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.

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.

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).

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.

Deep neurons in piriform cortex. I. Morphology and synaptically evoked responses including a unique high-amplitude paired shock facilitation

1989 ◽  
Vol 62 (2) ◽  
pp. 369-385 ◽  
Author(s):  
G. F. Tseng ◽  
L. B. Haberly
Keyword(s):  
Lucifer Yellow ◽  
Piriform Cortex ◽  
Afferent Fiber ◽  
Pyramidal Cells ◽  
Excitatory Postsynaptic Potential ◽  
Response Properties ◽  
Postsynaptic Potential ◽  
Association Fibers ◽  
Axonal Arbors ◽  
Stimulation Of

1. Synaptic responses of cells in layer III of the piriform cortex and the subjacent endopiriform nucleus (layer IV) were analyzed with intracellular recording techniques in a slice preparation from the rat, cut perpendicular to the pial surface. 2. Micropipettes containing Lucifer yellow (LY) were used to correlate response properties with morphology. An antiserum to LY was used to intensify staining and to prevent fading during detailed morphological study. Response properties were also examined with potassium acetate-containing electrodes. 3. Morphologically, two cell types were identified: pyramidal cells that were confined to layer III of the piriform cortex and multipolar cells that were in layer III and the endopiriform nucleus. 4. In morphology, deep pyramidal cells in layer III closely resembled superficial pyramidal cells in layer II, with the exception that primary apical dendritic trunks were longer and basal dendritic arborizations were more extensive than apical. Like superficial pyramidal cells, apical dendrites of all deep pyramidal cells stained extended through the afferent fiber termination zone in layer Ia and gave rise to local axonal arbors that were concentrated in layer III and the endopiriform nucleus. 5. Multipolar cells were morphologically indistinguishable in layer III and the endopiriform nucleus. All gave rise to nonvaricose spiny dendrites that never extended into layer II and local axonal arbors. 6. Response properties of deep pyramidal and multipolar cells were similar; responses of both of these populations were very different from those of superficial pyramidal cells. The primary difference between responses of deep pyramidal and multipolar cells was a shorter latency of postsynaptic potentials evoked in deep pyramidal cells by stimulation of afferent fibers, consistent with the extension of their dendrites into layer Ia. 7. Responses of most deep cells to stimulation of afferent and association fibers at sufficiently high strength consisted of an initial excitatory postsynaptic potential (EPSP), followed by a fast Cl- -mediated and a slow K+-mediated inhibitory postsynaptic potential (IPSP). 8. A characteristic feature of deep cells, which was only rarely observed in superficial pyramidal cells, was the presence of variable EPSPs evoked at long latencies (greater than 100 ms) by stimulation of afferent or association fibers. 9. A striking finding for deep pyramidal and multipolar cells, when studied with LY-containing pipettes, was a variable slowly rising depolarizing potential triggered at depolarized membrane potentials by stimulation of afferent or association fibers.(ABSTRACT TRUNCATED AT 400 WORDS)

Integration of biphasic synaptic input by electrotonically coupled neuroendocrine caudodorsal cells in the pond snail

1983 ◽  
Vol 49 (6) ◽  
pp. 1392-1409 ◽  
Author(s):  
A. ter Maat ◽  
E. W. Roubos ◽  
J. C. Lodder ◽  
P. Buma
Keyword(s):  
Synaptic Input ◽  
Lymnaea Stagnalis ◽  
Electrical Coupling ◽  
Pond Snail ◽  
Excitatory Postsynaptic Potential ◽  
Postsynaptic Potential ◽  
Electrophysiological Recordings ◽  
Coupled Cells ◽  
Lateral Branches ◽  
Dorsal Cells

The ovulation hormone-producing caudodorsal cells (CDCs) of the pond snail Lymnaea stagnalis form two clusters of electrotonically coupled cells, each containing a few specialized (ventral) cells that connect the clusters. The hormone is secreted during a pacemaker-driven discharge. The CDCs receive a biphasic cholinergic postsynaptic potential (PSP), consisting of a rapid excitatory postsynaptic potential (EPSP) and a slow inhibitory postsynaptic potential (IPSP) that is elicited by stimulation of nerves. The effect of the synaptic input on the discharge of the CDCs is described and the location of the synapse investigated by a combination of electrophysiological recordings and morphological techniques. The PSP interrupts the discharge and hastens its termination. In addition, it causes a reversal of the temporal order of the spikes of ventral cells (that normally lead) and dorsal cells (that lead only after the PSP). Ion-substitution experiments indicate that the ionic mechanism underlying the biphasic PSP is conventional, involving a conductance increase for Na+ (EPSP) and K+ (IPSP). Receptors mediating the inhibitory component occur only on the proximal axons of the ventral cells, both components are larger and reverse more readily in ventral cells. These findings suggest that the PSP is generated in the ventral cells. The biphasic PSP has no effect on electrical coupling, suggesting that it is not generated along the electrical pathways among the cells. Horseradish peroxidase (HRP) staining reveals that the lateral branches emerge from the proximal axons of the ventral cells only. In HRP-filled preparations processed for electron microscopy (EM) acetylcholinesterase is demonstrated at these branches where it occurs associated with synapses. The location on fine branches of the ventral cells explains the absence of an effect on electrotonic transmission, whereas the reluctance of components of the PSP to reverse at the expected potentials is due to the distribution of the synapses over more than one cell. It is concluded that the biphasic PSP is received only by the ventral cells and that it is conveyed electrotonically to the other cells.

Serotonin-Immunoreactive CPT Interneurons in Hermissenda: Identification of Sensory Input and Motor Projections

2006 ◽  
Vol 96 (1) ◽  
pp. 327-335 ◽  
Author(s):  
Lian-Ming Tian ◽  
Ryo Kawai ◽  
Terry Crow
Keyword(s):  
Motor Neurons ◽  
Sensory Input ◽  
Lucifer Yellow ◽  
Fluorescent Labeling ◽  
Excitatory Postsynaptic Potential ◽  
Ciliary Activity ◽  
Small Complex ◽  
Axonal Process ◽  
Immunohistochemical Techniques ◽  
Stimulation Of

Serotonin immunoreactive (5-HT-IR) neurons identified as cerebropleural ganglion triplets (CPTs) in Hermissenda may be homologues of 5-HT-IR neurons identified in other opisthobranch molluscs. In studies of isolated nervous systems and semi-intact preparations we used a combination of immunohistochemical techniques and fluorescent labeling with Lucifer yellow to identify 5-HT-IR CPT neurons after investigating sensory inputs and motor neuron projections. Here we show that identified 5-HT-IR CPT interneurons receive sensory input from mechanoreceptors and photoreceptors. In semi-intact preparations with intact pedal nerves P1 and P2, cutaneous stimulation of the middle or tail regions of the foot with calibrated von Frey hairs elicited spikes recorded from identified CPT interneurons. Illumination of the eyes evoked a small complex excitatory postsynaptic potential (EPSP) and resulted in a modest increase in the spike discharge of CPT interneurons. Immunostaining of Lucifer yellow–labeled neurons revealed that CPT interneurons projected an axonal process to the contralateral pedal ganglion. Depolarization of CPT interneurons with extrinsic current evoked EPSPs and spikes recorded from identified VP2 pedal neurons, motor neurons previously shown to elicit movement of the anterior foot. Extrinsic current stimulation of CPT interneurons in semi-intact preparations evoked movement of the anterior foot but did not facilitate ciliary activity or evoke PSPs recorded in identified VP1 ciliary motor neurons. Our results show that CPT neurons are polysensory interneurons that contribute to reflexive foot contractions in Hermissenda.

Intrinsic noise at synapses between a wing hinge stretch receptor and flight motor neurons in the locust

2001 ◽  
Vol 204 (1) ◽  
pp. 127-138 ◽  
Author(s):  
P.J. Simmons
Keyword(s):  
Motor Neurons ◽  
Background Noise ◽  
Intrinsic Noise ◽  
Stretch Receptor ◽  
Excitatory Postsynaptic Potential ◽  
Normal Distributions ◽  
Postsynaptic Potential ◽  
Synaptic Noise ◽  
Presynaptic Spike ◽  
Flight Motor

Variability in postsynaptic potential (PSP) amplitude due to intrinsic noise limits the reliability of communication between neurons. I measured PSP variability at synapses between a forewing stretch receptor and wing depressor motor neurons in locusts, a pathway that is important in the control of flying. The intrinsic noise in the stretch receptor output synapse was measured by subtracting the background noise, originating in other synaptic pathways onto the motor neuron, from the variability in the amplitudes of PSPs evoked by the stretch receptor. Intrinsic synaptic noise caused successive PSPs to vary by 4–10 % in basalar and subalar flight motor neurons. Recordings from pairs of these wing depressor motor neurons showed that the amount of transmitter released varied independently between different output sites from the stretch receptor. Histograms of excitatory postsynaptic potential amplitude were normal distributions that lacked separate peaks. I estimate that quantal amplitude is significantly less than 0.1 mV and that several hundred quanta are released for each presynaptic spike. This accords well with a previous estimate of the number of discrete anatomical synapses and would facilitate modulation of output from the stretch receptor.

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 Dopamine Modulation of Two Delayed Rectifier Potassium Currents in a Small Neural Network

2005 ◽  
Vol 94 (4) ◽  
pp. 2888-2900 ◽  
Author(s):  
Matthias Gruhn ◽  
John Guckenheimer ◽  
Bruce Land ◽  
Ronald M. Harris-Warrick
Keyword(s):  
Motor Neurons ◽  
Spiny Lobster ◽  
Potassium Currents ◽  
Cell Types ◽  
Spike Frequency ◽  
Differential Sensitivity ◽  
Single Type ◽  
Delayed Rectifier ◽  
Panulirus Interruptus ◽  
Pyloric Dilator

Delayed rectifier potassium currents [ IK(V)] generate sustained, noninactivating outward currents with characteristic fast rates of activation and deactivation and play important roles in shaping spike frequency. The pyloric motor network in the stomatogastric ganglion of the spiny lobster, Panulirus interruptus, is made up of one interneuron and 13 motor neurons of five different classes. Dopamine (DA) increases the firing frequencies of the anterior burster (AB), pyloric (PY), lateral pyloric (LP), and inferior cardiac (IC) neurons and decreases the firing frequencies of the pyloric dilator (PD) and ventricular dilator (VD) neurons. In all six types of pyloric neurons, IK(V) is small with respect to other K+ currents. It is made up of at least two TEA-sensitive components that show differential sensitivity to 4-aminopyridine and quinidine, and have differing thresholds of activation. One saturable component is activated at potentials above −25 mV, whereas the second component appears at more depolarized voltages and does not saturate at voltage steps up to +45 mV. The magnitude of the components varies among cell types but also shows considerable variation within a single type. A subset of PY neurons shows a marked enhancement in spike frequency with DA; DA evokes a pronounced reversible increase in IK(V) conductance of ≤30% in the PY neurons studied, and on average significantly increases both components of IK(V). The AB neuron also shows a reversible 20% increase in the steady state IK(V). DA had no effect on IK(V) in PD, LP, VD, and IC neurons. The physiological roles of these currents and their modulation by DA are discussed.

Sensory, interneuronal, and motor interactions within Hermissenda visual pathway

1984 ◽  
Vol 52 (1) ◽  
pp. 156-169 ◽  
Author(s):  
Y. Goh ◽  
D. L. Alkon
Keyword(s):  
Hair Cells ◽  
Lucifer Yellow ◽  
Type A ◽  
Visual Pathway ◽  
Excitatory Input ◽  
Excitatory Postsynaptic Potential ◽  
Type B ◽  
Postsynaptic Potential ◽  
Chemical Synapses ◽  
Stimulation Of

The visual pathway of Hermissenda was identified by means of intracellular recordings and iontophoretic injection of the fluorescent dye lucifer yellow. This pathway consisted of five neuron types, namely, type B photoreceptors and the medial type A photoreceptor within each of the two eyes, hair cells in the two statocysts, a group of interneurons in the cerebropleural ganglia, and a putative motor neuron (MN1) in each pedal ganglion. The MN1 cells responded during illumination of the eye with increased impulse and excitatory postsynaptic potential (EPSP) activity. This response was often followed by bursting activity for higher light intensities. The medial type A photoreceptor, which was found to be inhibited by medial and intermediate type B photoreceptors, was demonstrated to excite the MN1 cell indirectly via a group of identified interneurons. Hair cells were also found to excite the MN1 cell indirectly via these interneurons. Among the ipsilateral hair cells, cephalic hair cells were least frequently found to excite the MN1 cell. Among the contralateral hair cells, on the other hand, lateral hair cells were most often found to excite the MN1 cell. Interneurons that were shown to excite the MN1 cell received excitatory input from the medial type A photoreceptor and hair cells. Our observations are consistent with the interpretation that these interactions are mediated by monosynaptic chemical synapses. Electrical stimulation of the MN1 cell with positive-current injection produced turning of the posterior half of the animal's foot to the ipsilateral direction consistent with the animal's turning behavior toward light. The visual pathway identified in this experiment was considered to have some significance in explaining, at least in part, a causal role for changes within type B photoreceptors in producing Hermissenda's modified behavior following associative conditioning.

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