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.

Behavior-Dependent Activities of a Central Pattern Generator in Freely Behaving Lymnaea stagnalis

1997 ◽  
Vol 78 (6) ◽  
pp. 3415-3427 ◽  
Author(s):  
Rene F. Jansen ◽  
Anton W. Pieneman ◽  
Andries ter Maat
Keyword(s):  
Electrical Activity ◽  
Central Pattern Generator ◽  
Lymnaea Stagnalis ◽  
Central Pattern Generators ◽  
Pattern Generator ◽  
Egg Laying ◽  
Buccal Ganglion ◽  
Level Of Activity ◽  
Freely Behaving ◽  
Pattern Generators

Jansen, Rene F., Anton W. Pieneman, and Andries ter Maat. Behavior-dependent activities of a central pattern generator in freely behaving Lymnaea stagnalis. J. Neurophysiol. 78: 3415–3427, 1997. Cyclic or repeated movements are thought to be driven by networks of neurons (central pattern generators) that are dynamic in their connectivity. During two unrelated behaviors (feeding and egg laying), we investigated the behavioral output of the buccal pattern generator as well as the electrical activity of a pair of identified interneurons that have been shown to be involved in setting the level of activity of this pattern generator (PG). Analysis of the quantile plots of the parameters that describe the behavior (movements of the buccal mass) reveals that during egg laying, the behavioral output of the PG is different compared with that during feeding. Comparison of the average durations of the different parts of the buccal movements showed that during egg laying, the duration of one specific part of buccal movement is increased. Correlated with these changes in the behavioral output of the PG were changes in the firing rate of the cerebral giant neurons (CGC), a pair of interneurons that have been shown to modulate the activity of the PG by means of multiple synaptic contacts with neurons in the buccal ganglion. Interval- and autocorrelation histograms of the behavioral output and CGC spiking show that both the PG output and the spiking properties of the CGCs are different when comparing egg-laying animals with feeding animals. Analysis of the timing relations between the CGCs and the behavioral output of the PG showed that both during feeding and egg laying, the electrical activity of the CGCs is largely in phase with the PG output, although small changes occur. We discuss how these results lead to specific predictions about the kinds of changes that are likely to occur when the animal switches the PG from feeding to egg laying and how the hormones that cause egg laying are likely to be involved.

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)

Behavioural and network plasticity following conditioning of the aerial respiratory response of a pulmonate mollusc

2013 ◽  
Vol 91 (6) ◽  
pp. 382-390 ◽  
Author(s):  
G.E. Spencer ◽  
C.M. Rothwell
Keyword(s):  
Central Pattern Generator ◽  
Neuronal Network ◽  
Conditioned Response ◽  
Lymnaea Stagnalis ◽  
Pattern Generator ◽  
Pond Snail ◽  
Respiratory Response ◽  
Surrounding Atmosphere ◽  
Network Plasticity ◽  
Pulmonary Respiration

Most molluscs perform respiration using gills, but the pulmonate molluscs have developed a primitive lung with which they perform pulmonary respiration. The flow of air into this lung occurs through an opening called the pneumostome, and pulmonate molluscs travel to the surface of the water to obtain oxygen from the surrounding atmosphere. The aerial respiratory behaviour of the pulmonate mollusc, the great pond snail (Lymnaea stagnalis (L., 1758)), has been well studied, and a three-neuron central pattern generator (CPG) controlling this rhythmic behaviour has been identified. The aerial respiratory behaviour of L. stagnalis can be operantly conditioned and plasticity within the CPG has been associated with the conditioned response. In this review, we describe both the aerial respiratory behaviour and the underlying neuronal network of this pulmonate mollusc, and then discuss both the behavioural and network plasticity that results from the conditioning of this behaviour.

Cerebral Interneurones Controlling Feeding Motor Output In The Snail Lymnaea Stagnalis

1989 ◽  
Vol 147 (1) ◽  
pp. 361-374
Author(s):  
CATHERINE R. McCROHAN ◽  
MICHAEL A. KYRIAKIDES
Keyword(s):  
Central Pattern Generator ◽  
Lymnaea Stagnalis ◽  
Pattern Generator ◽  
Motor Output ◽  
Excitatory Postsynaptic Potentials ◽  
Gastropod Species ◽  
Postsynaptic Potentials ◽  
Inhibitory Postsynaptic Potentials ◽  
Buccal Ganglia

1. The cerebral ventral 1 (CV1) interneurones of Lymnaea occurred as a population of at least three in each ganglion, all with similar morphologies. Steady depolarization of a CV1 cell led to initiation and maintenance of rhythmic feeding motor output from the buccal ganglia. 2. CV1 interneurones produced facilitating excitatory postsynaptic potentials in Nl interneurones of the buccal central pattern generator for feeding. Connections with N2 interneurones were not found. 3. The CV1 population could be separated into two subgroups. CVla received strong synaptic feedback in phase with the buccal rhythm, leading to strong bursting during generation of feeding motor output. CVlb received only weak feedback, and often fired continuously when depolarized. 4. Unitary inhibitory postsynaptic potentials were characteristic of all CV1 neurones, but were only visible in CVlb when it was depolarized. These inputs are thought to arise indirectly from the buccal central pattern generator. 5. The CV1 population is probably homologous with similar neurones in other gastropod species.

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.

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.

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.

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.

Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurones

1991 ◽  
Vol 158 (1) ◽  
pp. 37-62 ◽  
Author(s):  
N. I. Syed ◽  
W. Winlow
Keyword(s):  
Body Wall ◽  
Lymnaea Stagnalis ◽  
The Body ◽  
Whole Body ◽  
Pond Snail ◽  
Selective Ablation ◽  
The Central Nervous System ◽  
Body Wall Muscles ◽  
Bilateral Pair ◽  
Left And Right

1. The morphology and electrophysiology of a newly identified bilateral pair of interneurones in the central nervous system of the pulmonate pond snail Lymnaea stagnalis is described. 2. These interneurones, identified as left and right pedal dorsal 11 (L/RPeD11), are electrically coupled to each other as well as to a large number of foot and body wall motoneurones, forming a fast-acting neural network which coordinates the activities of foot and body wall muscles. 3. The left and right sides of the body wall of Lymnaea are innervated by left and right cerebral A cluster neurones. Although these motoneurones have only ipsilateral projections, they are indirectly electrically coupled to their contralateral homologues via their connections with L/RPeD11. Similarly, the activities of left and right pedal G cluster neurones, which are known to be involved in locomotion, are also coordinated by L/RPeD11. 4. Selective ablation of both neurones PeD11 results in the loss of coordination between the bilateral cerebral A clusters. 5. Interneurones L/RPeD11 are multifunctional. In addition to coordinating motoneuronal activity, they make chemical excitatory connections with heart motoneurones. They also synapse upon respiratory motoneurones, hyperpolarizing those involved in pneumostome opening (expiration) and depolarizing those involved in pneumostome closure (inspiration). 6. An identified respiratory interneurone involved in pneumostome closure (visceral dorsal 4) inhibits L/RPeD11 together with all their electrically coupled follower cells. 7. Both L/RPeD11 have strong excitatory effects on another pair of electrically coupled neurones, visceral dorsal 1 and right parietal dorsal 2, which have previously been shown to be sensitive to changes in the partial pressure of environmental oxygen (PO2). 8. Although L/RPeD11 participate in whole-body withdrawal responses, electrical stimulation applied directly to these neurones was not sufficient to induce this behaviour.

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