Heterosynaptic modulation by the octopaminergic OC interneurons increases the synaptic outputs of protraction phase interneurons (SO, N1L) in the feeding system of Lymnaea stagnalis

Neuroscience ◽  
2002 ◽  
Vol 115 (2) ◽  
pp. 483-494 ◽  
Author(s):  
Á Vehovszky ◽  
C.J.H Elliott
Keyword(s):  
Lymnaea Stagnalis ◽  
Feeding System ◽  
Protraction Phase

Cholinergic interneurons in the feeding system of the pond snail lymnaea stagnalis. I. cholinergic receptors on feeding neurons

1992 ◽  
Vol 336 (1277) ◽  
pp. 157-166 ◽  
Keyword(s):  
Synaptic Input ◽  
Lymnaea Stagnalis ◽  
Cholinergic Receptors ◽  
Pond Snail ◽  
Feeding System ◽  
Inhibitory Receptor ◽  
Excitatory Response ◽  
Cholinergic Interneurons ◽  
Feeding Rhythm ◽  
Cholinergic Response

All the identified feeding motoneurons of Lymnaea respond to bath or iontophoretically applied acetylcholine (ACh). Three kinds of receptors (one excitatory, one fast inhibitory and one slow inhibitory) were distinguished pharmacologically. The agonist TMA (tetram ethylam m onium ) activates all three receptors, being weakest at the slow inhibitory receptor. PTMA (phenyltrim ethylam monium ) is less potent than TMA and is ineffective at the slow inhibitory receptor, which is the only receptor sensitive to arecoline. At 0.5 mM the antagonists HMT (hexamethonium) and ATR (atropine) selectively block the excitatory response, while PTMA reduces the response to ACh at all three receptors. d-TC (curare) antagonizes only the fast excitatory and the fast inhibitory responses, but MeXCh (methylxylocholine) blocks the fast excitatory and slow inhibitory responses solely. For each of the feeding motoneurons, the sign of the cholinergic response (excitation or inhibition) is the same as the synaptic input received in the N1 phase of the feeding rhythm .

Novel interneuron having hybrid modulatory-central pattern generator properties in the feeding system of the snail, Lymnaea stagnalis

1995 ◽  
Vol 73 (1) ◽  
pp. 112-124 ◽  
Author(s):  
M. S. Yeoman ◽  
A. Vehovszky ◽  
G. Kemenes ◽  
C. J. Elliott ◽  
P. R. Benjamin
Keyword(s):  
Central Pattern Generator ◽  
Lymnaea Stagnalis ◽  
Cell Types ◽  
Pattern Generator ◽  
Feeding System ◽  
Buccal Ganglia ◽  
Steady Current ◽  
Feeding Rhythm ◽  
Symmetrical Pair ◽  
Feeding Rhythms

1. We used intracellular recording techniques to examine the role of a novel type of protraction phase interneuron, the lateral N1 (N1L) in the feeding system of the snail Lymnaea stagnalis. 2. The N1Ls are a bilaterally symmetrical pair of electrotonically coupled interneurons located in the buccal ganglia. Each N1L sends a single axon to the contralateral buccal ganglia. Their neurite processes are confined to the buccal neuropile. 3. In the isolated CNS, depolarization of an N1L is capable of driving a full (N1-->N2-->N3), fast (1 cycle every 5 s) fictive feeding rhythm. This was unlike the previously described N1 medial (N1M) central pattern generator (CPG) interneurons that were only capable of driving a slow, irregular rhythm. Attempts to control the frequency of the fictive feeding rhythm by injecting varying amounts of steady current into the N1Ls were unsuccessful. This contrasts with a modulatory neuron, the slow oscillator (SO), that has very similar firing patterns to the N1Ls, but where the frequency of the rhythm depends on the level of injected current. 4. The N1Ls' ability to drive a fictive feeding rhythm in the isolated preparation was due to their strong, monosynaptic excitatory chemical connection with the N1M CPG interneurons. Bursts of spikes in the N1Ls generated summating excitatory postsynaptic potentials (EPSPs) in the N1Ms to drive them to firing. The SO excited the N1M cells in a similar way, but the EPSPs are strongly facilitatory, unlike the N1L-->N1M connection. 5. Fast (1 cycle every 5 s) fictive feeding rhythms driven by the N1L occurred in the absence of spike activity in the SO modulatory neuron. In contrast, the N1L was usually active in SO-driven rhythms. 6. The ability of the SO to drive the N1L was due to strong electrotonic coupling, SO-->N1L. The weaker coupling in the opposite direction, N1L-->SO, did not allow the N1L to drive the SO. 7. Experiments on semintact lip-brain preparations allowed fictive feeding to be evoked by application of 0.1 M sucrose to the lips (mimicking the normal sensory input) rather than by injection of depolarizing current. Rhythmic bursting, characteristic of fictive feeding, began in both the SO and N1L at exactly the same time, indicating that these two cell types are activated in "parallel" to drive the feeding rhythm. 8. The N1L is also part of the CPG network. It Excited the N2s and inhibited the N3 phasic (N3p) and N3 tonic (N3t) CPG interneurons like the N1Ms.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Octopamine: a new feeding modulator in Lymnaea

1998 ◽  
Vol 353 (1375) ◽  
pp. 1631-1643 ◽  
Author(s):  
Á Vehovszky ◽  
C. J. H. Elliott ◽  
E. E. Voronezhskaya ◽  
L. Hiripi ◽  
K. Elekes
Keyword(s):  
Central Nervous System ◽  
Nervous System ◽  
Lymnaea Stagnalis ◽  
Lucifer Yellow ◽  
Electrical Coupling ◽  
Pond Snail ◽  
Double Labelling ◽  
Feeding System ◽  
Morphological Criteria ◽  
Stimulation Of

The role of octopamine (OA) in the feeding system of the pond snail, Lymnaea stagnalis , was studied by applying behavioural tests on intact animals, and a combination of electrophysiological analysis and morphological labelling in the isolated central nervous system. OA antagonists phentolamine, demethylchlordimeform (DCDM) and 2–chloro–4–methyl–2–(phenylimino)–imidazolidine (NC–7) were injected into intact snails and the sucrose–induced feeding response of animals was monitored. Snails that received 25–50 mg kg -1 phentolamine did not start feeding in sucrose, and the same dose of NC–7 reduced the number of feeding animals by 80–90% 1–3 hours after injection. DCDM treatment reduced feeding by 20–60%. In addition, both phentolamine and NC–7 significantly decreased the feeding rate of those animals that still accepted food after 1–6 hours of injection. In the central nervous system a pair of buccal neurons was identified by electrophysiological and morphological criteria. After double labelling (intracellular staining with Lucifer yellow followed by OA–immunocytochemistry) these neurons were shown to be OA immunoreactive, and electrophysiological experiments confirmed that they are members of the buccal feeding system. Therefore the newly identified buccal neurons were called OC neurons (putative OA containing neurons or OAergic cells). Synchronous intracellular recordings demonstrated that the OC neurons share a common rhythm with feeding neurons either appearing spontaneously or evoked by intracellularly stimulated feeding interneurons. OC neurons also have synaptic connections with identified members of the feeding network: electrical coupling was demonstrated between OC neurons and members of the B4 cluster motoneurons, furthermore, chemically transmitted synaptic responses were recorded both on feeding motoneurons (B1, B2 cells) and the SO modulatory interneuron after the stimulation of OC neurons. However, elementary synaptic potentials could not be recorded on the follower cells of OC neurons. Prolonged (20 to 30 s) intracellular stimulation of OC cells activated the buccal feeding neurons leading to rhythmic activity pattern (fictive feeding) in a way similar to OA applied by perfusion onto isolated central nervous system (CNS) preparations. Our results suggest that OA acts as a modulatory substance in the feeding system of Lymnaea stagnalis and the newly identified pair of OC neurons belongs to the buccal feeding network.

Glutamatergic N2v Cells Are Central Pattern Generator Interneurons of the Lymnaea Feeding System: New Model for Rhythm Generation

1997 ◽  
Vol 78 (6) ◽  
pp. 3396-3407 ◽  
Author(s):  
M. J. Brierley ◽  
M. S. Yeoman ◽  
P. R. Benjamin
Keyword(s):  
Central Pattern Generator ◽  
Synaptic Connection ◽  
Giant Cells ◽  
Pattern Generator ◽  
Synaptic Connections ◽  
Rhythm Generation ◽  
Feeding System ◽  
New Model ◽  
Feeding Cycle ◽  
Protraction Phase

Brierley, M. J., M. S. Yeoman, and P. R. Benjamin. Glutamatergic N2v cells are central pattern generator interneurons of the Lymnaea feeding system: new model for rhythm generation. J. Neurophysiol. 78: 3396–3407, 1997. We aimed to show that the paired N2v (N2 ventral) plateauing cells of the buccal ganglia are important central pattern generator (CPG) interneurons of the Lymnaea feeding system. N2v plateauing is phase-locked to the rest of the CPG network in a slow oscillator (SO)-driven fictive feeding rhythm. The phase of the rhythm is reset by artificially evoked N2v bursts, a characteristic of CPG neurons. N2v cells have extensive input and output synaptic connections with the rest of the CPG network and the modulatory SO cell and cerebral giant cells (CGCs). Synaptic input from the protraction phase interneurons N1M (excitatory), N1L (inhibitory), and SO (inhibitory-excitatory) are likely to contribute to a ramp-shaped prepotential that triggers the N2v plateau. The prepotential has a highly complex waveform due to progressive changes in the amplitude of the component synaptic potentials. Most significant is the facilitation of the excitatory component of the SO → N2v monosynaptic connection. None of the other CPG interneurons has the appropriate input synaptic connections to terminate the N2v plateaus. The modulatory function of acetylcholine (ACh), the transmitter of the SO and N1M/N1Ls, was examined. Focal application of ACh (50-ms pulses) onto the N2v cells reproduced the SO → N2v biphasic synaptic response but also induced long-term plateauing (20–60 s). N2d cells show no endogenous ability to plateau, but this can be induced by focal applications of ACh. The N2v cells inhibit the N3 tonic (N3t) but not the N3 phasic (N3p) CPG interneurons. The N2v → N3t inhibitory synaptic connection is important in timing N3t activity. The N3t cells recover from this inhibition and fire during the swallow phase of the feeding pattern. Feedback N2v inhibition to the SO, N1L protraction phase interneurons prevents them firing during the retraction phase of the feeding cycle. The N2v → N1M synaptic connection was weak and only found in 50% of preparations. A weak N2v → CGC inhibitory connection prevents the CGCs firing during the rasp (N2) phase of the feeding cycle. These data allowed a new model for the Lymnaea feeding CPG to be proposed. This emphasizes that each of the six types of CPG interneuron has a unique set of synaptic connections, all of which contribute to the generation of a full CPG pattern.

Interactions of pattern-generating interneurons controlling feeding in Lymnaea stagnalis

1985 ◽  
Vol 54 (6) ◽  
pp. 1396-1411 ◽  
Author(s):  
C. J. Elliott ◽  
P. R. Benjamin
Keyword(s):  
Lymnaea Stagnalis ◽  
Inhibitory Input ◽  
Synaptic Connections ◽  
Feeding System ◽  
Intracellular Recordings ◽  
Inhibitory Pathway ◽  
Three Phase ◽  
Feeding Rhythm ◽  
Postinhibitory Rebound ◽  
Stimulation Of

Intracellular recordings were made from rhythm-generating interneurons in the Lymnaea feeding system. The feeding pattern is a three-phase rhythm of interneuronal activity (N1, N2, N3) corresponding to protraction, rasp, and swallow. We describe the firing pattern and anatomy of the premotor interneurons, each of which fires a predominant burst in only one phase of the feeding rhythm. The rhythm can be driven by steady depolarization of N1 cells. The phase of the rhythm is reset by brief stimulation of N2 or N3 interneurons. N1 neurons excite the N2 interneurons, and these in turn inhibit the N1 cells. This recurrent inhibitory pathway can account for the switch from the N1 phase of the feeding cycles to the N2 phase. The endogenous properties of the N2 interneurons are apparently responsible for the termination of N2 bursts. N3 interneurons display postinhibitory rebound (PIR), and this probably contributes to their burst after the end of the N2 inhibitory input. N2 and N3 interneurons inhibit the N1 cells. When the N3 burst dies away, activity in N1 cells resumes under the stimulus of depolarizing current. Interactions between interneurons are mainly by discrete, monophasic postsynaptic potentials, that follow 1:1. They have relatively short latency (2-12 ms) and duration (up to 100 ms). The synaptic connections between the three types of premotor interneurons are sufficient to account for the sequence of activity seen during feeding.

Cholinergic interneurons in the feeding system of the pond snail Lymnaea stagnalis . III. Pharmacological dissection of the feeding rhythm

1992 ◽  
Vol 336 (1277) ◽  
pp. 181-189 ◽  
Keyword(s):  
Lymnaea Stagnalis ◽  
Feeding Activity ◽  
Reciprocal Inhibition ◽  
Experimental Results ◽  
Cholinergic Antagonists ◽  
Pond Snail ◽  
Feeding System ◽  
Inhibition Model ◽  
Cholinergic Interneurons ◽  
Feeding Rhythm

The feeding activity of the pond snail Lymnaea stagnalis was stimulated by depolarization of a modulatory interneuron (SO) or of a N1 pattern-generating interneuron. The cholinergic antagonists phenyltrim ethylammonium (PTMA), methylxylocholine (MeXCh), hexamethonium (HMT) and atropine (ATR) were applied at 0.5 mM in the bath and their effects on the rhythmic feeding pattern were monitored. Each of the antagonists slowed or blocked the feeding rhythm. The block was due to interference in the pattern generating network, not to disturbance of modulatory inputs. The experimental results favour a model in which the alternation of protraction (N l) and retraction (N2) phases occurs by recurrent inhibition. The results would be more difficult to explain on the reciprocal inhibition model. When all the N1 output was blocked, the N1 neurons fired rhythmic bursts endogenously.

scholarly journals Properties of Ventral Cerebral Neurones Involved in the Feeding System of the Snail, Lymnaea Stagnalis

1984 ◽  
Vol 108 (1) ◽  
pp. 257-272
Author(s):  
C. R. MCCROHAN
Keyword(s):  
Lymnaea Stagnalis ◽  
Rhythmic Activity ◽  
Cell Types ◽  
Feeding System ◽  
Oral Aperture ◽  
Axonal Projections ◽  
Cerebral Ganglia ◽  
Buccal Ganglia ◽  
Relationship Of ◽  
The Relationship

Four identified neurone types (CV3, 7, 5 and 6), located in the ventral cerebral ganglia of Lymnaea stagnalis, are described. These cells have axonal projections in one or more of the nerves innervating the lips. In addition, they show rhythmic synaptic inputs leading to strong burst activity in phase with cyclic output from the buccal ganglia, suggesting a role in the control of the oral aperture during feeding. The innervation of lip muscle by one of the cell types (CV7) is confirmed electrophysiologically. The relationship of rhythmic activity in CV cells with that in the buccal feeding system is discussed.

Cholinergic interneurons in the feeding system of the pond snail Lymnaea stagnalis. II. N1 interneurons make cholinergic synapses with feeding m otoneurons

1992 ◽  
Vol 336 (1277) ◽  
pp. 167-180 ◽  
Keyword(s):  
Lymnaea Stagnalis ◽  
Preceding Paper ◽  
Cholinergic Receptor ◽  
Pond Snail ◽  
Postsynaptic Potentials ◽  
Cholinergic Interneurons ◽  
Cholinergic Synapses ◽  
Agonist And Antagonist ◽  
Protraction Phase ◽  
Chemical Synapses

The N1 neurons are a population of interneurons active during the protraction phase of the feeding rhythm . All the N1 neurons are coupled by electrical synapses which persist in a high Mg/low Ca saline which blocks chemical synapses. Individual N1 spikes produce discrete electrotonic postsynaptic potentials (PSPS) in other N1 cells, but the coupling is not strong enough to ensure 1:1 firing. Bursts of N1 spikes generate com pound PSPS in the feeding motoneurons. The sign (excitation or inhibition) of the N1 input corresponds with the synaptic barrage recorded during the protraction phase. Discrete PSPS are only resolved in a Hi-Di saline. Their variation in latency and number can be explained by variation in electrotonic propagation within the electrically coupled network of N1 cells. The excitatory postsynaptic potentials (EPSPS) in the 1 cell are reduced by 0.5 mM antagonists hexamethonium (HMT), atropine (ATR), curare (d-TC) and by methylxylocholine (MeXCh), all of which block the excitatory cholinergic receptor (Elliott et al. ( Phil. Trans. R. Soc. Lond. 336, 157-166 (Preceding paper.) (1992)). The 1 cell EPSPS were transiently blocked by phenyltrimethylammonium (PTMA), which is both an agonist and antagonist at the 1 cell excitatory acetylcholine (ACh) receptor (Elliott et al. 1992). The inhibitory postsynaptic potential (IPSP) in the 3 cell is blocked by bath applications of MeXCh and PTM A , which both abolish the response of the 3 cell to ACh (Elliott et al. 1992). It is concluded that the population of N1 cells are multiaction, premotor cholinergic interneurons.

Esophageal mechanoreceptors in the feeding system of the pond snail, Lymnaea stagnalis

1989 ◽  
Vol 61 (4) ◽  
pp. 727-736 ◽  
Author(s):  
C. J. Elliott ◽  
P. R. Benjamin
Keyword(s):  
Feeding Behavior ◽  
Synaptic Input ◽  
Lymnaea Stagnalis ◽  
Esophageal Wall ◽  
Pond Snail ◽  
Feeding System ◽  
Buccal Ganglia ◽  
Feeding Rhythm ◽  
Feeding Cycle ◽  
Stimulation Of

1. We identify esophageal mechanoreceptor (OM) neurons of Lymnaea with cell bodies in the buccal ganglia and axons that branch repeatedly to terminate in the esophageal wall. 2. The OM cells respond phasically to gut distension. Experiments with a high magnesium/low calcium solution suggest that the OM neurons are primary mechanoreceptors. 3. In the isolated CNS preparation, the OM cells receive little synaptic input during the feeding cycle. 4. The OM cells excite the motoneurons active in the rasp phase of the feeding cycle. 5. The OM cells inhibit each of the identified pattern-generating and modulatory interneurons in the buccal ganglia. Experiments with a saline rich in magnesium and calcium suggest that the connections are monosynaptic. 6. Stimulation of a single OM cell to fire at 5-15 Hz is sufficient to terminate the feeding rhythm in the isolated CNS preparation. 7. We conclude that these neurons play a role in terminating feeding behavior.

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