simmers
Keyword(s):  
Spiny Lobster ◽  
Motor Pattern ◽  
Ionic Currents ◽  
Cell Types ◽  
Delayed Rectifier ◽  
Potential Oscillations ◽  
Calcium Dependent ◽  
Pyloric Network ◽  
Network Maintenance

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.

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.

Slow active potentials and bursting motor patterns in pyloric network of the lobster, Panulirus interruptus

1982 ◽  
Vol 48 (4) ◽  
pp. 914-937 ◽  
Author(s):  
D. F. Russell ◽  
D. K. Hartline
Keyword(s):  
Motor Pattern ◽  
Membrane Properties ◽  
Plateau Potentials ◽  
Motor Patterns ◽  
Potential Oscillations ◽  
Panulirus Interruptus ◽  
Pyloric Network ◽  
Current Pulses ◽  
Voltage Dependent ◽  
High Level

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.

Long-Term Expression of Two Interacting Motor Pattern-Generating Networks in the Stomatogastric System of Freely Behaving Lobster

1998 ◽  
Vol 79 (3) ◽  
pp. 1396-1408 ◽  
Author(s):  
Stefan Clemens ◽  
Denis Combes ◽  
Pierre Meyrand ◽  
John Simmers
Keyword(s):  
Motor Neurons ◽  
Motor Pattern ◽  
Burst Duration ◽  
Cycle Period ◽  
Gastric Mill ◽  
Pyloric Network ◽  
Freely Behaving ◽  
Stomatogastric System

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.

Firing Properties of GABAergic Versus Non-GABAergic Vestibular Nucleus Neurons Conferred by a Differential Balance of Potassium Currents

2007 ◽  
Vol 97 (6) ◽  
pp. 3986-3996 ◽  
Author(s):  
Aryn H. Gittis ◽  
Sascha du Lac
Keyword(s):  
Vestibular Nucleus ◽  
Brain Slices ◽  
Ionic Currents ◽  
Vestibular Nuclei ◽  
Cell Types ◽  
Delayed Rectifier ◽  
Charge Densities ◽  
Outward Currents ◽  
Firing Properties ◽  
Kinetics Of

Neural circuits are composed of diverse cell types, the firing properties of which reflect their intrinsic ionic currents. GABAergic and non-GABAergic neurons in the medial vestibular nuclei, identified in GIN and YFP-16 lines of transgenic mice, respectively, exhibit different firing properties in brain slices. The intrinsic ionic currents of these cell types were investigated in acutely dissociated neurons from 3- to 4-wk-old mice, where differences in spontaneous firing and action potential parameters observed in slice preparations are preserved. Both GIN and YFP-16 neurons express a combination of four major outward currents: Ca2+-dependent K+ currents ( IKCa), 1 mM TEA-sensitive delayed rectifier K+ currents ( I1TEA), 10 mM TEA-sensitive delayed rectifier K+ currents ( I10TEA), and A-type K+ currents ( IA). The balance of these currents varied across cells, with GIN neurons tending to express proportionately more IKCa and IA, and YFP-16 neurons tending to express proportionately more I1TEA and I10TEA. Correlations in charge densities suggested that several currents were coregulated. Variations in the kinetics and density of I1TEA could account for differences in repolarization rates observed both within and between cell types. These data indicate that diversity in the firing properties of GABAergic and non-GABAergic vestibular nucleus neurons arises from graded differences in the balance and kinetics of ionic currents.

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.

scholarly journals Cell Specific Dopamine Modulation of the Transient Potassium Current in the Pyloric Network by the Canonical D1 Receptor Signal Transduction Cascade

2010 ◽  
Vol 104 (2) ◽  
pp. 873-884 ◽  
Author(s):  
Hongmei Zhang ◽  
Edmund W. Rodgers ◽  
Wulf-Dieter C. Krenz ◽  
Merry C. Clark ◽  
Deborah J. Baro
Keyword(s):  
Potassium Current ◽  
Expression System ◽  
Expression Patterns ◽  
Motor Pattern ◽  
Cell Types ◽  
Receptor Expression ◽  
Intracellular Camp ◽  
Cell Type ◽  
Pyloric Network ◽  
Cell Type Specific

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.

Transmural action potential and ionic current remodeling in ventricles of failing canine hearts

2002 ◽  
Vol 283 (3) ◽  
pp. H1031-H1041 ◽  
Author(s):  
Gui-Rong Li ◽  
Chu-Pak Lau ◽  
Anique Ducharme ◽  
Jean-Claude Tardif ◽  
Stanley Nattel
Keyword(s):  
Left Ventricle ◽  
Action Potential ◽  
Action Potentials ◽  
Slow Component ◽  
Ionic Current ◽  
Ionic Currents ◽  
Cell Types ◽  
Delayed Rectifier ◽  
Cardiac Repolarization ◽  
Early Afterdepolarizations

Heart failure (HF) produces important alterations in currents underlying cardiac repolarization, but the transmural distribution of such changes is unknown. We therefore recorded action potentials and ionic currents in cells isolated from the endocardium, midmyocardium, and epicardium of the left ventricle from dogs with and without tachypacing-induced HF. HF greatly increased action potential duration (APD) but attenuated APD heterogeneity in the three regions. Early afterdepolarizations (EADs) were observed in all cell types of failing hearts but not in controls. Inward rectifier K+ current ( I K1) was homogeneously reduced by ∼41% (at −60 mV) in the three cell types. Transient outward K+ current ( I to1) was decreased by 43–45% at +30 mV, and the slow component of the delayed rectifier K+ current ( I Ks) was significantly downregulated by 57%, 49%, and 58%, respectively, in epicardial, midmyocardial, and endocardial cells, whereas the rapid component of the delayed rectifier K+ current was not altered. The results indicate that HF remodels electrophysiology in all layers of the left ventricle, and the downregulation of I K1, I to1, and I Ks increases APD and favors occurrence of EADs.

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.

Ionic Currents Underlying Difference in Light Response Between Type A and Type B Photoreceptors

2006 ◽  
Vol 95 (5) ◽  
pp. 3060-3072 ◽  
Author(s):  
K. T. Blackwell
Keyword(s):  
Sodium Current ◽  
Light Response ◽  
Type A ◽  
Ionic Currents ◽  
Firing Frequency ◽  
Delayed Rectifier ◽  
Type B ◽  
Calcium Dependent ◽  
Fast Sodium Current

In Hermissenda crassicornis, the memory of light associated with turbulence is stored as changes in intrinsic and synaptic currents in both type A and type B photoreceptors. These photoreceptor types exhibit qualitatively different responses to light and current injection, and these differences shape the spatiotemporal firing patterns that control behavior. Thus the objective of the study was to identify the mechanisms underlying these differences. The approach was to develop a type B model that reproduced characteristics of type B photoreceptors recorded in vitro, and then to create a type A model by modifying a select number of ionic currents. Comparison of type A models with characteristics of type A photoreceptors recorded in vitro revealed that type A and type B photoreceptors have five main differences, three that have been characterized experimentally and two that constitute hypotheses to be tested with experiments in the future. The three differences between type A and type B photoreceptors previously characterized include the inward rectifier current, the fast sodium current, and conductance of calcium-dependent and transient potassium channels. Two additional changes were required to produce a type A photoreceptor model. The very fast firing frequency observed during the first second after light onset required a faster time constant of activation of the delayed rectifier. The fast spike adaptation required a fast, noninactivating calcium-dependent potassium current. Because these differences between type A and type B photoreceptors have not been confirmed in comparative experiments, they constitute hypotheses to be tested with future experiments.

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.

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