Interactions of the slow oscillator interneuron with feeding pattern-generating interneurons in Lymnaea stagnalis

We have used intracellular recording from groups of interneurons in the feeding system of the pond snail, Lymnaea stagnalis, to examine the connections of a modulatory interneuron, the slow oscillator (SO), with the network of pattern-generating interneurons (N1, N2, and N3). The SO is an interneuron whose axon branches solely within the buccal ganglia. There is only one such cell in each snail. In half the snails the cell body is in the right buccal ganglion and in the other half in the left buccal ganglion. Stimulation of either the SO or one of the N1 pattern-generating interneurons elicits the feeding rhythm, but of all the buccal neurons, only the SO can drive the feeding rhythm at the frequency seen in the intact snail. The SO makes reciprocal excitatory synapses with the N1 interneurons that drive the protraction of the radula. This ensures strong activation of the feeding system. The SO inhibits the N2 interneurons. Postsynaptic potentials evoked by stimulation of the SO facilitate without spike broadening in the SO. The SO is strongly inhibited by N2 and N3 interneurons, which are active during the retraction phase. This gates any excitatory inputs to the SO, probably preventing protraction of the radula while retraction is underway. The results support the idea of a single interneuron capable of driving a hierarchically organized motor system.

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

Journal of Neurophysiology ◽

10.1152/jn.1989.61.4.727 ◽

1989 ◽

Vol 61 (4) ◽

pp. 727-736 ◽

Cited By ~ 43

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

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1992.0053 ◽

1992 ◽

Vol 336 (1277) ◽

pp. 157-166 ◽

Cited By ~ 19

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 .

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Interneuronal Control of Feeding in the Pond Snail Lymnaea Stagnalis: I. Initiation of Feeding Cycles by a Single Buccal Interneurone

Journal of Experimental Biology ◽

10.1242/jeb.92.1.187 ◽

1981 ◽

Vol 92 (1) ◽

pp. 187-201

Author(s):

R. M. ROSE ◽

P. R. BENJAMIN

Keyword(s):

Lymnaea Stagnalis ◽

Pond Snail ◽

Buccal Ganglion ◽

Synaptic Inputs ◽

Feeding Rhythm ◽

Interneuronal Network

The Lymnaea buccal ganglion is organized such that the basic feeding rhythm is generated by an interneuronal network which imposes its activity on a set of follower cells. In this paper we extend our earlier observations (Benjamin & Rose, 1979) on the follower cells to show that they receive four consecutive synaptic inputs. The main objective of the paper is to describe the properties of an interneurone called the ‘slow oscillator’ which is capable of initiating feeding cycles. This interneurone will be used in the following paper (Rose & Benjamin, 1981) to drive other members of the interneuronal network in order to determine how it is organized, and to understand the origin and timing of the four synaptic inputs to the follower cells.

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

Journal of Neurophysiology ◽

10.1152/jn.1995.73.1.112 ◽

1995 ◽

Vol 73 (1) ◽

pp. 112-124 ◽

Cited By ~ 31

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)

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Octopamine: a new feeding modulator in Lymnaea

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1998.0315 ◽

1998 ◽

Vol 353 (1375) ◽

pp. 1631-1643 ◽

Cited By ~ 21

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.

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Interactions of pattern-generating interneurons controlling feeding in Lymnaea stagnalis

Journal of Neurophysiology ◽

10.1152/jn.1985.54.6.1396 ◽

1985 ◽

Vol 54 (6) ◽

pp. 1396-1411 ◽

Cited By ~ 77

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.

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

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1992.0055 ◽

1992 ◽

Vol 336 (1277) ◽

pp. 181-189 ◽

Cited By ~ 5

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.

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Central Coordination of Buccal and Pedal Neuronal Activity in the Pond Snail Lymnaea Stagnalis

Journal of Experimental Biology ◽

10.1242/jeb.136.1.103 ◽

1988 ◽

Vol 136 (1) ◽

pp. 103-123

Author(s):

M. A. KYRIAKIDES ◽

C. R. MCCROHAN

Keyword(s):

Central Pattern Generator ◽

Body Wall ◽

Lymnaea Stagnalis ◽

Pattern Generator ◽

Pond Snail ◽

Buccal Ganglion ◽

Buccal Ganglia ◽

Feeding Cycle ◽

Central Coordination

Cyclical synaptic inputs were recorded from identified giant neurones and neuronal cluster cells in the pedal ganglia of Lymnaea stagnalis. They occurred in phase with rhythmical inputs to buccal ganglion motoneurones, which have been shown to originate from interneurones of the buccal central pattern generator for feeding. In pedal neurones, the cyclical inputs were mainly inhibitory, and occurred predominantly during the radula retraction phase of the feeding cycle. Tonic depolarization of higher-order interneurones in the feeding system, to activate the buccal central pattern generator, led to the onset of cyclical inputs to pedal neurones. These inputs were abolished after cutting the cerebrobuccal connectives, supporting the hypothesis that they originate from the buccal ganglia. The possible role of these inputs in coordinating foot and body wall movements with the buccal feeding rhythm is discussed.

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Control of feeding motor output by paracerebral neurons in brain of Pleurobranchaea californica

Journal of Neurophysiology ◽

10.1152/jn.1982.47.5.885 ◽

1982 ◽

Vol 47 (5) ◽

pp. 885-908 ◽

Cited By ~ 52

Author(s):

R. Gillette ◽

M. P. Kovac ◽

W. J. Davis

Keyword(s):

Feeding Behavior ◽

Action Potentials ◽

Tactile Stimulation ◽

Natural Food ◽

Buccal Ganglion ◽

Pleurobranchaea Californica ◽

Feeding Rhythm ◽

Intracellular Stimulation ◽

Motor Rhythm ◽

Stimulation Of

1. A population of interneurons that control feeding behavior in the mollusk Pleurobranchaea has been analyzed by dye injection and intracellular stimulation/recording in whole animals and reduced preparations. The population consists of 12-16 somata distributed in two bilaterally symmetrical groups on the anterior edge of the cerebropleural ganglion (brain). On the basis of their position adjacent to the cerebral lobes, these cells have been named paracerebral neurons (PCNs). This study concerns pme subset pf [MCs. the large, phasic ones, which have the strongest effect on the feeding rhythm (21). 2. Each PCN sends a descending axon via the ipsilateral cerebrobuccal connective to the buccal ganglion. Axon branches have not been detected in other brain or buccal nerves and hence the PCNs appear to be interneurons. 3. In whole-animal preparations, tonic intracellular depolarization of the PNCs causes them to discharge cyclic bursts of action potentials interrupted by a characteristic hyperpolarization. In all specimens that exhibit feeding behavior, the interburst hyperpolarization is invariably accompanied by radula closure and the beginning of proboscis retraction (the "bite"). No other behavorial effect of PCN stimulation has been observed. 4. In whole-animal preparations, the PCNs are excited by food and tactile stimulation of the oral veil, rhinophores, and tentacles. When such stimuli induce feeding the PCNs discharge in the same bursting pattern seen during tonic PCN depolarization, with the cyclic interburst hyperpolarization phase locked to the bit. When specimens egest an unpalatable object by cyclic buccal movements, however, the PCNs are silent. The PCNs therefore exhibit properties expected of behaviorally specific "command" neurons for feeding. 5. Silencing one or two PCNs by hyperpolarization may weaken but does not prevent feeding induced by natural food stimuli. Single PCNs therefore can be sufficient but are not necessary to induction of feeding behavior. Instead the PCNs presumably operate as a population to control feeding. 6. In isolated nervous system preparations tonic extracellular stimulation of the stomatogastric nerve of the buccal ganglion elicits a cyclic motor rhythm that is similar in general features to the PNC-induced motor rhythm. Bursts of PCN action potentials intercalated at the normal phase position in this cycle intensify the buccal rhythm. Bursts of PCN impulses intercalated at abnormal phase positions reset the buccal rhythm. The PCNs, therefore, also exhibit properties expected of pattern-generator elements and/or coordinating neurons for the buccal rhythm. 7. The PCNs are recruited into activity when the buccal motor rhythm is elicited by stomatogastric nerve stimulation or stimulation of the reidentifiable ventral white cell. The functional synergy between the PCNs and the buccal rhythm is therefore reciprocal. 8...

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