scholarly journals Roles for electrical coupling in neural circuits as revealed by selective neuronal deletions

1984 ◽  
Vol 112 (1) ◽  
pp. 147-167 ◽  
Author(s):  
E. Marder
Keyword(s):  
Neural Circuits ◽  
Neural Circuit ◽  
Lucifer Yellow ◽  
Electrical Coupling ◽  
Separate Analysis ◽  
Panulirus Interruptus ◽  
Pyloric Network ◽  
Synaptic Interactions ◽  
Pyloric Dilator ◽  
The Individual

Understanding fully the operation of a neural circuit requires both a description of the individual neurones within the circuit as well as the characterization of their synaptic interactions. These aims are often particularly difficult to achieve in neural circuits containing electrically-coupled neurones. In recent years two new methods (photoinactivation after Lucifer Yellow injection and intracellular injection of pronase) have been employed to delete selectively single neurones or small groups of neurones from neural circuits. These techniques have been successfully used in the analysis of circuits containing electrically-coupled neurones. In several systems new roles for electrical synapses in the integrative function of neural circuits have been proposed. In the nervous systems of both the leech and lobster it is now thought that synaptic interactions previously thought to be direct are mediated through an interposed, electrically-coupled neurone. In the pyloric system of the stomatogastric ganglion of the lobster, Panulirus interruptus, the Lucifer Yellow photoinactivation technique has permitted a separate analysis of the properties of several electrically-coupled neurones previously thought quite similar. We now know that the Anterior Burster (AB) interneurone and the Pyloric Dilator (PD) motor neurones, which together act as the pacemaker ensemble for the pyloric network, differ in many regards including their intrinsic ability to generate bursting pacemaker potentials, their neurotransmitters, their sensitivity to some neurotransmitters and hormones, the neural inputs they receive and their pattern of synaptic connectivity. These results will be discussed in the context of the role of electrical coupling in neuronal integration.

Electrically coupled pacemaker neurons respond differently to same physiological inputs and neurotransmitters

1984 ◽  
Vol 51 (6) ◽  
pp. 1362-1374 ◽  
Author(s):  
E. Marder ◽  
J. S. Eisen
Keyword(s):  
Motor Neurons ◽  
Slow Wave ◽  
Lucifer Yellow ◽  
Electrical Coupling ◽  
Excitatory Postsynaptic Potential ◽  
Panulirus Interruptus ◽  
Bursting Neuron ◽  
Postsynaptic Potential ◽  
Pyloric Dilator ◽  
Muscarinic Cholinergic

The two pyloric dilator (PD) motor neurons and the single anterior burster (AB) interneuron are electrically coupled and together comprise the pacemaker for the pyloric central pattern generator of the stomatogastric ganglion of the lobster, Panulirus interruptus. Previous work (31) has shown that the AB neuron is an endogenously bursting neuron, while the PD neuron is a conditional burster. In this paper the effects of physiological inputs and neurotransmitters on isolated PD neurons and AB neurons were studied using the lucifer yellow photoinactivation technique (33). Stimulation of the inferior ventricular nerve (IVN) fibers at high frequencies elicits a triphasic response in AB and PD neurons: a rapid excitatory postsynaptic potential (EPSP) followed by a slow inhibitory postsynaptic potential (IPSP), followed by an enhancement of the pacemaker slow-wave depolarizations. Photoinactivation experiments indicate that the enhancement of the slow wave is due primarily to actions of the IVN fibers on the PD neurons but not on the AB neuron. Bath-applied dopamine dramatically alters the motor output of the pyloric system. Photoinactivation experiments show that 10(-4) M dopamine increases the amplitude and frequency of the slow-wave depolarizations recorded in the AB neurons but hyperpolarizes and inhibits the PD neurons. Bath-applied serotonin increases the frequency and amplitude of the slow-wave depolarizations in the AB neuron but has no effect on PD neurons. Pilocarpine, a muscarinic cholinergic agonist, stimulates slow-wave depolarization production in both PD neurons and the AB neuron, but the waveform and frequency of the slow waves elicited are quite different. These results show that although the electrically coupled PD and AB neurons always depolarize synchronously and act together as the pacemaker for the pyloric system, they respond differently to a neuronal input and to several putative neuromodulators. Thus, despite electrical coupling sufficient to ensure synchronous activity, the PD and AB neurons can be modulated independently.

Transmitter identification of pyloric neurons: electrically coupled neurons use different transmitters

1984 ◽  
Vol 51 (6) ◽  
pp. 1345-1361 ◽  
Author(s):  
E. Marder ◽  
J. S. Eisen
Keyword(s):  
Motor Neurons ◽  
Neuromuscular Junctions ◽  
Lucifer Yellow ◽  
Inhibitory Response ◽  
Published Data ◽  
Panulirus Interruptus ◽  
Synaptic Interactions ◽  
Low Concentrations ◽  
Pyloric Dilator ◽  
Functional Consequences

The neurotransmitters mediating the synaptic interactions among the neurons of the pyloric system of the stomatogastric ganglion (STG) of the lobster, Panulirus interruptus, were examined using a combination of electrophysiological, pharmacological, and biochemical techniques. Iontophoretically applied L-glutamate inhibited all motor neurons of the pyloric system. This inhibitory response was blocked by low concentrations of picrotoxin but unaffected by atropine. The anterior burster (AB) interneuron, pyloric dilator (PD) motor neurons, and ventricular dilator (VD) motor neuron were depolarized and excited by iontophoretically applied acetylcholine (ACh). The lateral pyloric (LP) and pyloric (PY) constrictor motor neurons were inhibited by ACh and by the cholinergic agonist, carbachol. These inhibitory cholinergic responses were blocked by atropine but not by picrotoxin. The inhibitory postsynaptic potentials (IPSPs) evoked by the constrictor motor neurons were blocked by picrotoxin but not by atropine. Taken together with previously published data (15, 18), this suggests that the constrictor motor neurons release glutamate at both their excitatory neuromuscular junctions and their inhibitory intraganglionic junctions. The lucifer yellow photoinactivation technique (27) was used to study separately the neurotransmitters released by the electrically coupled PD and AB neurons. The AB-evoked IPSPs were blocked by picrotoxin but not by atropine. The PD-evoked IPSPs were blocked by atropine and other muscarinic antagonists but not by picrotoxin. Somata of PD neurons contained choline acetyltransferase (CAT) activity, but somata of AB neurons contained no detectable CAT activity. On the basis of the data in this paper and previously published data (17, 18), we conclude that the PD neurons release ACh at both their excitatory neuromuscular junctions and their inhibitory intraganglionic connections. Although the AB neuron is electrically coupled to the PD neurons, the AB neuron is not cholinergic. Glutamate is a likely transmitter candidate for the AB neuron. These data show that electrically coupled neurons can release different transmitters. Furthermore, these data show that an IPSP can be the result of the combined actions of two different neurotransmitters, each released from a different neuron. The functional consequences of these conclusions are explored in the following papers (9, 22).

A rhythmic modulatory gating system in the stomatogastric nervous system of Homarus gammarus. I. Pyloric-related neurons in the commissural ganglia

1994 ◽  
Vol 71 (6) ◽  
pp. 2477-2489 ◽  
Author(s):  
F. Nagy ◽  
P. Cardi ◽  
I. Cournil
Keyword(s):  
Lucifer Yellow ◽  
Spiny Lobster ◽  
Electrical Coupling ◽  
Firing Frequency ◽  
Gamma Aminobutyric Acid ◽  
Stomatogastric Nervous System ◽  
Panulirus Interruptus ◽  
Homarus Gammarus ◽  
Commissural Neurons ◽  
Pyloric Network

1. Operation of the pyloric neural network in the crustacean stomatogastric ganglion (STG) depends on constant firing of modulatory inputs from anterior ganglia. We have identified two bilaterally symmetrical pairs of these inputs in the commissural ganglia (COGs) of the European rock lobster Homarus gammarus. During operation of the pyloric CPG, they fired in pyloric time, out of phase with the pyloric pacemakers. 2. One of the pair was the commissural pyloric (CP) neuron and the other was homologous to the P neuron described in the spiny lobster Panulirus interruptus. We describe their morphology and location in the COG. The CP neuron projected to the STG via the superior esophageal nerve (son) and the stomatogastric nerve (stn), whereas the P neuron projected via the inferior esophageal nerve (ion) and stn. 3. To determine the total number of commissural neurons projecting to the STG, we used cobalt and Lucifer yellow backfilling from their cut axons in the stn. With the ion cut, there were between 8 to 12 labeled somata in each COG including CP cell body, whereas only 2 somata (including P) were labeled with the son cut. Among these neurons, CP and P appeared to be the only commissural neurons that fired in pyloric time and projected in the STG on the pyloric network. 4. The CP neuron produced monosynaptic excitatory postsynaptic potentials (EPSPs) on the pyloric dilator (PD), lateral pyloric (LP), and inferior cardiac (IC) neurons, whereas the P neuron produced monosynaptic EPSPs on all pyloric motoneurons but IC. The P neuron was gamma-aminobutyric acid immunoreactive, and the P-derived EPSPs in pyloric neurons were reversibly blocked by bicuculline, picrotoxin, and D-tubocurarine. 5. The CP and P neurons were electrically coupled, and modification of membrane potential in either one of them appreciably changed the firing frequency of the coupled neuron. 6. A negative-feedback loop from the pyloric anterior burster (AB) interneuron provoked simultaneous rhythmic inhibitions in the P and CP neurons. Together with the electrical coupling, the rhythmic inhibition contributed to synchronize firing of the two commissural neurons. 7. The following papers in the series of describe the modulatory and rhythmic control exerted by the P and CP neurons over the pyloric pattern generator.

scholarly journals Neural architecture: from cells to circuits

2018 ◽  
Vol 120 (2) ◽  
pp. 854-866 ◽  
Author(s):  
Sarah E. V. Richards ◽  
Stephen D. Van Hooser
Keyword(s):  
Nervous System ◽  
Cerebral Cortex ◽  
Structure Function ◽  
Neural Circuits ◽  
Neural Circuit ◽  
Neuronal Morphology ◽  
Neural Architecture ◽  
Synaptic Interactions ◽  
Branching Patterns ◽  
Circuit Function

Circuit operations are determined jointly by the properties of the circuit elements and the properties of the connections among these elements. In the nervous system, neurons exhibit diverse morphologies and branching patterns, allowing rich compartmentalization within individual cells and complex synaptic interactions among groups of cells. In this review, we summarize work detailing how neuronal morphology impacts neural circuit function. In particular, we consider example neurons in the retina, cerebral cortex, and the stomatogastric ganglion of crustaceans. We also explore molecular coregulators of morphology and circuit function to begin bridging the gap between molecular and systems approaches. By identifying motifs in different systems, we move closer to understanding the structure-function relationships that are present in neural circuits.

Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. III. Synaptic connections of electrically coupled pyloric neurons

1982 ◽  
Vol 48 (6) ◽  
pp. 1392-1415 ◽  
Author(s):  
J. S. Eisen ◽  
E. Marder
Keyword(s):  
Motor Neurons ◽  
Lucifer Yellow ◽  
Electrical Coupling ◽  
Stomatogastric Ganglion ◽  
Pattern Generation ◽  
Inhibitory Postsynaptic Potentials ◽  
Pyloric Dilator ◽  
Time Courses ◽  
Ion Selectivities ◽  
Electrotonic Potential

1. The pyloric dilator (PD) and anterior burster (AB) neurons in the pyloric system of the lobster stomatogastric ganglion are electrically coupled and synchronously active. We have used the lucifer yellow photoinactivation technique to separate the connections made by the PD motor neurons from those made by the AB interneuron. 2. Photoinactivation of either the two PD neurons or the single AB neuron allowed us to separate the compound inhibitory postsynaptic potentials (IPSPs) in the lateral pyloric (LP) and pyloric (PY) motor neurons resulting from synchronous PD and AB activity into AB-evoked and PD-evoked components. These IPSPs have different time courses, reversal potentials, ion selectivities, and pharmacological properties. 3. Photoinactivation and membrane-potential manipulations indicated that a readily observable IPSP recorded in the AB neuron and correlated with action potentials in the LP neuron is actually an electrotonic potential due to an LP-evoked IPSP in the PD neurons. 4. Selective inactivation of either the two PD neurons or the AB neuron revealed that the IPSP recorded in the ventricular dilator (VD) motor neuron is due solely to AB-released transmitter. 5. The electrical coupling potentials measurable between the AB, PD, and VD neuron somata are due to direct electrical coupling between all of these neurons. 6. Circuit analysis and transmitter identification may be complicated by electrical coupling. We suggest that the presence of electrical coupling between nonidentical neurons may provide a new mechanism that allows changes in synaptic characteristics among neurons within a "hard-wired" circuit.

Follower Neurons in Lobster (Panulirus interruptus) Pyloric Network Regulate Pacemaker Period in Complementary Ways

2003 ◽  
Vol 89 (3) ◽  
pp. 1327-1338 ◽  
Author(s):  
Adam L. Weaver ◽  
Scott L. Hooper
Keyword(s):  
Neural Networks ◽  
Electrical Coupling ◽  
Network Activity ◽  
Cycle Period ◽  
Period Range ◽  
Panulirus Interruptus ◽  
Pyloric Network ◽  
Baseline Activity ◽  
Insight Into

Distributed neural networks (ones characterized by high levels of interconnectivity among network neurons) are not well understood. Increased insight into these systems can be obtained by perturbing network activity so as to study the functions of specific neurons not only in the network's “baseline” activity but across a range of network activities. We applied this technique to study cycle period control in the rhythmic pyloric network of the lobster, Panulirus interruptus. Pyloric rhythmicity is driven by an endogenous oscillator, the Anterior Burster (AB) neuron. Two network neurons feed back onto the pacemaker, the Lateral Pyloric (LP) neuron by inhibition and the Ventricular Dilator (VD) neuron by electrical coupling. LP and VD neuron effects on pyloric cycle period can be studied across a range of periods by altering period by injecting current into the AB neuron and functionally removing (by hyperpolarization) the LP and VD neurons from the network at each period. Within a range of pacemaker periods, the LP and VD neurons regulate period in complementary ways. LP neuron removal speeds the network and VD neuron removal slows it. Outside this range, network activity is disrupted because the LP neuron cannot follow slow periods, and the VD neuron cannot follow fast periods. These neurons thus also limit, in complementary ways, normal pyloric activity to a certain period range. These data show that follower neurons in pacemaker networks can play central roles in controlling pacemaker period and suggest that in some cases specific functions can be assigned to individual network neurons.

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.

Sensitive Periods in the Development of the Brain and Behavior

2004 ◽  
Vol 16 (8) ◽  
pp. 1412-1425 ◽  
Author(s):  
Eric I. Knudsen
Keyword(s):  
Neural Circuits ◽  
Neural Circuit ◽  
Critical Role ◽  
Sensitive Period ◽  
Critical Periods ◽  
Sensitive Periods ◽  
Brain And Behavior ◽  
The Individual ◽  
And Behavior ◽  
The Brain

Experience exerts a profound influence on the brain and, therefore, on behavior. When the effect of experience on the brain is particularly strong during a limited period in development, this period is referred to as a sensitive period. Such periods allow experience to instruct neural circuits to process or represent information in a way that is adaptive for the individual. When experience provides information that is essential for normal development and alters performance permanently, such sensitive periods are referred to as critical periods. Although sensitive periods are reflected in behavior, they are actually a property of neural circuits. Mechanisms of plasticity at the circuit level are discussed that have been shown to operate during sensitive periods. A hypothesis is proposed that experience during a sensitive period modifies the architecture of a circuit in fundamental ways, causing certain patterns of connectivity to become highly stable and, therefore, energetically preferred. Plasticity that occurs beyond the end of a sensitive period, which is substantial in many circuits, alters connectivity patterns within the architectural constraints established during the sensitive period. Preferences in a circuit that result from experience during sensitive periods are illustrated graphically as changes in a “stability landscape,” a metaphor that represents the relative contributions of genetic and experiential influences in shaping the information processing capabilities of a neural circuit. By understanding sensitive periods at the circuit level, as well as understanding the relationship between circuit properties and behavior, we gain a deeper insight into the critical role that experience plays in shaping the development of the brain and behavior.

Synaptic Modulation of the Interspike Interval Signatures of Bursting Pyloric Neurons

2003 ◽  
Vol 89 (3) ◽  
pp. 1363-1377 ◽  
Author(s):  
Attila Szűcs ◽  
Reynaldo D. Pinto ◽  
Michail I. Rabinovich ◽  
Henry D. I. Abarbanel ◽  
Allen I. Selverston
Keyword(s):  
Interspike Interval ◽  
Synaptic Connectivity ◽  
Stomatogastric Nervous System ◽  
Firing Patterns ◽  
Synaptic Modulation ◽  
Pyloric Network ◽  
Synaptic Interactions ◽  
Pyloric Dilator ◽  
Temporal Structures ◽  
Spike Patterns

The pyloric network of the lobster stomatogastric nervous system is one of the best described assemblies of oscillatory neurons producing bursts of action potentials. While the temporal patterns of bursts have been investigated in detail, those of spikes have received less attention. Here we analyze the intraburst firing patterns of pyloric neurons and the synaptic interactions shaping their dynamics in millisecond time scales not performed before. We find that different pyloric neurons express characteristic, cell-specific firing patterns in their bursts. Nonlinear analysis of the interspike intervals (ISIs) reveals distinctive temporal structures (‘interspike interval signatures’), which are found to depend on the synaptic connectivity of the network. We compare ISI patterns of the pyloric dilator (PD), lateral pyloric (LP), and ventricular dilator (VD) neurons in 1) normal conditions, 2) after blocking glutamatergic synaptic connections, and 3) in various functional configurations of the three neurons. Manipulation of the synaptic connectivity results in characteristic changes in the ISI signatures of the postsynaptic neurons. The intraburst firing pattern of the PD neuron is regularized by the inhibitory synaptic connection from the LP neuron as revealed in current-clamp experiments and also as reconstructed with a dynamic clamp. On the other hand, mutual inhibition between the LP and VD neurons tend to produce more irregular bursts with increased spike jitter. The results show that synaptic interactions fine-tune the output of pyloric neurons. The present data also suggest a way of processing of synaptic information: bursting neurons are capable of encoding incoming signals by altering the fine structure of their intraburst spike patterns.

Pharmacological dissection of pyloric network of the lobster stomatogastric ganglion using picrotoxin

1980 ◽  
Vol 44 (6) ◽  
pp. 1089-1101 ◽  
Author(s):  
M. Bidaut
Keyword(s):  
Stomatogastric Ganglion ◽  
Inhibitory Synapses ◽  
Primary Role ◽  
Panulirus Interruptus ◽  
Pyloric Network ◽  
Pyloric Dilator ◽  
Fast Rise ◽  
Later Phase ◽  
Pyloric Rhythm

1. Picrotoxin (PTX) (10(-7)-10(-6) M) completely blocked most inhibitory synapses in the pyloric pattern generator of the lobster (Panulirus interruptus) stomatogastric ganglion. The sensitivity of synapses from most classes of identified neurons was examined. Blockade was at least partly reversible with prolonged washing. 2. The synapses from pyloric dilator (PD) neurons were the only inhibitory synapses that picrotoxin failed to block completely. 3. A correlation is derived that brief, fast-rise inhibitory postsynaptic potentials (IPSPs) are picrotoxin sensitive, whereas a slow rounded component of IPSPs from PD neurons is not picrotoxin sensitive. 4. Picrotoxin caused specific changes in the pattern of the motor rhythm produced by the 16-cell pyloric network. This sheds some light on the functional role of particular synapses in the pyloric generator. 5. The endogenously bursting neurons (PD and anterior burster (AB)), which drive the pyloric rhythm, kept a similar burst rate. 6. Under picrotoxin, the pyloric "follower" neurons all moved to later phase relative to the "driver" group. Some normally antagonistic cells, related by reciprocal inhibitor connections, became in-phase. These and other pattern changes could be related to blockade of particular synapses. 7. The pyloric rhythm was still quite recognizable under picrotoxin despite the drastically altered circuitry of the synaptic network. This supports the idea that periodic inhibition from the PD driver neurons plays a primary role in creating the pyloric pattern.

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