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

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.

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

1985 ◽  
Vol 54 (6) ◽  
pp. 1412-1421 ◽  
Author(s):  
C. J. Elliott ◽  
P. R. Benjamin
Keyword(s):  
Motor System ◽  
Lymnaea Stagnalis ◽  
Pond Snail ◽  
Excitatory Synapses ◽  
Feeding System ◽  
Buccal Ganglion ◽  
Buccal Ganglia ◽  
Feeding Rhythm ◽  
The Right ◽  
Stimulation Of

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.

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 .

Interneuronal Control of Feeding in the Pond Snail Lymnaea Stagnalis: II. The Interneuronal Mechanism Generating Feeding Cycles

1981 ◽  
Vol 92 (1) ◽  
pp. 203-228
Author(s):  
R. M. ROSE ◽  
P. R. BENJAMIN
Keyword(s):  
Cell Population ◽  
Synaptic Input ◽  
Lymnaea Stagnalis ◽  
Pond Snail ◽  
Feeding Cycle ◽  
Interneuronal Network

The feeding cycle of Lymnaea is generated by a network of three types of interneurone, N1, N2 and N3. This network is driven by the slow oscillator (SO) interneurone described in the previous paper. Interaction between the different interneurones is dependent on both connectivity and endogenous properties, and utilizes such properties as post-inhibitory rebound and self-feedback within electrically-coupled populations. Each of the four components of the interneuronal network (SO, N1, N2 and N3) is responsible for a different phase of synaptic input to the follower cell population which was previously shown to directly control feeding movements.

Electrophysiological and Behavioral Analysis of Lip Touch as a Component of the Food Stimulus in the SnailLymnaea

1999 ◽  
Vol 81 (3) ◽  
pp. 1261-1273 ◽  
Author(s):  
Kevin Staras ◽  
György Kemenes ◽  
Paul R. Benjamin
Keyword(s):  
Tactile Stimulus ◽  
Lymnaea Stagnalis ◽  
Video Recording ◽  
Conditioning Stimulus ◽  
Behavioral Analysis ◽  
Pond Snail ◽  
Food Stimulus ◽  
Synaptic Inputs ◽  
Feeding Cycle ◽  
Being Moved

Electrophysiological and behavioral analysis of lip touch as a component of the food stimulus in the snail Lymnaea. Electrophysiological and video recording methods were used to investigate the function of lip touch in feeding ingestion behavior of the pond snail Lymnaea stagnalis. Although this stimulus was used successfully as a conditioning stimulus (CS) in appetitive learning experiments, the detailed role of lip touch as a component of the sensory stimulus provided by food in unconditioned feeding behavior was never ascertained. Synaptic responses to lip touch in identified feeding motoneurons, central pattern generator interneurons, and modulatory interneurons were recorded by intracellular electrodes in a semi-intact preparation. We showed that touch evoked a complex but characteristic sequence of synaptic inputs on each neuron type. Touch never simply activated feeding cycles but provided different types of synaptic input, determined by the feeding phase in which the neuron was normally active in the rhythmic feeding cycle. The tactile stimulus evoked mainly inhibitory synaptic inputs in protraction-phase neurons and excitation in rasp-phase neurons. Swallow-phase neurons were also excited after some delay, suggesting that touch first reinforces the rasp then swallow phase. Video analysis of freely feeding animals demonstrated that during normal ingestion of a solid food flake the food is drawn across the lips throughout the rasp phase and swallow phase and therefore provides a tactile stimulus during both these retraction phases of the feeding cycle. The tactile component of the food stimulus is strongest during the rasp phase when the lips are actively pressed onto the substrate that is being moved across them by the radula. By using a semi-intact preparation we demonstrated that application of touch to the lips during the rasp phase of a sucrose-driven fictive feeding rhythm increases both the regularity and frequency of rasp-phase motoneuron firing compared with sucrose applied alone.

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.

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.

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

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.

scholarly journals Serotonergic regulation of the buccal (feeding) rhythm of the pond snail,Lymnaea stagnalis. An immunocytochemical, biochemical and pharmacological approach

2018 ◽  
Vol 69 (3) ◽  
pp. 225-243
Author(s):  
Károly Elekes ◽  
László Hiripi ◽  
Gábor Balog ◽  
Gábor Maász ◽  
Izabella Battonyai ◽  
...  
Keyword(s):  
Lymnaea Stagnalis ◽  
Pond Snail ◽  
Pharmacological Approach ◽  
Feeding Rhythm
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