Role of the giant serotonin-containing cell of the cerebral ganglion in the edible snail in organizing its food-acquiring behavior

By adding dopamine or serotonin to a bath with snail's isolated nervous system and by intracellular activation of giant cerebral serotonergic cells it was established in neurophysiological experiments that, in spite of activating effect of serotonin on buccal motorneurones, dopamine is the transmitter triggering feeding movements of the buccal mass and feeding pattern in buccal motorneurones. This conclusion is confirmed by behavioural experiments in which an experimental group was injected by neruotoxin 5,6-dihydroxytryptamine selectively impairing serotonergic neurones. The consumatory phase of feeding (triggered by dopamine) did not change in treated animals, while the appetitive phase was significantly impaired. It was noted that the giant metacerebral cell was activated during burst activity in buccal motoneurones. The conclusion is made that giant serotonergic cerebral cells only modulate but do not trigger the feeding behaviour in the snail Helix lucorum.     

Properties of a symmetric pair of serotonin-containing neurones in the cerebral ganglia of Planorbis.

1. There is a bilaterally symmetric pair of large serotonin-containing neurones in the cerebral ganglia of Planorbis corneus. 2. In some animals these neurones are connected by a non-rectifying electrotonic synapse, and fire in synchrony even at prolonged high frequency. In other animals the neurones are not coupled, and fire independently except when driven by common input. Occasionally the coupling is weak. 3. Both coupled and non-coupled serotonin neurones have processes in the major nerve trunks of both buccal ganglia. 4. Synapses are made with many neurones in the buccal ganglia. The serotonin neurones can initiate firing in several motoneurones and thus produce movements of the buccal mass. 5. During spontaneous feeding cycles the input and firing pattern of the serotonin neurones do not bear any obvious relation to the movements of the buccal mass. 6. The data suggest that the serotonin neurones are modulatory cells, altering the level of excitability of buccal ganglion neurones.     

The actions of halothane on spontaneous activity, action potential shape and synaptic connections of the giant serotonin-containing neurone of Lymnaea stagnalis (L.)

1. Cerebral giant cells (CGCs) in the isolated central nervous system (CNS) of the pond snail Lymnaea stagnalis (L.) exhibit bursting activity when superfused with anaesthetic concentrations of halothane. 2. Calcium-dependent components of the CGC action potential appear more sensitive to halothane than do other ionic mechanisms. 3. Higher concentrations of halothane block the chemical synaptic connection between CGC and buccal motoneurone B1, but have no effect on the strong electrotonic coupling between the CGCs. 4. The mechanisms underlying CGC bursting and synaptic block in the presence of halothane are discussed.     

Premotor neurons in the feeding system of Aplysia californica

Central pattern generator (CPG) circuits control cyclic motor output underlying rhythmic behaviors. Although there have been extensive behavioral and cellular studies of food-induced feeding arousal as well as satiation in Aplysia, very little is known about the neuronal circuits controlling rhythmic consummatory feeding behavior. However, recent studies have identified premotor neurons that initiate and maintain buccal motor programs underlying ingestion and egestion in Aplysia. Other newly identified neurons receive synaptic input from feeding CPGs and in turn synapse with and control the output of buccal motor neurons. Some of these neurons and their effects within the buccal system are modulated by endogenous neuropeptides. With this information we can begin to understand how neuronal networks control buccal motor output and how their activity is modulated to produce flexibility in observed feeding behavior.     

Feeding motor program in Limax. I. Neuromuscular correlates and control by chemosensory input

The feeding motor program(FMP) of the terrestrial slug Limax maximus was examined in vivo and in vitro. The feeding pattern of intact animals shows an initial increase in bite frequency followed by a plateau phase. Recordings obtained from semi-intact preparations of the lips, brain, and buccal mass established the correlation of activity in buccal ganglion nerve roots with the protraction-retraction bite cycle. A preparation of the lips, cerebral ganglia, and buccal ganglia was developed, such that, repetitive chemostimulation of the lips yields reproducible bouts of FMP. Sources of proprioceptive feedback from buccal muscles were demonstrated. The feasibility of computer scoring of the FMP is documented. The results demonstrate that aspects of in vivo feeding behavior are retained and identifiable in highly dissected, in vivo preparations.     

Neural control of homologous behaviour patterns in two blaberid cockroaches

Activity patterns of motoneurones which innervate spiracular muscles in two blaberid cockroaches, Blaberus discoidalis and Gromphadorhina portentosa, have been monitored during two homologous behaviour patterns: respiratory and non-respiratory tracheal ventilation. Based upon the activity of spiracular motoneurones during these two activities, the abdominal spiracles have been divided into three functional groups: vestigial, respiratory and non-respiratory. In Blaberus discoidalis spiracle 3 is vestigial, spiracles 6, 7, 8 and 10 are respiratory, and spiracles 4, 5 and 9 are non-respiratory. In Gromphadorhina portentosa spiracles 3 and 10 are vestigial, spiracle 4 is non-respiratory and spiracles 5–9 are respiratory.Respiratory spiracles in both species are characterized by activity patterns of their motoneurones during respiratory tracheal ventilation: low frequency firing at irregular intervals during the respiratory pause and a higher frequency burst synchronous with the expiratory abdominal compression. Non-respiratory spiracles are characterized by complete inactivity of their opener motoneurones during respiratory tracheal ventilation. These motoneurones are activated by mechanical stimulation in both species, which simultaneously suppresses activity in respiratory opener motoneurones. In Blaberus discoidalis, there are no differences between activity patterns of respiratory and non-respiratory closer motoneurones. In Gromphadorhina portentosa, not only do respiratory and non-respiratory closer motoneurones have different activity patterns, but the activity pattern of respiratory closer motoneurones is different during respiratory and non-respiratory tracheal ventilation. The functional implications of these several spiracular motoneurone activity patterns are discussed.     

GABA regulates the buccal motor output of Helisoma by two pharmacologically distinct actions

GABA was tested for its effects on patterned motor activity (PMA) underlying feeding. Using buccal motoneuron B19 to monitor PMA through intracellular recordings, GABA was found to exert effects at two levels. First, GABA stimulated rhythmic patterned activity resembling fictive feeding, which is under the control of the buccal CPG. In addition, GABA produced a direct inhibition of neuron B19. Both effects were observed when the buccal ganglia were studied in isolation from the rest of the central nervous system, suggesting local interactions with GABA receptors of buccal neurons. Furthermore, these two actions of GABA were found to be pharmacologically distinguishable. The direct hyperpolarization of neuron B19 was mimicked by muscimol, but not baclofen, and involved an increased chloride conductance, which was blocked by picrotoxin.Baclofen duplicated CPG activation by GABA. Picrotoxin had no effect on GABA- or baclofen-induced PMA.These results demonstrate that the Helisoma buccal ganglia have two GABA receptor types which resemble, pharmacologically, mammalian GABA_A and GABA_B receptors, and that GABA plays a key role in feeding patterned motor activity in Helisoma.Abbreviations CPG central pattern generator - GABA gammaamino butyric acid - HPLC high performance liquid chromatography - IPSP inhibitory postsynaptic potential - PMA patterned motor activity - SLRT supralateral radular tensor muscle     

Effect of putative neuromodulators on rhythmic buccal motor output in Lymnaea stagnalis

The effects of a variety of neuromodulator substances on rhythmic motor output and activity in neurons in the feeding circuitry of Lymnaea stagnalis were examined. Each neuromodulator produced a unique combination of effects at different levels in the network: i.e., pattern-generating interneurons (N1, N2, and N3), an identified higher-order interneuron (cerebral giant cell, CGC), and buccal motoneurons. 5-Hydroxytryptamine, acetylcholine, and FMRFamide all inhibited rhythmic motor activity. However, this was achieved in different ways. Dopamine changed the nature of rhythmic activity from one in which N2 interneuronal activity was predominant ("N2 rhythm") to a feeding rhythm. Dopamine was the only substance capable of activating the feeding rhythm. Activity in the CGC was increased by 5-hydroxytryptamine, dopamine, and acetylcholine and reduced by FMRFamide. Differential responses in buccal motoneurons were also observed. The results are discussed in relation to previous work on other species and also in terms of the selection of different patterns of motor output by neuromodulators.     

Drilling in the dorid species Vayssierea cf. elegans (Gastropoda: Nudibranchia): Functional and comparative morphological aspects

The drilling mode of feeding is known from two clades of Gastropoda: Caenogastropoda and Heterobranchia. However, the level of convergence and parallelism or homology among these two lineages is unclear. The morphology of the buccal complex is well studied for drilling caenogastropods, but poorly known for drilling nudibranchs. It is also unclear whether the drilling feeding mechanism is similar between inside gastropods. Accordingly, a comparison between the feeding mechanisms of drilling nudibranchs and caenogastropods can help to understand the evolutional trends inside gastropods. In this study, we redescribe the morphology of the buccal complex of drilling dorid nudibranch Vayssierea cf. elegans, and compare it to that of previous investigations on this species and closely related dorid species. We describe the feeding mechanism of this species based on the obtained morphological and literature data and compare it to the feeding mechanisms described for drilling caenogastropods. The feeding apparatus of Vayssierea cf. elegans corresponds to the general morphology of the dorid buccal complex; that is, it has a similar arrangement of the buccal musculature and pattern of radular morphology. However, there are also adaptations to the drilling feeding mode similar to those found in Caenogastropoda: that is, specialized dissolving glands and lateral teeth with elongated pointed cusps; and even Sacoglossa: the specialized muscle for sucking. The feeding process of Vayssierea cf. elegans includes the same two stages as those described for drilling caenogastropods: (a) the boring stage, which is provided by mechanical and chemical activity, and (b) the swallowing stage.     

Octopamine: a new feeding modulator in Lymnaea

The role of octopamine (OA) in the feeding system of the pond snail, Lymnaea stagnalis, was studied by applying behavioural tests on intact animals, and a combination of electrophysiological analysis and morphological labelling in the isolated central nervous system. OA antagonists phentolamine, demethylchlordimeform (DCDM) and 2-chloro-4-methyl-2-(phenylimino)-imidazolidine (NC-7) were injected into intact snails and the sucrose-induced feeding response of animals was monitored. Snails that received 25 to 50 mg kg^-1 phentolamine did not start feeding in sucrose, and the same dose of NC-7 reduced the number of feeding animals by 80 to 90% 1 to 3 hours after injection. DCDM treatment reduced feeding by 20 to 60%. In addition, both phentolamine and NC-7 significantly decreased the feeding rate of those animals that still accepted food after 1 to 6 hours of injection. In the central nervous system a pair of buccal neurons was identified by electrophysiological and morphological criteria. After double labelling (intracellular staining with Lucifer yellow followed by OA-immunocytochemistry) these neurons were shown to be OA immunoreactive, and electrophysiological experiments confirmed that they are members of the buccal feeding system. Therefore the newly identified buccal neurons were called OC neurons (putative octopamine containing neurons or octopaminergic cells). Synchronous intracellular recordings demonstrated that the OC neurons share a common rhythm with feeding neurons either appearing spontaneously or evoked by intracellularly stimulated feeding interneurons. OC neurons also have synaptic connections with identified members of the feeding network: electrical coupling was demonstrated between OC neurons and members of the B4 cluster motoneurons, furthermore, chemically transmitted synaptic responses were recorded both on feeding motoneurons (B1, B2 cells) and the SO modulatory interneuron after the stimulation of OC neurons. However, elementary synaptic potentials could not be recorded on the follower cells of OC neurons. Prolonged (20 to 30 s) intracellular stimulation of OC cells activated the buccal feeding neurons leading to rhythmic activity pattern (fictive feeding) in a way similar to OA applied by perfusion onto isolated central nervous system (CNS) preparations. Our results suggest that OA acts as a modulatory substance in the feeding system of Lymnaea stagnalis and the newly identified pair of OC neurons belongs to the buccal feeding network.     

The Role of Small Cardioactive Peptide, SCPB, in the Regulatory Responses of Terrestrial Slugs

The feeding motor program in Limax maximus is the neural correlateof feeding and consists of a discrete pattern of cyclical efferentactivity generated by the buccal ganglia in response to stimulationof chemosensory pathways. The small cardioactive peptide, SCP_B(10^–6 to 10^–9 M), increases the responsiveness ofthe FMP and the endogenous activity of specific feeding motoneuronssuch as the fast salivary burster. Stimulation of buccal neuron,B1, which contains SCP_B-like immunoreactive substance, similarlyincreases the activity of feeding motoneurons. Furthermore,both exogenous SCP_B and stimulation of Bl increase the contractileforce of the heart. Thus it appears that the peptidergic neuronBl is a multifunctional interneuron that is involved in thecontrol of both peripheral and central targets.     

Electrophysiological study of serotoninergic neuron Cl in the pteropod mollusk Clione

Functional characteristics of cerebral serotoninergic neuron Cl, axons of which terminate at the buccal ganglia [7], were investigated in the pteropod molluskClione. Stimulating neuron Cl induced activation of the feeding rhythm generator located in the buccal ganglia — an effect arising after a long latency and persisting for some tens of seconds once stimulation had ended. Neuron Cl receives feedback from buccal ganglion cells and this brings about periodic modulation in ganglia activity during the generation of feeding rhythm. Activity of neuron Cl is correlated with operation of the locomotor rhythm generator located in the pedal ganglia. The firing rate of Cl neurons increased upon activation of the locomotor generator (whether spontaneous or induced by stimulating certain command neurons). The correlation found between workings of the locomotor generator and activity of Cl neurons is thought to be one of the manifestations of feeding synergy involving simultaneous activation of the locomotor and buccal apparatus.Institute for Research on Information Transmission, Academy of Sciences of the USSR, Moscow. M. V. Lomonosov State University, Moscow. Translated from Neirofiziologiya, Vol. 23, No. 1, pp. 18–25, January–February, 1991.     

Phase-dependent coordination of two motor programs in the buccal ganglion of a pteropod mollusk

Rhythmic activities of two feeding structures of the pteropod mollusk Clione limacina, redula and hooks, controlled by the neural networks in the buccal ganglia must be coordinated in order to produce a meaningful feeding response. Optical recording from the buccal ganglia, which allows the simultaneous activities of numerous neurons to be traced, revealed that such coordination exists in a phase-dependent manner. Instead of recording four theoretically possible phases of neuronal rhythmic activity, we always recorded only two phases, even after the electrical stimulation of the cerebro-buccal connective, which triggers both radula and hook rhythmic movements in the preparation.     

Feeding mechanisms in anuran larvae

Larvae of the neotropical frogs Phyllomedusa are distinctive in that they feed normally in mid-water on phytoplankton, maintaining neutral buoyancy by means of an independently beating tail filament. The feeding mechanism of larval Phyllomedusa trinitatis was studied morphologically and experimentally. The primary feeding mechanism involves a buccal rasp which may in some circumstances render food into small particles, a pumping mechanism which forces water through the buccal cavity and the gill filters, an entanglement system which traps particles in mucous strings produced in special organs, and the formation of mucous cords which transport particles to the oesophagus. In mid-water feeding and surface feeding the buccal rasp serves only its other function in preventing backflow of the respiratory stream. The primary feeding mechanism is discussed and compared with schemes proposed for Rana temporaria and R. agilis. Little agreement exists between these schemes and that which is here proposed. It is concluded that the primary feeding mechanism is the same in the three forms but that there are behavioural differences in feeding generally. Some comment is made on the primary feeding mechanism in the Microhylidae.     

Evidence for homologous peptidergic neurons in the buccal ganglia of diverse nudibranch mollusks.

The buccal ganglia of seven nudibranches (Aeolidia papillosa, Armina californica, Dirona albolineata, D. picta, Hermissenda crassicornis, Melibe leonina, and Tritonia diomedea) were examined to explore possible homologies between large cells that reacted with antibodies directed against small cardioactive peptide B (SCPB). The buccal ganglion of each species possessed a pair of large, dorsal-lateral, whitish neurons that contained an SCPB-like peptide. We refer to these neurons as the SLB (SCPB-immunoreactive Large Buccal) cells. In all species examined, the SLB cells project out the gastroesophageal nerves and appear to innervate the esophagus. In each species, an apparent rhythmic feeding motor program (FMP) was observed by intracellular recording from both SLB neurons and other neurons in isolated preparations of the buccal ganglia. SLB cells often fire at a high frequency, and usually burst in a specific phase relation to the FMP activity. Stimulation of SLB cells enhances expression of the feeding motor program, either by potentiating existing activity or eliciting the FMP in quiescent preparations. Finally, perfusion of isolated buccal ganglia with SCPB excites the SLB cells and activates FMPs. Thus, both the immunohistochemical and electrophysiological data suggest that the SLB cells within three suborders of the opisthobranchia (Dendronotacea, Arminacea, and Aeolidacea) are homologous. A comparison of our data with previously published studies indicates that SLB cell homologs may exist in other gastropods as well.     

The octopamine-containing buccal neurons are a new group of feeding interneurons in the pond snail Lymnaea stagnalis

In the pond snail, Lymnaea stagnalis, the paired buccal ganglia contain 3 octopamine-immunoreactive neurons, which have previously been shown to be part of the feeding network. All 3 OC cells are electrically coupled together and interact with all the known buccal feeding motoneurons, as well as with all the modulatory and central pattern generating interneurons in the buccal ganglia. N1 (protraction) phase neurons: Motoneurons firing in this phase of the feeding cycle receive either single excitatory (depolarising) synaptic inputs (B1, B6 neurons) or a biphasic response (hyperpolarisation followed by depolarisation) (B5, B7 motoneurons). Protraction phase feeding interneurons (SO, N1L, NIM) also receive this biphasic synaptic input after OC stimulation. All of protraction phase interneurons inhibit the OC neurons. N2 (retraction) phase neurons: These motoneurons (B2, B3, B9, B10) and N2 interneurons are hyperpolarised by OC stimulation. N2 interneurons have a variable (probably polysynaptic) effect on the activity of the OC neurons. N3 (swallowing) phase: OC neurons are strongly electrically coupled to both N3 phase (B4, B4cluster, B8) motoneurons and to the N3p interneurons. In case of the interneuronal connection (OC<->N3) the electrical synapse is supplemented by reciprocal chemical inhibition. However, the synaptic connections formed by the OC neurons or N3p interneurons to the other members of the feeding network are not identical. CGC: The cerebral, serotonergic CGC neurons excite the OC cells, but the OC neurons have no effect on the CGC activity. In addition to direct synaptic effects, the OC neurons also evoke long-lasting changes in the activity of feeding neurons. In a silent preparation, OC stimulation may start the feeding pattern, but when fictive feeding is already occurring, OC stimulation decreases the rate of the fictive feeding. Our results suggest that the octopaminergic OC neurons form a sub-population of N3 phase feeding interneurons, different from the previously identified N3p and N3t interneurons. The long-lasting effects of OC neurons suggest that they straddle the boundary between central pattern generator and modulatory neurons.     

Models for unambiguousE-vector navigation in the bee

Summary The metacerebral giant (MCG) neurons of the molluskPleurobranchaea have been analyzed using a wide range of methods (cobalt staining, histochemical, biophysical and electrophysiological) on several types of preparations (isolated nervous systems, semi-intact preparations, and behaving whole-animal preparations). The MCG is serotonergic. The bilaterally-symmetrical neurons have somata in the anterior brain. Each MCG neuron sends an axon out the ipsilateral mouth nerve of the brain and also into the ipsilateral cerebrobuccal connective which descends to the buccal ganglion. The descending axon sends one or more branches out most buccal nerves.The MCG makes mono- and polysynaptic chemical excitatory and inhibitory connections with identified feeding motoneurons in the buccal ganglion. In quiescent preparations (isolated CNS or semi-intact), MCG stimulation caused coordinated eversion activity followed immediately by withdrawal activity. During an ongoing feeding rhythm (spontaneous output or induced by stimulation of the stomatogastric nerve), tonic stimulation of one or both MCG's at physiological discharge frequencies typically caused a significant increase in the frequency of the rhythm, and usually emphasized the eversion component at the expense of the withdrawal component. Phasic stimulation of one or both MCG's at physiological discharge frequencies and in normal discharge patterns (bursts; see below) accelerated and phaselocked the feeding rhythm.The MCG neurons receive synaptic feedback from identified neurons in the feeding network. Brain motoneurons are reciprocally coupled with the MCG by non-rectifying electrical synapses, while buccal ganglion neurons (the previously identified corollary discharge neurons) inhibit the MCG. Recordings from the MCG during cyclic feeding show that it discharges cyclically and that its membrane potential oscillates in phase with the feeding rhythm, presumably reflecting the above synaptic feedback. Two biophysical properties of the MCG membrane, namely anomalous rectification and postspike conductance increase, are presumed to contribute to the MCG's oscillatory activity.Chemosensory (food stimuli) and mechanosensory inputs from the oral veil excite the MCG's. In whole-animal preparations, these sensory inputs typically cause discharge in the MCG's and other descending neurons, accompanied by feeding motor output.The data collectively suggest that the MCG's ofPleurobranchaea are members of a population of neurons that normally function to command (i.e., arouse, initiate and sustain) the rhythmic feeding behavior. The demonstrated central feedback to the MCG is presumed to amplify these command functions.Supported by an NIH Postdoctoral Fellowship (1 F22 NS00511) to R.G. and NIH Research Grants NS 09050 and MH 23254 to W.J.D. We thank Kathryn H. Britton for histological assistance. We also thank Mark P. Kovac, who produced the records of Figures 8 and 18, for permission to reproduce them here.     

Reflex activation of locust flight motoneurones by proprioceptors responsive to muscle contractions

 This report investigates the reflex activation of locust flight motoneurones following their spiking activity. As shown elsewhere, an electrical stimulus applied to a flight muscle produces multiple waves of delayed excitation in wing elevator and depressor motoneurones. Nerve ablation experiments show that this response is initiated by the mechanical movement of the stimulated muscle, and not the antidromic spike evoked in the motoneurone. The delayed excitation still occurs in the absence of inputs from the wing receptor systems, and also when all other sources of afferent feedback are abolished, excepting thoracic nerve 2. Following complete deafferentation, spikes in flight motoneurones had no influence on other flight motoneurones. Numerous afferents in the purely sensory nerve 2 are excited by flight muscle contractions. The responses are consistent for repeated contractions of the same muscle, but differ when other muscles are stimulated. During tethered flight, changes in the activation of single flight muscles are reflected in changes of the nerve 2 discharge pattern. Electrical stimulation of this nerve causes delayed excitation of flight motoneurones, and can initiate flight activity. It is suggested that internal proprioceptors, such as those associated with nerve 2, will contribute to shaping the final motor output for flight behaviour. Accepted: 24 April 1996