Transforming Tonic Firing Into a Rhythmic Output in the Aplysia Feeding System: Presynaptic Inhibition of a Command-Like Neuron by a CPG Element

2005 ◽  
Vol 93 (2) ◽  
pp. 829-842 ◽  
Author(s):  
Itay Hurwitz ◽  
Abraham J. Susswein ◽  
Klaudiusz R. Weiss
Keyword(s):  
Presynaptic Inhibition ◽  
Neural Circuit ◽  
Feeding System ◽  
Rhythmic Movements ◽  
Postsynaptic Inhibition ◽  
Buccal Ganglion ◽  
Tonic Firing ◽  
Buccal Ganglia ◽  
Identified Neuron ◽  
Protraction Phase

Tonic stimuli can elicit rhythmic responses. The neural circuit underlying Aplysia californica consummatory feeding was used to examine how a maintained stimulus elicits repetitive, rhythmic movements. The command-like cerebral-buccal interneuron 2 (CBI-2) is excited by tonic food stimuli but initiates rhythmic consummatory responses by exciting only protraction-phase neurons, which then excite retraction-phase neurons after a delay. CBI-2 is inhibited during retraction, generally preventing it from exciting protraction-phase neurons during retraction. We have found that depolarizing CBI-2 during retraction overcomes the inhibition and causes CBI-2 to fire, potentially leading CBI-2 to excite protraction-phase neurons during retraction. However, CBI-2 synaptic outputs to protraction-phase neurons were blocked during retraction, thereby preventing excitation during retraction. The block was caused by presynaptic inhibition of CBI-2 by a key buccal ganglion retraction-phase interneuron, B64, which also causes postsynaptic inhibition of protraction-phase neurons. Pre- and postsynaptic inhibition could be separated. First, only presynaptic inhibition affected facilitation of excitatory postsynaptic potentials (EPSPs) from CBI-2 to its followers. Second, a newly identified neuron, B54, produced postsynaptic inhibition similar to that of B64 but did not cause presynaptic inhibition. Third, in some target neurons B64 produced only presynaptic but not postsynaptic inhibition. Blocking CBI-2 transmitter release in the buccal ganglia during retraction functions to prevent CBI-2 from driving protraction-phase neurons during retraction and regulates the facilitation of the CBI-2 induced EPSPs in protraction-phase neurons.

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.

Synaptic Actions of Oesophageal Proprioceptors in the Mollusc, Philine

1981 ◽  
Vol 94 (1) ◽  
pp. 95-104
Author(s):  
J. N. SIGGER ◽  
D. A. DORSETT
Keyword(s):  
Receptive Fields ◽  
Large Cell ◽  
The Other ◽  
Small Cells ◽  
Sensory Cells ◽  
Periodic Activity ◽  
Buccal Ganglia ◽  
Excitatory Synaptic Input ◽  
Feeding Cycle ◽  
Protraction Phase

The buccal ganglia of Philine each contain a group of mechanoreceptors, consisting of 1 large and 3 small cells, with receptive fields in the oesophagus. Synaptic contacts occur between the receptors; the large cell providing an EIPSP input to its contralateral partner and to the two groups of smaller receptors. The small receptors make weak excitatory contacts with both the large receptors. The sensory cells synapse with other buccal motoneurones and interneurones, some of which show periodic activity associated with the feeding movements. Protraction phase neurones are divisible into two groups, one of which receives EPSPs from the receptors, while the other group receives IPSPs. Retraction phase neurones receive a biphasic EIPSP. The receptors provide excitatory synaptic input to a pair of interneurones which ‘gate’ the feeding cycle. A third class of neurones which are not rhythmically active during feeding receive a predominantly inhibitory EIPSP.

The Integration of the Patterned Output of Buccal Motoneurones During Feeding in Tritonia Hombergi

1979 ◽  
Vol 79 (1) ◽  
pp. 23-40
Author(s):  
A.G. M. BULLOCH ◽  
D. A. DORSETT
Keyword(s):  
Feeding Activity ◽  
Electrical Coupling ◽  
Cell Activity ◽  
Giant Cells ◽  
Posterior Border ◽  
Buccal Ganglion ◽  
Synaptic Inputs ◽  
Proprioceptive Input ◽  
Buccal Ganglia ◽  
Feeding Cycle

Three phases of activity may be recognized in the buccal mass of Tritonia hombergi during the feeding cycle. These have been termed Protraction, Retraction and Flattening. Each phase is driven by a group of motoneurones along the posterior border of the buccal ganglia. The patterned bursting observed in the motoneurone groups during feeding activity is phased by synaptic inputs which are common to two or more groups. Evidence is presented which indicates these inputs are derived from three unidentified multi-action interneurone sources within each buccal ganglion, and whose action primarily determines the patterned output of the motoneurones. Electrical coupling between between synergistic motoneurones and, in one case, post-inhibitory rebound, contribute to the synchronization of group activity. Proprioceptive input to the motoneurones was not identified, but may project to the interneurones. Some small neurones having synaptic inputs on the motoneurones appropriate to two of the interneurones were found, but require confirmation in this role. The cerebral giant cells synapse on representatives of three motoneurone groups, and also activate the buccal interneurones driving the feeding cycle. The patterned activity of the motoneurones can occur in the absence of cerebral cell activity.

Modulation of Fictive Feeding by Dopamine and Serotonin inAplysia

2000 ◽  
Vol 83 (1) ◽  
pp. 374-392 ◽  
Author(s):  
Evgeni A. Kabotyanski ◽  
Douglas A. Baxter ◽  
Susan J. Cushman ◽  
John H. Byrne
Keyword(s):  
Feeding Activity ◽  
Neural Correlates ◽  
Neural Circuitry ◽  
Pattern Generator ◽  
Synaptic Connections ◽  
Rhythmic Movements ◽  
Motor Programs ◽  
Dopaminergic Cells ◽  
Buccal Ganglia ◽  
Bath Application

The buccal ganglia of Aplysia contain a central pattern generator (CPG) that mediates rhythmic movements of the buccal apparatus during feeding. Activity in this CPG is believed to be regulated, in part, by extrinsic serotonergic inputs and by an intrinsic and extrinsic system of putative dopaminergic cells. The present study investigated the roles of dopamine (DA) and serotonin (5-HT) in regulating feeding movements of the buccal apparatus and properties of the underlying neural circuitry. Perfusing a semi-intact head preparation with DA (50 μM) or the metabolic precursor of catecholamines (l-3–4-dihydroxyphenylalanine, DOPA, 250 μM) induced feeding-like movements of the jaws and radula/odontophore. These DA-induced movements were similar to bites in intact animals. Perfusing with 5-HT (5 μM) also induced feeding-like movements, but the 5-HT-induced movements were similar to swallows. In preparations of isolated buccal ganglia, buccal motor programs (BMPs) that represented at least two different aspects of fictive feeding (i.e., ingestion and rejection) could be recorded. Bath application of DA (50 μM) increased the frequency of BMPs, in part, by increasing the number of ingestion-like BMPs. Bath application of 5-HT (5 μM) did not significantly increase the frequency of BMPs nor did it significantly increase the proportion of ingestion-like BMPs being expressed. Many of the cells and synaptic connections within the CPG appeared to be modulated by DA or 5-HT. For example, bath application of DA decreased the excitability of cells B4/5 and B34, which in turn may have contributed to the DA-induced increase in ingestion-like BMPs. In summary, bite-like movements were induced by DA in the semi-intact preparation, and neural correlates of these DA-induced effects were manifest as an increase in ingestion-like BMPs in the isolated ganglia. Swallow-like movements were induced by 5-HT in the semi-intact preparation. Neural correlates of these 5-HT-induced effects were not evident in isolated buccal ganglia, however.

Control of extrinsic feeding muscles in Aplysia

1983 ◽  
Vol 49 (6) ◽  
pp. 1481-1503 ◽  
Author(s):  
B. Jahan-Parwar ◽  
S. M. Fredman
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Synaptic Input ◽  
Cerebral Ganglion ◽  
Cyclic Activity ◽  
Buccal Mass ◽  
Buccal Ganglia ◽  
Identified Neuron ◽  
Single Oscillator ◽  
Extrinsic Muscles

The extrinsic buccal muscles in Aplysia are responsible for the overall protraction and retraction of the buccal mass during feeding. The six pairs of extrinsic muscles are organized into two groups, consisting of three protractors and three retractors. Insights into how the extrinsic muscles are controlled were obtained by examining the organization of the motor neurons that innervated them. The extrinsic buccal muscles are innervated by cerebral ganglion nerves and neurons. All the muscles examined appear to be multiply innervated. Identified neurons in the cerebral B, E, and G clusters were found to be motor neurons for individual extrinsic muscles. Some extrinsic muscles had both excitatory and inhibitory innervation. Two synergistic muscles, the extrinsic ventrolateral protractor (ExVLP) and the extrinsic dorsal protractor (ExDP), had common excitatory innervation by identified neuron E5. Two antagonistic muscles, the ExVLP and the extrinsic ventral retractor (ExVR), also had common innervation. Identified neuron E1 appeared to be an inhibitory motor neuron for the ExVLP but an excitatory motor neuron for the ExVR. Common innervation provides a simple mechanism for coordinating synergistic and antagonistic extrinsic muscles. On the basis of these data, a model for the control of buccal mass protraction and retraction is proposed. Bursting by extrinsic buccal muscles was coordinated with cyclic activity in the intrinsic muscles of the buccal mass. Antagonistic extrinsic muscles burst antiphasically and synergistic extrinsic muscles burst in phase when the buccal mass was fully protracted and exhibited a series of rhythmic contractions. Additionally, cerebral E cluster neurons burst in phase with stereotyped rhythmic buccal motor neuron discharges recorded from buccal nerves. The cerebral E cluster motor neurons were coordinated by common synaptic input. No monosynaptic connections were observed; homologous neurons in each E cluster received synaptic input with similar but not identical timing, indicating that the interneurons that coordinate the homologous motor neurons are synchronized. The source of the rhythm that drives synaptically mediated cerebral extrinsic muscle motor neuron bursting was in the buccal ganglia. Cutting one cerebral-buccal connective eliminated E neuron bursting on that side but had no effect on homologous neurons on the intact side. This suggests that a single oscillator in the buccal ganglia may coordinate both the extrinsic and intrinsic buccal muscles during feeding.

Synaptic Modulation Contributes to Firing Pattern Generation in Jaw Motor Neurons During Rejection of Seaweed in Aplysia kurodai

1999 ◽  
Vol 82 (5) ◽  
pp. 2579-2589 ◽  
Author(s):  
Tatsumi Nagahama ◽  
Kenji Narusuye ◽  
Hidekazu Arai
Keyword(s):  
Motor Neurons ◽  
Firing Frequency ◽  
Pattern Generation ◽  
Jaw Movements ◽  
Japanese Species ◽  
Initial Portion ◽  
Synaptic Modulation ◽  
Buccal Ganglia ◽  
Cerebral Neurons ◽  
Protraction Phase

Japanese species, Aplysia kurodai, feeds well on Ulva but rejects Gelidium ( Geli.) or Pachydictyon ( Pach.) with different rhythmic patterned movements of the jaws and radula. During ingestion the jaws open at the radula-protraction phase and remain half open at the initial phase of the radula-retraction, whereas during rejection the jaws open similarly but start to close immediately after the onset of the radula-retraction. These can be induced not only by the natural seaweed but by the extract solutions. We previously showed that the change of the patterned jaw movements from the ingestion to the rejection may result from the decrease in the delay of the firing onset of the jaw-closing (JC) motor neurons during their depolarization. This diminished delay produces a phase advance relative to the radula-retraction phase. In that study, we showed that during ingestion the buccal multiaction (MA) neurons may generate the delay of firing onset of the JC motor neurons by producing monosynaptic inhibitory postsynaptic potentials (IPSPs) during the initial portion of their depolarization. In the present experiments, the firing patterns in the MA neurons induced by application of the Geli. or Pach. extract to the lips were explored in the semi-intact preparations. During the Pach. response the duration and the firing frequency of the MA firing at each depolarizing phase were decreased in comparison with the Ulvaresponse. No decreases in the MA firing were observed during the Geli. response, suggesting that the similar patterned jaw movements during rejection of Geli. and Pach. may be generated by different neural mechanisms. Moreover, the size of the MA-induced IPSP in the JC motor neurons was largely decreased by application of the Geli. or Pach. extract to the lips in the reduced preparations consisting of the tentacle-lips and the cerebral-buccal ganglia. Voltage-clamp experiments on the JC motor neurons showed that the size of synaptic current induced by the MA spikes was decreased by application of these solutions to the lips. The decrease was induced when the buccal ganglia were bathed in a solution to block polysynaptic pathways. These results suggest that the advance of the onset of the JC firing at each depolarizing phase during the Geli. or Pach. response may be mainly or partly caused by the decrease in the size of the MA-induced IPSP in the motor neurons. Modulatory action of cerebral neurons or peripheral afferent neurons in the lip region may contribute to this synaptic plasticity.

Feeding CPG in Aplysia Directly Controls Two Distinct Outputs of a Compartmentalized Interneuron That Functions as a CPG Element

2007 ◽  
Vol 98 (6) ◽  
pp. 3796-3801 ◽  
Author(s):  
Kosei Sasaki ◽  
Michael R. Due ◽  
Jian Jing ◽  
Klaudiusz R. Weiss
Keyword(s):  
Action Potentials ◽  
Electrical Coupling ◽  
Motor Program ◽  
Pattern Generator ◽  
Synaptic Connections ◽  
Buccal Ganglion ◽  
Full Size ◽  
Program Generation ◽  
Functional Aspects ◽  
Protraction Phase

In the context of motor program generation in Aplysia, we characterize several functional aspects of intraneuronal compartmentalization in an interganglionic interneuron, CBI-5/6. CBI-5/6 was shown previously to have a cerebral compartment (CC) that includes a soma that does not generate full-size action potentials and a buccal compartment (BC) that does. We find that the synaptic connections made by the BC of CBI-5/6 in the buccal ganglion counter the activity of protraction-phase neurons and reinforce the activity of retraction-phase neurons. In buccal motor programs, the BC of CBI-5/6 fires phasically, and its premature activation can phase advance protraction termination and retraction initiation. Thus the BC of CBI-5/6 can act as an element of the central pattern generator (CPG). During protraction, the CC of CBI-5/6 receives direct excitatory inputs from the CPG elements, B34 and B63, and during retraction, it receives antidromically propagating action potentials that originate in the BC of CBI-5/6. Consequently, in its CC, CBI-5/6 receives depolarizing inputs during both protraction and retraction, and these depolarizations can be transmitted via electrical coupling to other neurons. In contrast, in its BC, CBI-5/6 uses spike-dependent synaptic transmission. Thus the CPG directly and differentially controls the program phases in which the two compartments of CBI-5/6 may transmit information to its targets.

Effects of NH4+ on reflexes in cat spinal cord

1990 ◽  
Vol 64 (2) ◽  
pp. 565-574 ◽  
Author(s):  
W. Raabe
Keyword(s):  
Spinal Cord ◽  
Synaptic Transmission ◽  
Nerve Stimulation ◽  
Action Potentials ◽  
Presynaptic Inhibition ◽  
Excitatory Synaptic Transmission ◽  
P Wave ◽  
Postsynaptic Inhibition ◽  
Presynaptic Terminals ◽  
Muscle Nerve

1. In deeply barbiturate-anesthetized animals. NH4+ decreases spinal excitatory synaptic transmission by neuronal depolarization and subsequent block of conduction of action potentials into presynaptic terminals of low-threshold (presumably Ia-) afferents. Because barbiturates by themselves depress excitatory synaptic transmission and may have modified the effects of NH4+, this study examines the effect of NH4+ on excitatory synaptic transmission in the unanesthetized animal. 2. The effects of NH4+ on monosynaptic and polysynaptic excitatory reflexes as well as di- and polysynaptic inhibition were investigated in the spinal cord of the decerebrate and unanesthetized cat in vivo. 3. The monosynaptic excitatory reflex (MSR) elicited by muscle nerve stimulation and polysynaptic excitatory reflexes elicited by muscle (MSR-PSR) or cutaneous nerve stimulation (Cut-PSR) were recorded from the ventral roots L7 or S1. The P-wave was recorded from the cord dorsum. Di- and polysynaptic inhibition was elicited by muscle nerve stimulation and measured as decrease of the MSR. 4. Intravenous infusion of ammonium acetate (AA) decreased MSR and the monosynaptic motoneuron pool excitatory postsynaptic potential (EPSP) recorded from the ventral root (VR-EPSP). Decrease of MSR and VR-EPSP was accompanied by an increase of the intraspinal conduction time in presynaptic terminals. The maximal decrease of the MSR was preceded by a period of transient increase of the MSR and reflex discharges from previously subthreshold VR-EPSPs. 5. The effects of NH4+ on MSR and VR-EPSP are consistent with those in barbiturate-anesthetized animals and suggest that NH4+ also decreases monosynaptic excitation in unanesthetized animals by depolarization and subsequent conduction block for action potentials in presynaptic terminals. 6. Decrease of the MSR was accompanied by a decrease of the P-wave, indicating that NH4+ simultaneously decreases mono- and oligosynaptic excitatory synaptic transmission as well as presynaptic inhibition. 7. Decrease of the MSR was accompanied by increases of MSR-PSR and Cut-PSR and decreases of di- and polysynaptic postsynaptic inhibition. 8. The neuronal circuits underlying MSR-PSR and Cut-PSR include presynaptic inhibition of group I and II afferents as well as postsynaptic inhibition of motoneurons. It is suggested that increases of MSR-PSR and Cut-PSR are contributed to by decreases of pre- and postsynaptic inhibition and neuronal depolarization by NH4+. These effects increase afferent input to motoneurons, permit uncontrolled discharge of motoneurons, and initiate reflex discharges by previously subthreshold excitatory postsynaptic potentials.

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)

scholarly journals Contralateral sprouting and compensatory innervation following the permanent lesion of a ganglionic connective in the snail

1996 ◽  
Vol 199 (12) ◽  
pp. 2631-2643
Author(s):  
M Baker ◽  
B Chiasson ◽  
R Croll
Keyword(s):  
Central Nervous System ◽  
Achatina Fulica ◽  
Buccal Ganglion ◽  
Axonal Projections ◽  
Buccal Ganglia ◽  
Electrophysiological Measurements ◽  
A Cell ◽  
The Central Nervous System ◽  
Synaptic Drive

The fate of sprouted fibres was examined following long-term recovery from lesions to the central nervous system of the snail Achatina fulica. Axonal dye-labelling of one of the cerebrobuccal connectives (CBC), following either a cut or a crush to the opposite CBC, revealed supernumerary labelling of neuronal elements in both the cerebral and buccal ganglia in the weeks following treatment. A part of this sprouting response involved the rerouting of axonal projections from injured neurones that project contralaterally into the uninjured CBC. In addition, intracellular dye-fills, immunocytochemistry for detection of serotonin and electrophysiological measurements all revealed that a contralateral, uninjured neurone, the metacerebral giant (MCG) cell, sprouted new processes to invade the buccal ganglion denervated by the lesion. The contralateral MCG also increased synaptic drive over a neurone in the denervated buccal ganglion, a cell that normally receives strong input only from the lesioned ipsilateral MCG. After 5 weeks of recovery, morphological and electrophysiological measurements returned to normal levels in animals receiving a crush to the CBC, suggesting a retraction of sprouted projections following successful regeneration across the lesioned pathway. In contrast, the measurements indicative of sprouted fibres continued for up to 5 months when the regenerative response was prevented by cutting the CBC. Together, these results suggest that both the cessation of sprouting and the eventual retraction of sprouted fibres in Achatina fulica is contingent upon successful regeneration of the damaged axonal pathway.

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