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

M. S. Yeoman, A. Vehovszky, G. Kemenes, C. J H Elliott, P. R. Benjamin

Research output: Contribution to journalArticle

42 Citations (Scopus)

Abstract

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 semiintact 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. The N1L in turn was inhibited strongly by the N2, N3p, and N3t interneurons. These synaptic connections with other CPG interneurons were necessary for fictive feeding to occur. For instance, suppressing N1L activity in a food-driven rhythm in a semiintact preparation stopped activity in the whole CPG network. Similar experiments where activity in the modulatory SO was suppressed merely slowed the rhythm. 9. The N1L has a limited set of connections with the buccal motor neurons. It only excited the B1 salivary gland motor neuron and inhibited the B4 retractor motor neuron, making it similar to the SO modulatory interneuron, but different from the N1M cells that have widespread connections with all 10 previously described types of motor neurons. 10. The data shows that the N1Ls have some properties that resemble a modulatory neuron such as the SO, but their cells also form part of the CPG network. They are thus a hybrid cell type that is normally activated in parallel with the SO and CPG neurons (N1M, N2, N3p, and N3t) to generate the Lymnaea feeding rhythm.

Original languageEnglish
Pages (from-to)112-124
Number of pages13
JournalJournal of Neurophysiology
Volume73
Issue number1
Publication statusPublished - 1995

Fingerprint

Central Pattern Generators
Lymnaea
Snails
Interneurons
Cheek
Motor Neurons
Excitatory Postsynaptic Potentials
Lip
Neurons
Ganglia
Neuropil
Hybrid Cells
Neurites
Salivary Glands
Axons
Sucrose
Food
Injections

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Novel interneuron having hybrid modulatory-central pattern generator properties in the feeding system of the snail, Lymnaea stagnalis. / Yeoman, M. S.; Vehovszky, A.; Kemenes, G.; Elliott, C. J H; Benjamin, P. R.

In: Journal of Neurophysiology, Vol. 73, No. 1, 1995, p. 112-124.

Research output: Contribution to journalArticle

@article{9d3dd098d6eb4eee8b9719a53dbde0b6,
title = "Novel interneuron having hybrid modulatory-central pattern generator properties in the feeding system of the snail, Lymnaea stagnalis",
abstract = "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 semiintact 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. The N1L in turn was inhibited strongly by the N2, N3p, and N3t interneurons. These synaptic connections with other CPG interneurons were necessary for fictive feeding to occur. For instance, suppressing N1L activity in a food-driven rhythm in a semiintact preparation stopped activity in the whole CPG network. Similar experiments where activity in the modulatory SO was suppressed merely slowed the rhythm. 9. The N1L has a limited set of connections with the buccal motor neurons. It only excited the B1 salivary gland motor neuron and inhibited the B4 retractor motor neuron, making it similar to the SO modulatory interneuron, but different from the N1M cells that have widespread connections with all 10 previously described types of motor neurons. 10. The data shows that the N1Ls have some properties that resemble a modulatory neuron such as the SO, but their cells also form part of the CPG network. They are thus a hybrid cell type that is normally activated in parallel with the SO and CPG neurons (N1M, N2, N3p, and N3t) to generate the Lymnaea feeding rhythm.",
author = "Yeoman, {M. S.} and A. Vehovszky and G. Kemenes and Elliott, {C. J H} and Benjamin, {P. R.}",
year = "1995",
language = "English",
volume = "73",
pages = "112--124",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "1",

}

TY - JOUR

T1 - Novel interneuron having hybrid modulatory-central pattern generator properties in the feeding system of the snail, Lymnaea stagnalis

AU - Yeoman, M. S.

AU - Vehovszky, A.

AU - Kemenes, G.

AU - Elliott, C. J H

AU - Benjamin, P. R.

PY - 1995

Y1 - 1995

N2 - 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 semiintact 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. The N1L in turn was inhibited strongly by the N2, N3p, and N3t interneurons. These synaptic connections with other CPG interneurons were necessary for fictive feeding to occur. For instance, suppressing N1L activity in a food-driven rhythm in a semiintact preparation stopped activity in the whole CPG network. Similar experiments where activity in the modulatory SO was suppressed merely slowed the rhythm. 9. The N1L has a limited set of connections with the buccal motor neurons. It only excited the B1 salivary gland motor neuron and inhibited the B4 retractor motor neuron, making it similar to the SO modulatory interneuron, but different from the N1M cells that have widespread connections with all 10 previously described types of motor neurons. 10. The data shows that the N1Ls have some properties that resemble a modulatory neuron such as the SO, but their cells also form part of the CPG network. They are thus a hybrid cell type that is normally activated in parallel with the SO and CPG neurons (N1M, N2, N3p, and N3t) to generate the Lymnaea feeding rhythm.

AB - 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 semiintact 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. The N1L in turn was inhibited strongly by the N2, N3p, and N3t interneurons. These synaptic connections with other CPG interneurons were necessary for fictive feeding to occur. For instance, suppressing N1L activity in a food-driven rhythm in a semiintact preparation stopped activity in the whole CPG network. Similar experiments where activity in the modulatory SO was suppressed merely slowed the rhythm. 9. The N1L has a limited set of connections with the buccal motor neurons. It only excited the B1 salivary gland motor neuron and inhibited the B4 retractor motor neuron, making it similar to the SO modulatory interneuron, but different from the N1M cells that have widespread connections with all 10 previously described types of motor neurons. 10. The data shows that the N1Ls have some properties that resemble a modulatory neuron such as the SO, but their cells also form part of the CPG network. They are thus a hybrid cell type that is normally activated in parallel with the SO and CPG neurons (N1M, N2, N3p, and N3t) to generate the Lymnaea feeding rhythm.

UR - http://www.scopus.com/inward/record.url?scp=0028887448&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0028887448&partnerID=8YFLogxK

M3 - Article

VL - 73

SP - 112

EP - 124

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 1

ER -