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

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.

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.


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 .


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.


1983 ◽  
Vol 49 (6) ◽  
pp. 1392-1409 ◽  
Author(s):  
A. ter Maat ◽  
E. W. Roubos ◽  
J. C. Lodder ◽  
P. Buma

The ovulation hormone-producing caudodorsal cells (CDCs) of the pond snail Lymnaea stagnalis form two clusters of electrotonically coupled cells, each containing a few specialized (ventral) cells that connect the clusters. The hormone is secreted during a pacemaker-driven discharge. The CDCs receive a biphasic cholinergic postsynaptic potential (PSP), consisting of a rapid excitatory postsynaptic potential (EPSP) and a slow inhibitory postsynaptic potential (IPSP) that is elicited by stimulation of nerves. The effect of the synaptic input on the discharge of the CDCs is described and the location of the synapse investigated by a combination of electrophysiological recordings and morphological techniques. The PSP interrupts the discharge and hastens its termination. In addition, it causes a reversal of the temporal order of the spikes of ventral cells (that normally lead) and dorsal cells (that lead only after the PSP). Ion-substitution experiments indicate that the ionic mechanism underlying the biphasic PSP is conventional, involving a conductance increase for Na+ (EPSP) and K+ (IPSP). Receptors mediating the inhibitory component occur only on the proximal axons of the ventral cells, both components are larger and reverse more readily in ventral cells. These findings suggest that the PSP is generated in the ventral cells. The biphasic PSP has no effect on electrical coupling, suggesting that it is not generated along the electrical pathways among the cells. Horseradish peroxidase (HRP) staining reveals that the lateral branches emerge from the proximal axons of the ventral cells only. In HRP-filled preparations processed for electron microscopy (EM) acetylcholinesterase is demonstrated at these branches where it occurs associated with synapses. The location on fine branches of the ventral cells explains the absence of an effect on electrotonic transmission, whereas the reluctance of components of the PSP to reverse at the expected potentials is due to the distribution of the synapses over more than one cell. It is concluded that the biphasic PSP is received only by the ventral cells and that it is conveyed electrotonically to the other cells.


1999 ◽  
Vol 81 (3) ◽  
pp. 1261-1273 ◽  
Author(s):  
Kevin Staras ◽  
György Kemenes ◽  
Paul R. Benjamin

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.


1988 ◽  
Vol 136 (1) ◽  
pp. 103-123
Author(s):  
M. A. KYRIAKIDES ◽  
C. R. MCCROHAN

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.


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.


2021 ◽  
Vol 1 (1) ◽  
Author(s):  
Nicolas Cerveau ◽  
Daniel John Jackson

AbstractMicroRNAs (miRNAs) are a deeply conserved class of small, single stranded RNA molecules that post-transcriptionally regulate mRNA levels via several targeted degradation pathways. They are involved in a wide variety of biological processes and have been used to infer the deep evolutionary relationships of major groups such as the Metazoa. Here we have surveyed several adult tissues of the freshwater pulmonate Lymnaea stagnalis (the Great Pond Snail) for miRNAs. In addition we perform a shell regeneration assay to identify miRNAs that may be involved in regulating mRNAs directly involved in the shell-forming process. From seven mature tissues we identify a total of 370 unique precursor miRNAs that give rise to 336 unique mature miRNAs. While the majority of these appear to be evolutionarily novel, most of the 70 most highly expressed (which account for 99.8% of all reads) share sequence similarity with a miRBase or mirGeneDB2.0 entry. We also identify 10 miRNAs that are differentially regulated in mantle tissue that is actively regenerating shell material, 5 of which appear to be evolutionarily novel and none of which share similarity with any miRNA previously reported to regulate biomineralization in molluscs. One significantly down-regulated miRNA is predicted to target Lst-Dermatopontin, a previously characterized shell matrix protein from another freshwater gastropod. This survey provides a foundation for future studies that would seek to characterize the functional role of these molecules in biomineralization or other processes of interest.


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