Central Generation of Bursting in the Feeding System of the Snail, Lymnaea Stagnalis

1979 ◽  
Vol 80 (1) ◽  
pp. 93-118 ◽  
Author(s):  
P. R. BENJAMIN ◽  
R. M. ROSE

The central generation of burst activity was investigated in the buccal ganglia of Lymnaea. Eight different patterns of burst activity were generated by one or two consecutive phases of compound synaptic potentials resulting from activity of neurones outside the population of recorded neurones. These inputs acted upon the different endogenous properties of buccal neurones such as post-inhibitory rebound and spike adaptation. Effects of synaptic inputs were reinforced by electrotonic coupling of some buccal neurones of the same type.

1980 ◽  
Vol 85 (1) ◽  
pp. 169-186
Author(s):  
C. R. McCrohan ◽  
P. R. Benjamin

1.The cerebral giant cells (CGCs) of Lymnaea have a tonic, modulatory effect on the intensity of output from feeding motoneurones in the buccal ganglia. 2. Short latency, excitatory and probably monosynaptic connexions occur between the CGCs and three identified feeding motoneurones. Unitary excitatory postsynaptic potentials in these motoneurones, following CGC spikes, are of different sizes and durations, and hence have different summation properties. 3. The CGCs make long latency, excitatory polysynaptic connexions with four other feeding motoneurone types. 4. Bursts of spikes in the CGCs, resulting from phasic synaptic input, synchronous with the feeding cycle, amplify their modulatory effect on burst intensity in feeding motoneurones. 5. Thte for reinforcing their cyclic burst activity.


1995 ◽  
Vol 73 (1) ◽  
pp. 112-124 ◽  
Author(s):  
M. S. Yeoman ◽  
A. Vehovszky ◽  
G. Kemenes ◽  
C. J. Elliott ◽  
P. R. Benjamin

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)


1984 ◽  
Vol 108 (1) ◽  
pp. 257-272
Author(s):  
C. R. MCCROHAN

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.


1989 ◽  
Vol 61 (4) ◽  
pp. 727-736 ◽  
Author(s):  
C. J. Elliott ◽  
P. R. Benjamin

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.


1984 ◽  
Vol 113 (1) ◽  
pp. 351-366
Author(s):  
C. R. MCCROHAN

1. The cerebral ventral 1 (CV1) cells of Lymnaea are located in the cerebral ganglia, and have axonal projections to the buccal ganglia. 2. Maintained depolarization of a CV1 neurone leads to initiation, maintenance and modulation of rhythmic feeding motor output from buccal and cerebral ganglia. 3. The CV1 cells receive rhythmic synaptic inputs, in phase with feeding cycles, which probably originate from buccal rhythm-generating interneurones. 4. CV1 cells initiate feeding cycles independently of the buccal slow oscillator (SO) neurone, previously described. The possible roles of CV1 and SO are discussed.


1985 ◽  
Vol 54 (6) ◽  
pp. 1412-1421 ◽  
Author(s):  
C. J. Elliott ◽  
P. R. Benjamin

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.


1992 ◽  
Vol 336 (1277) ◽  
pp. 157-166 ◽  

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 .


1972 ◽  
Vol 56 (3) ◽  
pp. 621-637
Author(s):  
MICHAEL S. BERRY

1. The buccal ganglia of Planorbis contain a population of electrically coupled small cells. This has been studied, in preparations of isolated ganglia, by recording intracellularly from the cells two at a time. 2. The population is usually silent but activity initiated in any one of its members tends to spread to the rest of the population in both ganglia. Failure of spread, or fatigue, gradually occurs on repetition. 3. The group has the properties of a trigger system, initiating prolonged patterned activity in large numbers of neurones in the buccal ganglia. This may normally initiate feeding. 4. In addition to central processes, both in the buccal ganglia and to the rest of the CNS, the system has peripheral axons in most of the buccal nerves. No synaptic input could be demonstrated. 5. Action potentials in some of the cells increase greatly in duration with repetition. The resulting electrotonic EPSP's, recorded in closely coupled trigger cells, correspondingly increase in size. The possible integrative significance of this is discussed, especially its effect in offsetting fatigue. 6. In some preparations spontaneous bursting occurred in trigger cells and this elicited burst activity in large neurones, including motoneurones. The system may have an intrinsic pacemaker.


1981 ◽  
Vol 92 (1) ◽  
pp. 187-201
Author(s):  
R. M. ROSE ◽  
P. R. BENJAMIN

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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