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.     

Comparative pharmacology of feeding in molluscs

1. This paper reviews the role of transmitters in identified neurons of gastropod molluscs in generating and modulating fictive feeding. 2. In Lymnaea and Helisoma the 3 phase rhythm is generated by sets of interneurons which use acetylcholine for the N1 (protraction) phase, glutamate for the N2 (rasp) phase interneurons. The N3 interneurons are likely to use several different transmitters, of which one is octopamine. 3. In all the species examined, serotonin (5-HT) is released from giant cerebral cells. Other amines, including dopamine and octopamine, are present in the buccal ganglia and all these amines activate or enhance feeding. 4. Nitric oxide (NO), mostly originating from sensory processes, can also activate fictive feeding, but (at least in Lymnaea) may also be released centrally from buccal (B2) and cerebral neurons (CGC). 5. The central pattern generator for feeding is also modulated by peptides including APGWamide, SCP(B) and FMRFamide. 6. There is increasing evidence that most of these transmitters/modulators act on feeding neurons through second messenger systems--allowing them to act as longer-lasting neuromodulators of the feeding network. 7. Many of the transmitters are used in similar ways by each of the gastropods examined so far, so that their function in the CNS seems to have been conserved through evolution.     

Multilevel inhibition of feeding by a peptidergic pleural interneuron in the mollusc<Emphasis Type="Italic"> Lymnaea stagnalis</Emphasis>

The pleural interneuron PlB is a white neuron in the pleural ganglion of the snail Lymnaea. We test the hypothesis that it inhibits neurons at all levels of the feeding system, using a combination of anatomy, physiology and pharmacology. There is just one PlB in each pleural ganglion. Its axon traverses the pedal and cerebral ganglia, running into the buccal ganglia. It has neuropilar branches in the regions of the cerebral and buccal ganglia where neurons that are active during feeding also branch. Activation of the PlB blocks fictive feeding, whether the feeding rhythm occurs spontaneously or is driven by a modulatory interneuron. The PlB inhibits all the neurons in the feeding network, including protraction and retraction motoneurons, central pattern generator interneurons, buccal modulatory interneurons (SO, OC), and cerebral modulatory interneurons (CV1, CGC). Only the CV1 interneuron shows discrete 1:1 IPSPs; all other effects are slow, smooth hyperpolarizations. All connections persist in Ca²⁺/Mg²⁺-rich saline, which reduces polysynaptic effects. The inhibitory effects are mimicked by 0.5 to 100 mol l^–1 FMRFamide, which the PlB soma contains. We conclude that the PlB inhibits neurons in the feeding system at all levels, probably acting though the peptide transmitter FMRFamide.Electronic Supplementary Material Supplementary material is available in the online version of this article at http://dx.doi.org/10.1007/s00359-004-0503-x     

The hybrid modulatory/pattern generating N1L interneuron in the buccal feeding system ofLymnaea is cholinergic

This study examines neurotransmission between identified buccal interneurons in the feeding system of the snailLymnaea stagnalis. We compare the pharmacology of the individual synaptic connections from a hybrid modulatory/pattern generating interneuron (N1L) to a pattern generating interneuron (N1M) with that from a modulatory interneuron (SO) to the same follower cell (N1M). The pharmacological properties of the N1L to N1M and the SO to N1M connections closely resemble each other. Both interneurons produce fast cholinergic EPSPs as judged by the blocking effects of cholinergic antagonists hexamethonium,d-tubocurarine and the cholinergic neurotoxin AF-64A. A slower, more complex but non-cholinergic component of the synaptic response is also present after stimulating either the presynaptic N1L or SO interneurons. This second component of the postsynaptic response is not dopaminergic, on the basis of its persistence in the presence of dopaminergic antagonists ergometrine and fluphenazine and the dopaminergic neurotoxin MPP+. We conclude that, although there has been an evolutionary divergence in function, the modulatory SO and the hybrid modulatory/pattern generating N1L are pharmacologically similar. Neither of them contributes directly to dopaminergic modulation of the feeding activity. These neurons also resemble the N1M protraction phase pattern generating neurons which are cholinergic (Elliott and Kemenes, 1992).     

Octopamine-containing (OC) interneurons enhance central pattern generator activity in sucrose-induced feeding in the snail <Emphasis Type="Italic">Lymnaea</Emphasis>

In the pond snail Lymnaea stagnalis octopamine-containing (OC) interneurons trigger and reconfigure the feeding pattern in isolated CNS by excitation of the central pattern generator. In semi-intact (lip–mouth—CNS) preparations, this central pattern generator is activated by chemosensory inputs. We now test if sucrose application to the lips activates the OC neurons independently of the rest of the feeding central pattern generator, or if the OC interneuron is activated by inputs from the feeding network. In 66% of experiments, sucrose stimulated feeding rhythms and OC interneurons received regular synaptic inputs. Only rarely (14%) did the OC interneuron fire action potentials, proving that firing of OC interneurons is not necessary for the sucrose-induced feeding. Prestimulation of OC neurons increased the intensity and duration of the feeding rhythm evoked by subsequent sucrose presentations. One micromolar octopamine in the CNS bath mimicked the effect of OC interneuron stimulation, enhancing the feeding response when sucrose is applied to the lips. We conclude that the modulatory OC neurons are not independently excited by chemosensory inputs to the lips, but rather from the buccal central pattern generator network. However, when OC neurons fire, they release modulatory octopamine, which provides a positive feedback to the network to enhance the sucrose-activated central pattern generator rhythm.     

Cholinergic interneurons in the feeding system of the pond snail Lymnaea stagnalis. II. N1 interneurons make cholinergic synapses with feeding motoneurons.

The N1 neurons are a population of interneurons active during the protraction phase of the feeding rhythm. All the N1 neurons are coupled by electrical synapses which persist in a high Mg/low Ca saline which blocks chemical synapses. Individual N1 spikes produce discrete electrotonic postsynaptic potentials (PSPS) in other N1 cells, but the coupling is not strong enough to ensure 1:1 firing. Bursts of N1 spikes generate compound PSPS in the feeding motoneurons. The sign (excitation or inhibition) of the N1 input corresponds with the synaptic barrage recorded during the protraction phase. Discrete PSPS are only resolved in a Hi-Di saline. Their variation in latency and number can be explained by variation in electrotonic propagation within the electrically coupled network of N1 cells. The excitatory postsynaptic potentials (ESPS) in the 1 cell are reduced by 0.5 mM antagonists hexamethonium (HMT), atropine (ATR), curare (d-TC) and by methylxylocholine (MeXCh), all of which block the excitatory cholinergic receptor (Elliott et al. (Phil. Trans. R. Soc. Lond. 336, 157-166 (Preceding paper.) (1992)). The 1 cell EPSPS were transiently blocked by phenyltrimethylammonium (PTMA), which is both an agonist and antagonist at the 1 cell excitatory acetylcholine (ACh) receptor (Elliott et al. 1992). The inhibitory postsynaptic potential (IPSP) in the 3 cell is blocked by bath applications of MeXCh and PTMA, which both abolish the response of the 3 cell to ACh (Elliott et. al. 1992). The effects of the cholinergic antagonists on the response of 4 cluster and 5 cells to N1 stimulation matches their response to ACh (Elliott et al. 1992). It is concluded that the population of N1 cells are multiaction, premotor cholinergic interneurons.     

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.     

Neural organization of the ventilatory activity in the frog,Rana catesbeiana. II

The paralyzed, decerebrate frog, Rana catesbeiana, displays “fictive” oropharyngeal and pulmonary ventilations. In order to evaluate the neuronal correlates of these two centrally programmed ventilatory bursting patterns, we have performed intra-and extracellular recordings of bulbar respiratory neurons in this fictively breathing preparation. A total of 123 respiratory neurons were recorded from the caudal medulla. Of 51 antidromically activated neurons, 20 were vagal motoneurons and 31 were hypoglossal motoneurons. Respiratory neurons that depolarized during the lung (L) or non-lung (N) ventilatory phases were classified as L or N neurons, respectively. Phase spanning neurons (S) were active during both L and N phases. Some neurons showed oscillations of membrane potential synchronous with oropharyngeal ventilation. Those active during the buccal elevation phase were exclusively L neurons whereas those having buccal depressor activity were exclusively N neurons. Synaptic drive potentials were observed in all neurons recorded intracellularly. In some neurons, hyperpolarization was caused by inhibitory postsynaptic potentials, as demonstrated by reversal of membrane potential trajectory after intracellular chloride iontophoresis. Some individual motoneurons and interneurons exhibited both pulmonary and buccal ventilatory activity, indicating that both pattern generators project to a common motor control system. 1994 John Wiley & Sons, Inc.     

Feeding neural networks in the mollusc Aplysia

Aplysia feeding is striking in that it is executed with a great deal of plasticity. At least in part, this flexibility is a result of the organization of the feeding neural network. To illustrate this, we primarily discuss motor programs triggered via stimulation of the command-like cerebral-buccal interneuron 2 (CBI-2). CBI-2 is interesting in that it can generate motor programs that serve opposing functions, i.e., programs can be ingestive or egestive. When programs are egestive, radula-closing motor neurons are activated during the protraction phase of the motor program. When programs are ingestive, radula-closing motor neurons are activated during retraction. When motor programs change in nature, activity in the radula-closing circuitry is altered. Thus, CBI-2 stimulation stereotypically activates the protraction and retraction circuitry, with protraction being generated first, and retraction immediately thereafter. In contrast, radula-closing motor neurons can be activated during either protraction or retraction. Which will occur is determined by whether other cerebral and buccal neurons are recruited, e.g. radula-closing motor neurons tend to be activated during retraction if a second CBI, CBI-3, is recruited. Fundamentally different motor programs are, therefore, generated because CBI-2 activates some interneurons in a stereotypic manner and other interneurons in a variable manner.     

Memory trace in feeding neural circuitry underlying conditioned taste aversion in lymnaea

Background

The pond snail Lymnaea stagnalis can maintain a conditioned taste aversion (CTA) as a long-term memory. Previous studies have shown that the inhibitory postsynaptic potential (IPSP) evoked in the neuron 1 medial (N1M) cell by activation of the cerebral giant cell (CGC) in taste aversion-trained snails was larger and lasted longer than that in control snails. The N1M cell is one of the interneurons in the feeding central pattern generator (CPG), and the CGC is a key regulatory neuron for the feeding CPG.

Methodology/Principle Findings

Previous studies have suggested that the neural circuit between the CGC and the N1M cell consists of two synaptic connections: (1) the excitatory connection from the CGC to the neuron 3 tonic (N3t) cell and (2) the inhibitory connection from the N3t cell to the N1M cell. However, because the N3t cell is too small to access consistently by electrophysiological methods, in the present study the synaptic inputs from the CGC to the N3t cell and those from the N3t cell to the N1M cell were monitored as the monosynaptic excitatory postsynaptic potential (EPSP) recorded in the large B1 and B3 motor neurons, respectively. The evoked monosynaptic EPSPs of the B1 motor neurons in the brains isolated from the taste aversion-trained snails were identical to those in the control snails, whereas the spontaneous monosynaptic EPSPs of the B3 motor neurons were significantly enlarged.

Conclusion/Significance

These results suggest that, after taste aversion training, the monosynaptic inputs from the N3t cell to the following neurons including the N1M cell are specifically facilitated. That is, one of the memory traces for taste aversion remains as an increase in neurotransmitter released from the N3t cell. We thus conclude that the N3t cell suppresses the N1M cell in the feeding CPG, in response to the conditioned stimulus in Lymnaea CTA.     

Cerebral interneurons controlling fictive feeding in Limax maximus

Summary Initiation and modulation of fictive feeding by cerebral to buccal interneurons (CBs) was examined in an isolated CNS preparation of Limax maximus. Three CBs which are phasically active during fictive feeding, CB₁, CB₃ and CB₄, will reliably trigger bouts of fictive feeding when activated alone or in pairs. Another phasic CB, CB_EC, is not effective for triggering feeding. One CB which is tonically active during fictive feeding, CB_ST, drives fictive feeding in 50% of preparations when activated alone and enhances triggering of feeding when co-activated with phasic CBs. The metacerebral giant cell (MGC) was found to be capable of triggering fictive feeding in preparations with an intact subcerebral commissure. The MGC was especially effective at increasing the effectiveness of other CBs for initiation of feeding. Short high-frequency bursts of phasic CB or MGC action potentials are capable of resetting ongoing fictive feeding. Resetting effects of CB action potentials are relatively independent of the phase of the bite-cycle in which they are activated. CB₄ phase-advances the bite-cycle while the other phasic CBs phase-delay the bite cycle. Moderate frequency stimulation of CB₄ speeds up the bite rate while moderate frequency stimulation of CB₃ slows biting. All CBs, except the tonic CB, CB_DL, increase the intensity of buccal motor neuron bursting during feeding. The excitatory effects of phasic CBs and the tonic CB, CB_EPSP, on fictive feeding persist for many seconds after the offset of stimulation. CBs form both monosynaptic excitatory and monosynaptic inhibitory connections with different BG motor neurons.Abbreviations BG buccal ganglion - BR buccal root - CB cerebral-buccal interneuron - CBC cerebral-buccal connective - CPG central pattern generator - FB fast burster neuron - FMP feeding motor program - IBI interbite interval - MGC metacerebral giant cell     

Octopaminergic modulation of the membrane currents in the central feeding system of the pond snail Lymnaea stagnalis

Octopamine is released by the intrinsic OC interneurons in the paired buccal ganglia and serves both as a neurotransmitter and a neuromodulator in the central feeding network of the pond snail Lymnaea stagnalis. The identified B1 buccal motoneuron receives excitatory inputs from the OC interneurons and is more excitable in the presence of 10 microM octopamine in the bath. This modulatory effect of octopamine on the B1 motoneuron was studied using the two electrode voltage clamp method. In normal physiological saline depolarising voltage steps from the holding potential of -80 mV evoke a transient inward current, presumably carried by Na(+) ions. The peak values of this inward current are increased in the presence of 10 microM octopamine in the bath. In contrast, both the transient (IA) and delayed (IK) outward currents are unaffected by octopamine application. Replacing the normal saline with a Na(+)-free bathing solution containing K(+) channel blockers (50 mM TEACl, 4 mM 4AP) revealed the presence of an additional inward current of the B1 neurons, carried by Ca(2+). Octopamine (10 microM) in the bath decreased the amplitudes of this current. These results suggest that the membrane mechanisms which underlie the modulatory effect of octopamine on the B1 motoneuron include selective changes of the Na(+)- and Ca(2+)-channels.     

Assessing the roles of glutamatergic and cholinergic synaptic drive in the control of fictive swimming frequency in young Xenopus tadpoles

This paper investigates the proposal that the frequency of the swimming central pattern generator in young Xenopus tadpoles is partly determined by the population of glutamatergic premotor interneurons active on each cycle. During fictive swimming spinal neurons also receive cholinergic and electrotonic excitation from motoneurons. As frequency changes during swimming we make two predictions: first, since most motoneurons fire very reliably at all frequencies, the electrotonic and nicotinic drive from motoneurons should remain constant, and second, when swimming frequency decreases, the glutamatergic drive should decrease as the number of active premotor excitatory interneurons decreases. We have tested these predictions by measuring the excitatory synaptic drive to motoneurons as frequency changes during fictive swimming. The components of synaptic drive were revealed by the local microperfusion of strychnine together with different excitatory antagonists. After blocking the nicotinic acetylcholine receptor, the mainly glutmatergic excitatory synaptic drive still changed with frequency. However, when glutamate receptors or all chemical transmission was blocked, excitation did not change with frequency. Our predictions are confirmed, suggesting that premotor excitatory interneurons are a major factor in frequency control in the tadpole central pattern generator and that motoneurons provide a stable background excitation. Accepted: 14 August 1998     

Optical detection of neuromodulatory effects of conditioned taste aversion in the pond snail Lymnaea stagnalis

Multiple site optical recording was used to analyze the neural activity changes caused by conditioned taste aversion (CTA) training in the pond snail Lymnaea stagnalis. In response to electrical stimulation of the median lip nerve, which transmits chemosensory signals of appetitive taste to the central nervous system, we optically detected large numbers of spikes in several parts of the buccal ganglion. The effects of CTA training on the spike responses were examined in two areas of the ganglion where the most active neural responses occurred. In one area (termed Area I) that included the N1 medial (N1M) cells, a class of central pattern generator interneurons involved in feeding behavior, the number of spikes in a period 1500-2000 ms after median lip nerve stimulation was significantly reduced in conditioned animals compared to control animals. In another area (termed Area II) positioned between buccal motoneurons, the B3 and B4CL (cluster) cells, the evoked spike responses were unaffected by CTA training. These results, taken together with our previous results indicating an enhancement of an inhibitory input to the N1M cells during CTA, suggest that an appetitive taste signal transmitted to the N1M cells through the median lip nerves is suppressed during CTA, resulting in a decrease of the feeding response.     

Cerebral-buccal pathways in Aplysia californica: synaptic connections, cooperative interneuronal effects and feedback during buccal motor programs

Ingestion of seaweed by Aplysia is in part mediated by cerebral-buccal interneurons that drive rhythmic motor output from the buccal ganglia and in some cases cerebral-buccal interneurons act as members of the feeding central pattern generator. Here we document cooperative interactions between cerebral-buccal interneuron 2 and cerebral-buccal interneuron 12, characterize synaptic input to cerebral-buccal interneuron 2 and cerebral-buccal interneuron 12 from buccal peripheral nerve 2,3, describe a synaptic connection between cerebral-buccal interneuron 1 and buccal neuron B34, further characterize connections made by cerebral-buccal interneurons 2 and -12 with B34 and B61/62, and describe a novel, inhibitory connection made by cerebral-buccal interneuron 2 with a buccal neuron. When cerebral-buccal interneurons 2 and 12 were driven synchronously at low frequencies, ingestion-like buccal motor programs were elicited, and if either was driven alone, indirect synaptic input was recruited in the other cerebral-buccal interneuron. Stimulation of BN2,3 recruited both ingestion and rejection-like motor programs without firing in cerebral-buccal interneurons 2 or 12. During motor programs elicited by cerebral-buccal interneurons 2 or 12, high-voltage stimulation of BN2,3 inhibited firing in both cerebral-buccal interneurons. Our results suggest that cerebral-buccal interneurons 2 and 12 use cooperative interactions to modulate buccal motor programs, yet firing in cerebral-buccal interneurons 2 or 12 is not necessary for recruiting motor programs by buccal peripheral nerve BN2,3, even in preparations with intact cerebral-buccal pathways.     

Cerebral neurons underlying prey capture movements in the pteropod mollusc,Clione limacina

The pteropod mollusc Clione limacina is a highly specialized carnivore which feeds on shelled pteropods and uses, for their capture, three pairs of oral appendages, called buccal cones. Contact with the prey induces rapid eversion of buccal cones, which then become tentacle-like and grasp the shell of the prey. In the previous paper, a large group of electrically coupled, normally silent cells (A motoneurons) has been described in the cerebral ganglia of Clione. Activation of A neurons induces opening of oral skin folds and extrusion of the buccal cones. The present study continues the analysis of the electrical properties of A motoneurons.Brief intracellular stimulation of an A neuron can produce prolonged firing (afterdischarge), lasting up to 40 s, in the entire population of A neurons. Afterdischarge activity is based on an afterdepolarization evoked by an initial strong burst of A neuron spikes. The data suggest that this afterdepolarization represents excitatory synaptic input from unidentified neurons which in turn receive excitatory inputs from A neurons, thus organizing positive feedback. The main functional role of this positive feedback is the spread and synchronization of spike activity among all A neurons in the population. In addition, it serves to transform a brief excitatory input to A neurons into their prolonged and stable firing, which is required during certain phases of feeding behavior in Clione.     

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.     

Peptidergic motoneurons in the buccal ganglia of Aplysia californica Immunocytochemical,morphological, and physiological characterizations

Summary We used physiological recordings, intracellular dye injections and immunocytochemistry to further identify and characterize neurons in the buccal ganglia of Aplysia calif ornica expressing Small Cardioactive Peptide-like immunoreactivity (SCP-LI). Neurons were identified based upon soma size and position, input from premotor cells B4 and B5, axonal projections, muscle innervation patterns, and neuromuscular synaptic properties. SCP-LI was observed in several large ventral neurons including B6, B7, B9, B10, and B11, groups of s1 and s2 cluster cells, at least one cell located at a branch point of buccal nerve n2, and the previously characterized neurons B1, B2 and B15.B6, B7, B9, B10 and B11 are motoneurons to intrinsic muscles of the buccal mass, each displaying a unique innervation pattern and neuromuscular plasticity. Combined, these motoneurons innervate all major intrinsic buccal muscles (I1/I3, I2, I4, I5, I6). Correspondingly, SCP-LI processes were observed on all of these muscles. Innervation of multiple nonhomologous buccal muscles by individual motoneurons having extremely plastic neuromuscular synapses, represents a unique form of neuromuscular organization which is prevalent in this system. Our results show numerous SCPergic buccal motoneurons with widespread ganglionic processes and buccal muscle innervation, and support extensive use of SCPs in the control of feeding musculature.Abbreviations SCP-LI small cardioactive peptide-like immunoreactivity - PSC postsynaptic current - EPSP excitatory postsynaptic potential - IPSP inhibitory postsynaptic potential - FI facilitation index - TMR time to maximal response     

Neural mechanism generating firing patterns in jaw motoneurons during the food-induced response in Aplysia kurodai

1. In each right and left buccal ganglia of Aplysia kurodai, we identified 4 premotor neurons impinging on the ipsilateral jaw-closing and -opening motoneurons. Three of them (MA1 neurons) had features of multifunctional neurons. Current-induced spikes in the MA1 neurons produced excitatory junction potentials (EJPs) in the buccal muscle fibers. In addition, tactile stimulation of the buccal muscle surface produced a train of spikes in the MA1 neurons without synaptic input. The other neuron (MA2) had only a premotor function. 2. The MA1 and MA2 neurons had similar synaptic effects on the jaw-closing and -opening motoneurons. Current-induced spikes in the premotor neurons gave rise to monosynaptic inhibitory postsynaptic potentials (IPSPs) in the ipsilateral jaw-closing motoneurons. Simultaneously, spikes in one of the MA1 neurons and the MA2 also gave rise to monosynaptic excitatory postsynaptic potentials (EPSPs) in the ipsilateral jaw-opening motoneuron. 3. The IPSPs and the EPSPs induced by spikes in the premotor neurons were reversibly blocked by d-tubocurarine and hexamethonium, respectively, suggesting that the MA1 and MA2 neurons are cholinergic. 4. When depolarizing and hyperpolarizing current pulses were passed into one premotor neuron, attenuated but similar potential changes were produced in another randomly selected premotor neuron in the same ganglion, suggesting that they are electronically coupled.     

An identified cerebral interneuron initiates different elements of prey capture behavior in the pteropod mollusc,Clione limacina

The prey capture phase of feeding behavior in the pteropod molluscClione limacina consists of an explosive extrusion of buccal cones, specialized oral appendages which are used to catch the prey, and significant acceleration of swimming. Several groups of neurons which control different components of prey capture behavior inClione have been previously identified in the CNS. However, the question of their coordination in order to develop a normal behavioral reaction still remains open. We describe here a cerebral interneuron which has wide-spread excitatory and inhibitory effects on a number of neurons in the cerebral and pedal ganglia, directed toward the initiation of prey capture behavior inClione. This bilaterally symmetrical neuron, designated Cr-PC (Cerebral interneuron initiating Prey Capture), produced monosynaptic activation of Cr-A motoneurons, which control buccal cone extrusion, and inhibition of Cr-B and Cr-L motoneurons, whose spike activities maintain buccal cones in a withdrawn position inside the head in non-feeding animals. In addition, Cr-PC produced monosynaptic activation of a number of swim motoneurons and interneurons of the swim central pattern generator (CPG) in the pedal ganglia, pedal serotonergic Pd-SW neurons involved in a peripheral modulation of swimming and the serotonergic Heart Excitor neuron.