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

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.

1983 ◽  
Vol 105 (1) ◽  
pp. 59-82
Author(s):  
P. S. Dickinson ◽  
F. Nagy

In the isolated stomatogastric nervous system of the lobster Fasus lalandii, the strong modifications of the pyloric motor pattern induced by firing of the single anterior pyloric modulator neurone (APM) are due primarily to modulation by APM activity of the regenerative membrane properties which are responsible for the ‘burstiness’ of all the pyloric neurones and particularly of the non-pacemaker neurones (constrictor motoneurones). This modulation has been studied under experimental conditions where the main extrinsic influences usually received by the pyloric constrictor neurones (intra-network synaptic interactions, activity of pacemaker neurones, and phasic central inputs from two premotor centres) are minimal. Under these conditions a brief discharge of neurone APM induces long plateaus of firing in all of the pyloric neurones. The non-pacemaker neurones of the pyloric network are not simply passive follower neurones, but can produce regenerative depolarizations (plateau potentials) during which the neurones fire spikes. The ability of the pyloric constrictor neurones to produce plateau potentials (plateau properties) contributes greatly to the generation of the rhythmical pyloric motor pattern. When these neurones spontaneously express their plateau properties, firing of neurone APM amplifies these properties. When most of the central inputs usually received by the pyloric constrictor neurones are experimentally suppressed, these neurones can no longer produce plateau potentials. In such conditions, firing of the single modulatory neurone APM can reinduce plateau properties of the pyloric constrictor neurones. In addition, firing in APM neurone slows down the active repolarization phase which terminates the plateau potentials of pyloric constrictor neurones. This effect is long-lasting and voltage-dependent. Modulation by APM of the plateau properties of the pyloric neurones also changes the sensitivity of these neurones to synaptic inputs. This effect can explain the strong modifications that an APM discharge exerts on a current pyloric motor pattern. Moreover, it might render the motoneurones of the pyloric pattern generator more sensitive to inputs from a command oscillator, and contribute to switching on the pyloric motor pattern.


2001 ◽  
Vol 86 (4) ◽  
pp. 1816-1825 ◽  
Author(s):  
Takeshi Otsuka ◽  
Fujio Murakami ◽  
Wen-Jie Song

The subthalamic nucleus (STN) directly innervates the output structures of the basal ganglia, playing a key role in basal ganglia function. It is therefore important to understand the regulatory mechanisms for the activity of STN neurons. In the present study, we aimed to investigate how the intrinsic membrane properties of STN neurons interact with their synaptic inputs, focusing on their generation and the properties of the long-lasting, plateau potential. Whole cell recordings were obtained from STN neurons in slices prepared from postnatal day 14 (P14) to P20 rats. We found that activation of glutamate receptor-mediated excitatory synaptic potentials (EPSPs) evoked a plateau potential in a subpopulation of STN neurons ( n = 13/22), in a voltage-dependent manner. Plateau potentials could be induced only when the cell was hyperpolarized to more negative than about −75 mV. Plateau potentials, evoked with a depolarizing current pulse, again only from a hyperpolarized state, were observed in about half of STN neurons tested ( n = 162/327). Only in neurons in which a plateau potential could be evoked by current injection did EPSPs evoke plateau potentials. L-type Ca2+ channels, Ca2+-dependent K+ channels, and TEA-sensitive K+ channels were found to be involved in the generation of the potential. The stability of the plateau potential, tested by the injection of a negative pulse current during the plateau phase, was found to be robust at the early phase of the potential, but decreased toward the end. As a result the early part of the plateau potential was resistant to membrane potential perturbations and would be able to support a train of action potentials. We conclude that excitatory postsynaptic potentials, evoked in a subpopulation of STN neurons at a hyperpolarized state, activate L-type Ca2+ and other channels, leading to the generation of a plateau potential. Thus about half of STN neurons can transform short-lasting synaptic excitation into a long train of output spikes by voltage-dependent generation of a plateau potential.


1997 ◽  
Vol 78 (5) ◽  
pp. 2483-2492 ◽  
Author(s):  
Jens C. Rekling ◽  
Jack L. Feldman

Rekling, Jens C. and Jack L. Feldman. Calcium-dependent plateau potentials in rostral ambiguus neurons in the newborn mouse brain stem in vitro. J. Neurophysiol. 78: 2483–2492, 1997. The nucleus ambiguus contains vagal and glossopharyngeal motoneurons and preganglionic neurons involved in respiration, swallowing, vocalization, and control of heart beat. Here we show that the rostral compact formation's ambiguus neurons, which control the esophageal phase of swallowing, display calcium-dependent plateau potentials in response to tetanic orthodromic stimulation or current injection. Whole cell recordings were made from visualized neurons in the rostral nucleus ambiguus using a slice preparation from the newborn mouse. Biocytin-labeling revealed dendritic trees with pronounced rostrocaudal orientations confined to the nucleus ambiguus, a morphological profile matching that of vagal motoneurons projecting to the esophagus. Single-stimulus orthodromic activation, using an electrode placed in the dorsomedial slice near the nucleus tractus solitarius, evoked single excitatory postsynaptic potentials (EPSPs) or short trains of EPSPs (500 ms to 1 s). However, tetanic stimulation (5 pulses, 10 Hz) induced voltage-dependent afterdepolarizations or long-lasting plateau potentials (>1 min) with a constant firing pattern. Depolarizing or hyperpolarizing current pulses elicited voltage-dependent afterdepolarizations or plateau potentials lasting a few seconds to several minutes. Constant spike activity accompanied the long-lasting plateau potentials, which ended spontaneously or could be terminated by weak hyperpolarizing current pulses. Current-induced afterdepolarizations and plateau potentials were dependent on extracellularand intracellular Ca2+, as they were blocked completely by extracellular Co2+, Cd2+, or intracellular bis-( o-aminophenoxy)- N,N,N′,N′-tetraacetic acid (BAPTA). Orthodromically induced afterdepolarizations and plateau potentials were blocked by intracellular BAPTA. Afterdepolarizations and plateau potentials were completely blocked by substitution of extracellular Na+ with choline. Afterdepolarizations persisted in tetrodotoxin. We conclude that rostral ambiguus neurons have a Ca2+-activated inward current carried by Na+. Synaptic activation of this conductance may generate prolonged spike activity in these neurons during the esophageal phase of swallowing.


1996 ◽  
Vol 76 (3) ◽  
pp. 1491-1502 ◽  
Author(s):  
J. D. Angstadt ◽  
J. J. Choo

1. Individual leech Retzius (Rz) cells were removed from mid-body ganglia and plated in cell culture on concanavalin A or polylysine. Experiments on the majority of cells were performed after 6-11 days in culture. Isolated Rz cells were superfused with normal leech saline (NS), cobalt saline (Ca2+ replaced with Co2+), or one of a variety of other modified salines. 2. Prolonged plateau potentials (PPs) with durations ranging from several seconds to nearly 2 min were evoked in isolated Rz cells in response to 1-s depolarizing current pulses delivered under discontinuous current clamp. Some PPs terminated spontaneously while others were terminated with hyperpolarizing current pulses. PPs were associated with a dramatic increase in the input conductance of the neuron. The PP decayed slightly over time, and this decay was accompanied by a small decrease in the input conductance. 3. PP duration was enhanced by penetrating cells with electrodes containing tetraethylammonium (TEA) and by bathing cells in Co2+ saline, but PPs were evoked also in NS and using electrodes without TEA. The effects of TEA and Co2+ saline suggest that voltage-dependent and especially calcium-dependent outward currents normally suppress plateau formation. 4. PPs occurred most reliably in neurons with extensive neurite sprouting. Isolated somata with few or no neurites usually failed to express PP, although there were several exceptions to this trend. 5. PPs persisted when Ca2+ was replaced with either of the calcium channel blockers Co2+, Ni2+, or Mn2+, when 200 microM Cd2+ was added to normal saline, or when Na+ was replaced with Li+. In contrast, PPs were eliminated rapidly when Na+ was replaced with N-methyl-D-glucamine. 6. Isolated Rz cells also expressed repetitive PPs either spontaneously or in response to injection of sustained depolarizing current. Spontaneous repetitive PPs were suppressed by hyperpolarizing current. Repetitive PPs in isolated Rz cells are similar in many respects to the bursting electrical activity induced by Co2+ saline in Rz and other neurons in intact ganglia. 7. The ionic dependence and prolonged duration of PPs suggest that these responses are generated by a persistent voltage-dependent Na+ current. A quantitative computer simulation of PPs was achieved using a depolarization-activated Na+ conductance with very slow inactivation. Repetitive PPs were simulated by addition of a slow outward current in the form of an electrogenic pump.


1998 ◽  
Vol 79 (4) ◽  
pp. 2063-2069 ◽  
Author(s):  
Amir Ayali ◽  
Bruce R. Johnson ◽  
Ronald M. Harris-Warrick

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.


1996 ◽  
Vol 76 (6) ◽  
pp. 3597-3608 ◽  
Author(s):  
F. Tennigkeit ◽  
D. W. Schwarz ◽  
E. Puil

1. During alertness, lemniscal thalamocortical neurons in the ventral medial geniculate body (MGBv) encode sound signals by firing action potentials in a tonic mode. When they are in a burst firing mode, characteristic of thalamic neurons during some sleep states, the same stimuli may have an alerting function, leading to conscious perception of sound. We investigated the intrinsic membrane properties of MGBv neurons in search of mechanisms that enable them to convert from burst to tonic firing modes, allowing accurate signal coding of sensory stimuli. 2. We studied thalamocortical relay neurons and identified neurons morphologically with injected N-(2-aminoethyl) biotinamide hydrochloride in in vitro slice preparations of young rats. With the use of the whole cell recording method, we examined the contributions of distinct conductances to voltage responses evoked by current pulses. The neurons (n = 74) displayed a narrow range of resting potentials (-68 +/- 4 mV, mean +/- SD) and an average input resistance of 226 +/- 100 M omega. The membrane time constant was 40 +/- 17.6 ms and the action potential threshold was -51.6 +/- 3 mV. 3. Injections of hyperpolarizing current pulses from rest revealed an inward rectification produced by two voltage-dependent components. A fast component, sensitive to blockade with Ba2+ (100–200 microM), was attributed to an inward rectifier, IIR. Such applications also increased input resistance and depolarized neurons, consistent with a blockade of various K+ conductances. Application of Ba2+ often unmasked another voltage-dependent rectification with a slower time course. The second component was sensitive to blockade with Cs+ (1.5 mM), reminiscent of a hyperpolarization-activated current, IH. 4. Depolarizing pulses from rest produced ramp-shaped voltage responses that led to delayed tonic firing. Blockade of Na+ conductances by tetrodotoxin (TTX, 300–600 nM), or extracellular replacement of Ca2+ with Mg2+ (with TTX present), reduced the slope of the ramp and the overall depolarizing response. Application of 4-aminopyridine (4-AP, 100 microM), a blocker of A-type K+ conductances, increased input resistance and the overall depolarizing response. The voltage ramp therefore represents a complex rectification due to voltage-dependent contributions of persistent Na-, Ca2+, and K+ conductances. 5. Depolarizing pulses from potentials of less than -75 mV evoked phasic burst responses, consisting of one to seven action potentials riding on a low-threshold spike (LTS). The LTS was absent in low extracellular Ca2+ conditions and was blocked by application of Ni2+ (0.6 mM), but not by Cd2+ (50 microM). Similar depolarization from less than -80 mV evoked several action potentials, often followed by a TTX-resistant high-threshold spike (HTS) of longer duration. Firing of HTSs always occurred during 4-AP (100 microM) application, inferring that, normally, A-type K+ conductances may control ability to fire an HTS. As in the LTS, a Ca2+ current is a major participant in the HTS because extracellular replacement of Ca2+ with Mg2+ or application of Cd2+ (50 microM) blocked its genesis. After TTX blockade of Na+ conductances, “tonic firing” of HTSs occurred during depolarization above -45 mV. 6. During tonic firing evoked by current pulses, the second and subsequent spikes were longer in duration than the initial action potentials. Low extracellular concentrations of Ca2+ or Cd2+ (50 microM) application reduced the durations of the nonprimary spikes, inferring a contribution of high-threshold voltage-dependent Ca2+ conductances to their repolarizing phase. Also, K+ conductances may contribute to spike repolarization, because 4-AP (100 microM) or tetraethylammonium (2 mM) application led to prolonged action potentials and the generation of plateau potentials. A fast afterhyperpolarization, likely mediated by a Ca(2+)-dependent K+ conductance, limited the tonic firing. Such conductances, therefore, may regulate the re


2002 ◽  
Vol 88 (6) ◽  
pp. 2942-2953 ◽  
Author(s):  
Muriel Thoby-Brisson ◽  
John Simmers

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.


1997 ◽  
Vol 78 (6) ◽  
pp. 3210-3221 ◽  
Author(s):  
Bruce R. Johnson ◽  
Ronald M. Harris-Warrick

Johnson, Bruce R. and Ronald M. Harris-Warrick. Amine modulation of glutamate responses from pyloric motor neurons in lobster stomatogastric ganglion. J. Neurophysiol. 78: 3210–3221, 1997. The amines dopamine (DA), serotonin (5-HT), and octopamine (Oct) each elicit a distinctive motor pattern from a quiescent pyloric network in the lobster stomatogastric ganglion (STG). We previously have demonstrated that these amines alter the synaptic strength at multiple, distributed sites within the pyloric network that could contribute to the amine-induced motor patterns. Here, we examined the postsynaptic contribution to these changes in synaptic strength by determining how the amines modify responses of pyloric motor neurons to glutamate (Glu), one of the network transmitters, applied iontophoretically into the STG neuropil. Dopamine reduced the Glu responses of the pyloric dilator (PD), ventricular dilator (VD), and inferior cardiac (IC) neurons and enhanced the Glu responses of the lateral pyloric (LP) and pyloric constrictor (PY) neurons. The only effect of 5-HT was to reduce the Glu response of the VD neuron. Oct enhanced the Glu responses of the LP and PY neurons but did not affect the PD, VD, and IC responses. We also examined amine effects on the depolarizing responses to iontophoresed acetylcholine (ACh) in the PD and VD and found that they paralleled the amine effects on Glu responses in these neurons. This suggests that amine modulation of PD and VD responses to Glu and ACh may be explained by general changes in the ionic conductance of these neurons. We compare our results with our earlier work describing amine effects on synaptic strength and input resistance to show that amines act at both pre- and postsynaptic sites to modify graded synaptic transmission in the pyloric network.


1986 ◽  
Vol 55 (5) ◽  
pp. 866-881 ◽  
Author(s):  
R. E. Flamm ◽  
R. M. Harris-Warrick

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.


1986 ◽  
Vol 55 (5) ◽  
pp. 847-865 ◽  
Author(s):  
R. E. Flamm ◽  
R. M. Harris-Warrick

We investigated the effects of dopamine, octopamine, and serotonin on the motor output of the pyloric circuit in the stomatogastric ganglion of the lobster, Panulirus interruptus. Amines were bath applied at concentrations from 10(-8) to 10(-4) M, and the responses of the six classes of pyloric neurons were monitored both intracellularly and extracellularly. Each amine modified the pyloric motor pattern in a specific way. In addition, dopamine and octopamine were each able to produce different motor patterns at different concentrations. Amine effects on pyloric neurons included initiation and enhancement or inhibition of spike activity, changes in the phase relationships of neurons, and changes in the cycle frequency of the pyloric rhythm. These results show that the motor pattern produced by this well-studied central pattern generator circuit is highly plastic and can be modulated by endogenous biogenic amines.


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