Endogenous Bursting Research Articles

A multiaction synapse evoking both EPSPs and enhancement of endogenous bursting

Selective stimulation of two identified input neurons called the ‘IV neurons’ has a dual influence on the endogenous bursting activity of certain ‘PD’ motorneurons in the stomatogastric ganglion of the spiny lobster. The effects include: (i) large, conventional and apparently monosynaptic EPSPs; and (ii) enhancement of the endogenous bursting of the pyloric dilator (PD) cells, seen as an increased implitude of PD oscillations and a higher spiking rate during burst. The burst enhancement decayed relatively slowly after stimulation ceased, over seconds or tens-of-seconds, depending on stimulus parameters. Modification of the voltage-dependent membrane properties of the PD cells appeared to underlie this effect. The dual-action nature of the IV-to-PD connection was confirmed by selectively blocking the brief EPSP component with 5 × 10 −4 M curare, uncer which conditions the burst enhancement still persisted. Data from low-Ca 2+ experiments were consistent with a conventional mode of synaptic transmitter release underlying the burst enhancement. Enhancement was found to differ significantly from actions of injected current. The IV inputs appear to act on at least two types of synaptic receptors on PD neurons: a curare-sensitive receptor for the brief conventional EPSP, and a curare-resistant receptor for burst enchancement. Analogies may be drawn to the nicotinic and muscarinic cholinergic receptors of vertebrates. These findings may be considered within the contexts of multiaction synapses, modification of cellular properties, and mechanisms for the CNS activation of motor pattern generators.

Development of intrinsic burst generation in identified neuron R 15 of Aplysia

The development of endogenous bursting pattern of identified neuron R 15 of Aplysia was studied, in animals ranging from juvenils weighing 27 mg to adult animals weighing 350 g. In the youngest animals studied, R 15 only fires irregularly, somewhat later it begins firing in brief bursts, and only in early adulthood does it acquire its characteristic burst firing pattern.

Cyclic Adenosine Monophosphate Mediation of Peptide Neurohormone Effects on the Lobster Cardiac Ganglion

ABSTRACT Two cardioexcitors which can be extracted or released from crustacean neurohaemal structures, the pericardial organs, alter the endogenous bursting activity of isolated lobster cardiac ganglia in different ways. A small peptide increases the burst frequency of the ganglion, the duration of each burst, and the number of spikes per burst, while 5-hydroxytryptamine (5-HT) increases burst frequency, but decreases the burst duration and number of spikes per burst. Four lines of evidence are presented that cyclic adenosine monophosphate (cAMP) mediates the effects of peptide on the ganglion, but does not play a significant role in 5-HT action: (1) exogenous cAMP mimics the effects of peptide but not of 5-HT on burst parameters; (2) inhibition of the enzyme phosphodiesterase, which increases endogenous levels of cAMP, mimics the effects of peptide and potentiates peptide action but not that of 5-HT; (3) putative blockers of adenylate cyclase block the action of peptide but not of 5-HT; (4) peptide causes a large increase in cAMP content of the ganglion, while 5-HT application results in a much smaller increase.

Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. I. Pyloric system

1. Four factors contribute to pattern generation in the pyloric network of the lobster stomatogastric ganglion. These are: a) endogenously oscillating neurons; b) synaptic network properties; c) nonlinear cellular properties, including the generation of plateau potentials; and d) excitatory input from the commissural ganglia. The roles and relative importance of these factors were investigated with a new technique for inactivating single specific identified neurons. 2. In stomatogastric ganglia in which the excitatory input is left intact, a) pattern generation continues when any cell or pair of cells other than the endogenous bursters are inactivated, b) pattern generation also continues when the endogenous bursters are inactivated, c) pattern generation ceases when the endogenous bursters plus one other particular cell are inactivated. This cell, although not an endogenous burster, displays a strong tendency to generate plateau potentials. 3. In stomatogastric ganglia that have been isolated from excitatory input, a) pattern generation continues when any cell or pair of cells other than the endogenous bursters are inactivated, b) pattern generation ceases when the endogenous bursters are inactivated. 4. Some of the inputs to the stomatogastric ganglion normally fire in bursts. However, their potentiation and acceleration of the output pattern are also produced by tonic stimulation of the nerve. The effect of one of those inputs is mimicked by bath application of dopamine to the stomatogastric ganglion. 5. The roles and importance of the three most important factors were qualitatively summarized in a chart specifying the activity of the network as a function of its intactness.

Serotonin-induced hyperpolarization of an indentified Aplysia neuron is mediated by cyclic AMP.

Addition of serotonin to the medium bathing an Aplysia abdominal ganglion causes a change in the endogenous bursting activity of the identified neuron R15. At serotonin concentrations in the micromolar range, the predominant effect is an increase in depth and duration of the interburst hyperpolarization and consequent decrease in burst rate. At higher concentrations (10 microM) serototin can inhibit bursting completely. We have shown previously that these changes can be mimicked by bath application or intracellular injection of several cyclic AMP analogs substituted at the 8 position. Voltage clamp analysis indicates that serotonin and cyclic AMP analogs both cause an increase in membrane slope conductance in R15, with reversal potentials for the responses between -75 and -80 mV, close to the K+ equilibrium potential. When the K+ concentration in the bathing medium is changed, the reversal potentials change in a manner suggesting that serotonin and cyclic AMP analogs on K+ conductance are not additive. Furthermore, the effects of low concentrations of serotonin can be potentiated by the phosphodiesterase inhibitor Ro 20-1724. A pharmacological analysis indicates that the serotonin receptor that mediates hyperpolarization in R15 is similar to the serotonin receptor that we have shown to be coupled to adenylate cyclase. The present electrophysiological and pharmacological observations, together with our previous biochemical and pharmacological results, demonstrate that the serotonin-induced hyperpolarization of neuron R15 is mediated by cyclic AMP.

Burst generation in coordinating interneurons of the ventilatory system of the locust

1. Intracellular recordings were made from the processes of the interneurons coordinating ventilatory pumping movements in two species of locust,Schistocerca gregaria andLocusta migratoria. These neurons have their cell body in the metathoracic ganglion and their axon extends to the last abdominal ganglion via the contralateral abdominal connective. The structure of these interneurons within the metathoracic ganglion was determined by intracellular staining with cobalt followed by Timm's intensification, or by the injection of the fluorescent dye Lucifer Yellow. 2. During expiration the coordinating interneurons receive a large excitatory synaptic input causing them to discharge in an accelerating burst. Within the interburst interval no inhibitory postsynaptic potentials were observed, and excitatory postsynaptic potentials occurred only occasionally. 3. A number of tests failed to demonstrate that the coordinating interneurons were endogenous bursters, or that there was any coupling between different coordinating interneurons. Thus, bursts in these interneurons appear to be produced entirely by periods of intense excitatory synaptic input from as yet unidentified interneurons. 4. The rate of ventilation could be increased by a factor of two by the intracellular injection of constant depolarizing current into a coordinating interneuron. Although this result indicates that the coordinating interneurons are elements within the ventilatory rhythm generating system, it is probable that they are normally involved in generating the rhythm only when the demand for oxygen is high.

Investigation of burst generation by the electrically coupled cyberchron network in the snail Helisoma using a single-electrode voltage clamp.

This paper describes the results of investigating burst generation by the cyberchron network in the snail Helisoma. The cyberchron network is composed of aproximately 20 electrically coupled neurons and controls the feeding behavior of the snail. The electrical coupling between network members has made it particularly difficult to distinguish between the importance and involvement of single-cell and network properties in burst generation by this system. The present investigations utilized the new single-electrode voltage clamp to examine the membrane properties and network interactions of the cyberchron neurons: (1) A slow outward current is activated by moderately large depolarizing commands (-40 to 0 mV) and does not undergo inactivation decay (i.e., decline in magnitude) during a command potential step maintained for 10 sec or more. The lack of inactivation of the outward current in cyberchron neurons appears to be due to the dominating role of a Ca-dependent K current. (2) There are two functionally distinct classes of cyberchrons--current generator cyberchrons and follower cyberchrons. (3) Primary current generator cyberchrons have membrane properties similar to endogenous bursting neurons (e.g., persistent inward Ca current and negative resistance region in I-V plot) and appear to provide the main driving and timing current for the rest of the network. (4) The vast majority of cyberchrons are secondary current generator cyberchrons with membrane properties which exhibit inward-going rectification and appear to burst as a result of regenerative excitation with one another and the primary current generator cyberchrons. (5) The second class of cyberchrons are driven by the electrical synaptic input from the current generator cyberchrons, do not exhibit inward-going rectification, and are called follower cyberchrons. (6) Burst termination is due to activation of a slow outward tail current in most cyberchrons during the burst (probably Ca-activated K current) which causes a hyperpolarization in individual cyberchrons, terminating the burst. (7) Decay of the outward tail current causes the cyberchrons to depolarize, which activates the persistent inward Ca current in the primary current generator cyberchrons, starting the burst cycle anew.

On the endogenous bursting properties of 'light yellow' neurosecretory cells in the freshwater snail Lymnaea stagnalis (L.).

Intracellular microelectrodes were used to study a cluster of neurosecretory 'Light Yellow' Cells (LYC) in the central nervous system of Lymnaea stagnalis. LYC usually have a spontaneous firing pattern of bursts, lasting 10--600 s, alternating with periods of silence. Experiments on isolated single cells showed that the bursting activity has an endogenous origin. Each action potential is followed by a depolarizing afterpotential (DAP), with an amplitude of about 10 mV, lasting several seconds. Bursts end with a subthreshold DAP. It is concluded that two pace-maker mechanisms are responsible for the bursting pr-perties, one initiating and the other (the DAP) maintaining the burst. The relationship between the electrical and the neurosecretory properties of the cells is discussed.

Modulation of electrical activity and cyclic nucleotide metabolism in molluscan nervous system by a peptide-containing nervous system extract

A peptide-containing extract (PE) from Helix nervous system modifies the endogenous bursting pattern of electrical activity in Helix neurone F-1. This effect is similar to that induced in neuron F-1 by certain phosphodiesterase inhibitors and cAMP derivatives. The PE, and the vertebrate peptide hormones vasopressin and oxytocin, also cause an accumulation of cAMP in Helix ganglia in vitro. The factor in the PE which causes the cAMP accumulation is destroyed by Pronase, is lost on dialysis, and is stable to boiling. In all these respects it is identical to the factor which causes the change in neuronal electrical activity. The PE also stimulates adenylate cyclase activity in a crude membrane fraction prepared from Helix ganglion homogenates. This stimulation is abolished by prior dialysis of the PE, or pretreatment of the PE with pepsin, but is not affected by boiling of the PE. Pepsin-treated PE has no effect on electrical activity in neuron F-1. The adenylate cyclase-stimulating activity of the PE, like the factor which modifies neurone F-1 electrical activity, elutes in the void volume of a Sephadex G-10 column. The included volume of this column contains a factor which inhibits PE modification of neuronal electrical activity, and also inhibits both basal and PE-stimulated adenylate cyclase activity. The data are consistent with the possibility that cAMP mediates the effects of the PE on electrical activity in molluscan neurones.

Circadian Rhythm of Output from Neurones in the Eye of Aplysia

ABSTRACT The compound action potential (CAP) output from the isolated eye of Aplysia, in darkness at constant temperature, exhibits a circadian rhythm of CAP frequency and a circadian rhythm of CAP amplitude when recorded in culture medium for up to two weeks. Deuterated culture medium lengthened the period of the CAP frequency rhythm linearly from 26-7 h in normal culture medium to 33·7 h in 50% D2O culture medium. In 60 % D2O culture medium, the rhythm of CAP frequency was abolished after a single cycle. Lowering temperature had a direct inhibitory effect on the CAP generating mechanism, so that CAP production was virtually abolished below 7 °C. Lowering temperature decreased the amplitude and increased the period of the rhythm, and in eyes maintained at 9·5 °C the rhythm damped out after several cycles. Between 15 and 22·5 °C there was almost complete temperature compensation (Q10 1·07). It is suggested that the CAP generating cells of the eye may be similar in mechanism to central endogenous bursters in Aplysia and other gastropods, and that the circadian rhythm of CAP frequency and CAP burst frequency may be due to a clock-controlled change in frequency of a membrane potential oscillation in the electrotonically coupled secondary neurones.

Short-term modulation of endogenous bursting rhythms by monosynaptic inhibition in Aplysia neurons: Effects of contingent stimulation

A presynaptic neuron fires a high-frequency train of spikes that produces longlasting synaptic inhibition that modulates the bursting rhythm in a small population of endogenous bursting neurons in the left upper quadrant of the isolated abdominal ganglion of Aplysia. Single inputs decrease or increase the duration of the burst cycle as a function of the precise phase of the input (the phase response curve). Two phases of the burst cycle were used to analyze the effects of repeated contingent (phase-locked) stimulation. One contingency involved synaptic input early in the burst cycle that inhibited spikes and decreased the duration, whereas the other contingency involved input late in the cycle that increased the duration. Under both contingencies of stimulation, buildup and short-term persistence were found, however these cumulative effects were not dependent upon the phase of the burst cycle. The locus of the short-term plasticity that underlies the buildup and persistence in the pacemaker properties of the postsynaptic cell rather than in the synapse. The plastic change appears to involve a nonspecific postinhibitory rebound that follows a single input and builds up with repetition. These results support the suggestion that endogenous rhythms of pacemaker cells can undergo plastic changes and can therefore serve as a means of short-term information storage in the nervous system. However, this neuronal circuit does not have the specificity required to mediate operant conditioning.

Control systems model of the spontaneous and light-evoked patterns of the compound action potentials in the eye of Aplysia.

The spontaneous and light-evoked firing patterns of the compound action potentials (CAPs) in the isolated eye of Aplysia are experimentally observed from a control systems viewpoint. The eye, exhibiting an endogenous bursting activity and a marked circadian rhythm in darkness, is a self-excited system and responds to illumination with a controlled electrical activity. It is represented by the nonlinear systems model predicting the firing-rate variation of the CAPs. Construction of the model is based on the eye's biological model reported in the literature, and involves an experimental analysis of the system characteristics using linear approximation and conventional control systems techniques. The model is simulated and found to adequately conform to the observed behavior of the eye under various experimental conditions.

Simulation of network activity in stomatogastric ganglion of the spiny lobster, panulirus

We have compared experimental and model studies on the rhythmic activity of the lobster stomatogastric ganglion. Both the pyloric and gastric mill systems were simulated using a physiologically based network model. In the pyloric simulation the known synaptic connectivity of the 3 principal cell types in the pyloric rhythm was found to be sufficient to produce the correct sequence of cyclic bursting activity over a substantial range of parameter values, even though we did not simulate the known endogenous oscillatory driver potential of one of the cell types. It is not yet known whether the synaptic inhibition in the real system is in the right range to cause cyclic bursting in the absence of the driver potential, but the synaptic connectivity does appear to reinforce the cyclic pattern. Simulations were also done with alternative connectivity schemes to determine which synapses appear essential to generate the correct bursting sequence (in the absence of endogenous bursting activity). Other, more complex, systems simulated were: (1) all 5 cell groups of the pyloric system, and (2) the cells responsible for movement of the lateral teeth in the gastric mill. In both cases good qualitative agreement was achieved between model and real systems.

Endogenous bursting in Tritonia neurons at low temperature

Endogenous bursting in Tritonia neurons at low temperature

Structural and Functional Basis of Motor Pattern Generation in the Stomatogastric Ganglion of the Lobster

The stomatogastric ganglion of the lobster Panulirus interruptus contains about 30 neurons and controls the striated musculature of the stomach. The ganglion produces two complex rhythms, the pyloric cycle and the gastric mill cycle, when completely deafferented. This paper describes the neural circuitry underlying this activity in terms of interactions among motor neurons. The pyloric motor neurons are coordinated by electrotonic and inhibitory synaptic interactions which are driven by a group of three neurons having endogenous bursting capability. The gastric mill cycle does not appear to have any such driving source, and instead relies on the overall properties of the network to generate its burst patterns. Preliminary computer modeling indicates that alternate bursting between antagonists can occur without cyclically bursting driver cells. Computer reconstruction of Procion-filled stomatogastric neurons are used both to corroborate the results of the physiological studies and to quantify the geometry for purposes of modeling the intraneuronal flow of synaptic currents.