ABSTRACT
Changes caused by learning that a food is inedible in Aplysia were examined for fast and slow synaptic connections from the buccal ganglia S1 cluster of mechanoafferents to five followers, in response to repeated stimulus trains. Learning affected only fast connections. For these, unique patterns of change were present in each follower, indicating that learning differentially affects the different branches of the mechanoafferents to their followers. In some followers, there were increases in either excitatory or inhibitory connections, and in others, there were decreases. Changes in connectivity resulted from changes in the amplitude of excitation or inhibition, or as a result of the number of connections, or of both. Some followers also exhibited changes in either within or between stimulus train plasticity as a result of learning. In one follower, changes differed from the different areas of the S1 cluster. The patterns of changes in connectivity were consistent with the behavioral changes produced by learning, in that they would produce an increase in the bias to reject or to release food, and a decrease in the likelihood to respond to food.
Subject(s)
Aplysia , Ganglia, Invertebrate , Motor Neurons , Aplysia/physiology , Animals , Motor Neurons/physiology , Ganglia, Invertebrate/physiology , Learning/physiology , Mechanoreceptors/physiology , Neuronal Plasticity/physiology , Food , Feeding Behavior/physiologyABSTRACT
How does repeated stimulation of mechanoafferents affect feeding motor neurons? Monosynaptic connections from a mechanoafferent population in the Aplysia buccal ganglia to five motor followers with different functions were examined during repeated stimulus trains. The mechanoafferents produced both fast and slow synaptic outputs, which could be excitatory or inhibitory. In contrast, other Aplysia mechanoafferents produce only fast excitation on their followers. In addition, patterns of synaptic connections were different to the different motor followers. Some followers received both fast excitation and fast inhibition, whereas others received exclusively fast excitation. All followers showed strong decreases in fast postsynaptic potential (PSP) amplitude within a stimulus train. Fast and slow synaptic connections were of net opposite signs in some followers but not in others. For one follower, synaptic contacts were not uniform from all subareas of the mechanoafferent cluster. Differences in properties of the buccal ganglia mechanoafferents and other Aplysia mechanoafferents may arise because the buccal ganglia neurons innervate the interior of the feeding apparatus, rather than an external surface, and connect to motor neurons for muscles with different motor functions. Fast connection patterns suggest that these synapses may be activated when food slips, biasing the musculature to release food. The largest slow inhibitory synaptic PSPs may contribute to a delay in the onset of the next behavior. Additional functions are also possible.
Subject(s)
Aplysia , Feeding Behavior , Ganglia, Invertebrate , Motor Neurons , Animals , Aplysia/physiology , Motor Neurons/physiology , Ganglia, Invertebrate/physiology , Feeding Behavior/physiology , Mechanoreceptors/physiology , Synapses/physiology , Physical StimulationABSTRACT
Learning causes local changes in synaptic connectivity and coordinated, global changes affecting many aspects of behavior. How do local synaptic changes produce global behavioral changes? In the hermaphroditic mollusc Aplysia, after learning that food is inedible, memory is expressed as bias to reject a food and to reduce responses to that food. We now show that memory is also expressed as an increased bias to reject even a nonfood object. The increased bias to rejection is partially explained by changes in synaptic connections from primary mechanoafferents to five follower neurons with well defined roles in producing different feeding behaviors. Previously, these mechanoafferents had been shown to play a role in memory consolidation. Connectivity changes differed for each follower neuron: the probability that cells were connected changed; excitation changed to inhibition and vice versa; and connection amplitude changed. Thus, multiple neural changes at different sites underlie specific aspects of a coordinated behavioral change. Changes in the connectivity between mechanoafferents and their followers cannot account for all of the behavioral changes expressed after learning, indicating that additional synaptic sites are also changed. Access to the circuit controlling feeding can help determine the logic and cellular mechanisms by which multiple local synaptic changes produce an integrated, global change in behavior.SIGNIFICANCE STATEMENT How do local changes in synapses affect global behavior? Studies on invertebrate preparations usually examine synaptic changes at specific neural sites, producing a specific behavioral change. However, memory may be expressed by multiple behavioral changes. We report that a change in behavior after learning in Aplysia is accomplished, in part, by regulating connections between mechanoafferents and their synaptic followers. For some followers, the connection probabilities change; for others, the connection signs are reversed; in others, the connection strength is modified. Thus, learning produces changes in connectivity at multiple sites, via multiple synaptic mechanisms that are consistent with the observed behavioral change.
Subject(s)
Adaptation, Physiological , Feeding Behavior , Learning , Synapses/physiology , Synaptic Potentials , Animals , Aplysia , Movement , Neural Inhibition , Neurons, Afferent/physiologyABSTRACT
A learning experience may lead to changes in behavior during the experience, and also to memory expressed at a later time. Are signals causing changes in behavior during the learning experience related to the formation and expression of memory? We examined this question, using learning that food is inedible in Aplysia Treatment of an isolated buccal ganglia preparation with an NO donor elicited rejection-like motor programs. Rejection initiated by NO production is consistent with aspects of behavioral changes seen while animals learn, and with memory formation. Nonetheless, applying the NO donor during training had only minor effects on behavior during the training, and did not improve memory, indicating that the induction of rejection in the buccal ganglia is unlikely to be the means by which NO during training contributes to memory formation. Block of NO during memory retrieval prevented the expression of memory, as measured by a lack of savings in time to stop responding to food. Applying an NO donor to the cerebral ganglion while eliciting fictive feeding inhibited the expression of feeding activity, indicating that some NO effects on memory consolidation and on expression of memory may be via effects on the cerebral ganglion.
Subject(s)
Aplysia/physiology , Feeding Behavior , Ganglia, Invertebrate/physiology , Memory/physiology , Nitric Oxide/physiology , Animals , Ganglia, Invertebrate/drug effects , Memory/drug effects , Motor Activity/drug effects , Neurons/drug effects , Neurons/physiology , Nitric Oxide/administration & dosageABSTRACT
BACKGROUND: Neural activity can be affected by nitric oxide (NO) produced by spiking neurons. Can neural activity also be affected by NO produced in neurons in the absence of spiking? METHODOLOGY/PRINCIPAL FINDINGS: Applying an NO scavenger to quiescent Aplysia buccal ganglia initiated fictive feeding, indicating that NO production at rest inhibits feeding. The inhibition is in part via effects on neurons B31/B32, neurons initiating food consumption. Applying NO scavengers or nitric oxide synthase (NOS) blockers to B31/B32 neurons cultured in isolation caused inactive neurons to depolarize and fire, indicating that B31/B32 produce NO tonically without action potentials, and tonic NO production contributes to the B31/B32 resting potentials. Guanylyl cyclase blockers also caused depolarization and firing, indicating that the cGMP second messenger cascade, presumably activated by the tonic presence of NO, contributes to the B31/B32 resting potential. Blocking NO while voltage-clamping revealed an inward leak current, indicating that NO prevents this current from depolarizing the neuron. Blocking nitrergic transmission had no effect on a number of other cultured, isolated neurons. However, treatment with NO blockers did excite cerebral ganglion neuron C-PR, a command-like neuron initiating food-finding behavior, both in situ, and when the neuron was cultured in isolation, indicating that this neuron also inhibits itself by producing NO at rest. CONCLUSION/SIGNIFICANCE: Self-inhibitory, tonic NO production is a novel mechanism for the modulation of neural activity. Localization of this mechanism to critical neurons in different ganglia controlling different aspects of a behavior provides a mechanism by which a humeral signal affecting background NO production, such as the NO precursor L-arginine, could control multiple aspects of the behavior.
Subject(s)
Feeding Behavior/physiology , Neural Inhibition/physiology , Neurons/physiology , Nitric Oxide/biosynthesis , Action Potentials/drug effects , Animals , Aplysia , Artifacts , Cells, Cultured , Cyclic N-Oxides/pharmacology , Feeding Behavior/drug effects , Ganglia, Invertebrate/drug effects , Ganglia, Invertebrate/physiology , Guanylate Cyclase/antagonists & inhibitors , Guanylate Cyclase/metabolism , Imidazoles/pharmacology , Intracellular Space/drug effects , Intracellular Space/physiology , Neural Inhibition/drug effects , Neurons/drug effects , Neurons/enzymology , Nitrergic Neurons/drug effects , Nitrergic Neurons/physiologyABSTRACT
Synaptic connections from a neuron onto itself (autapses) are not uncommon, but their contributions to information processing and behavior are not fully understood. Positive feedback mediated by autapses could in principle give rise to persistent activity, a property of some neurons in which a brief stimulus causes a long-lasting response. We have identified an autapse that underlies a plateau potential causing persistent activity in the B31/B32 neurons of Aplysia. The persistent activity is essential to the ability of these neurons to initiate and maintain components of feeding behavior. Persistent activity in B31/B32 arises from a voltage-dependent muscarinic autapse and from pharmacologically identical network-based positive feedback. Depolarization via the autapse begins later than network-driven excitation, and the effect of the autapse is therefore overshadowed by the earlier network-based depolarization. In B31/B32 neurons isolated in culture only the autapse is present, and the autapse functionally replaces the missing network-based feedback. Properties of B31/B32 provide insight into a possible general function of autapses. Autapses might function along with synapses from presynaptic neurons as components of feedback loops.
Subject(s)
Feeding Behavior/physiology , Motor Neurons/physiology , Synapses/physiology , Animals , Aplysia/physiology , Axons/physiology , Behavior, Animal/physiology , Evoked Potentials/physiology , Feedback , Ganglia/physiology , Membrane Potentials/physiology , Receptors, Muscarinic/physiology , Sensory Thresholds/physiologyABSTRACT
Biophysical properties of neurons contributing to the ability of an animal to decide whether or not to respond were examined. B31/B32, two pairs of bilaterally symmetrical Aplysia neurons, are major participants in deciding to initiate a buccal motor program, the neural correlate of a consummatory feeding response. B31/B32 respond to an adequate stimulus after a delay, during which time additional stimuli influence the decision to respond. B31/B32 then respond with a ramp depolarization followed by a sustained soma depolarization and axon spiking that is the expression of a commitment to respond to food. Four currents contributing to decision making in B31/B32 were characterized, and their functional effects were determined, in current- and voltage-clamp experiments and with simulations. Inward currents arising from slow muscarinic transmission were characterized. These currents contribute to the B31/B32 depolarization. Their slow activation kinetics contribute to the delay preceding B31/B32 activity. After the delay, inward currents affect B31/B32 in the context of two endogenous inactivating outward currents: a delayed rectifier K+ current (I(K-V)) and an A-type K+ current (I(K-A)), as well as a high-threshold noninactivating outward current (I(maintained)). Hodgkin-Huxley kinetic analyses were performed on the outward currents. Simulations using equations from these analyses showed that I(K-V) and I(K-A) slow the ramp depolarization preceding the sustained depolarization. The three outward currents contribute to braking the B31/B32 depolarization and keeping the sustained depolarization at a constant voltage. The currents identified are sufficient to explain the properties of B31/B32 that play a role in generating the decision to feed.
Subject(s)
Aplysia/cytology , Decision Making/physiology , Electric Stimulation , Locomotion/physiology , Motor Neurons/radiation effects , 4-Aminopyridine/pharmacology , Action Potentials/drug effects , Action Potentials/physiology , Action Potentials/radiation effects , Animals , Behavior, Animal , Computer Simulation , Dose-Response Relationship, Radiation , Drug Interactions , Electric Conductivity , Locomotion/radiation effects , Models, Neurological , Motor Neurons/drug effects , Motor Neurons/physiology , Muscarinic Agonists/pharmacology , Oxotremorine/pharmacology , Patch-Clamp Techniques , Potassium Channel Blockers/pharmacology , Sodium Channel Blockers/pharmacology , Tetraethylammonium/pharmacology , Tetrodotoxin/pharmacology , Time FactorsABSTRACT
Inhibiting nitric oxide (NO) synthesis during learning that food is inedible in Aplysia blocks subsequent memory formation. To gain insight into the function of NO transmission during learning we tested whether blocking NO synthesis affects aspects of feeding that are expressed both in a nonlearning context and during learning. Inhibiting NO synthesis with L-NAME and blocking guanylyl cyclase with methylene blue decreased the efficacy of ad libitum feeding. D-NAME had no effect. L-NAME also decreased rejection responses frequency, but did not affect rejection amplitude. The effect of L-NAME was explained by a decreased signaling that efforts to swallow are not successful, leading to a decreased rejection rate, and a decreased ability to reposition and subsequently consume food in ad libitum feeding. Signaling that animals have made an effort to swallow is a critical component of learning that food is inedible. Stimulation of the lips with food alone did not produce memory, but stimulation combined with the NO donor SNAP did produce memory. Exogenous NO at a concentration causing memory also excited a key neuron responding to NO, the MCC. Block of the cGMP second-messenger cascade during training by methylene blue also blocked memory formation after learning. Our data indicate that memory arises from the contingency of three events during learning that food is inedible. One of the events is efforts to swallow, which are signaled by NO by cGMP.
Subject(s)
Aplysia/physiology , Feeding Behavior/physiology , Learning/physiology , Memory/physiology , Nitric Oxide/physiology , Animals , Avoidance Learning/drug effects , Avoidance Learning/physiology , Choice Behavior , Feeding Behavior/drug effects , Learning/drug effects , Memory/drug effects , Methylene Blue/pharmacology , NG-Nitroarginine Methyl Ester/pharmacology , Signal TransductionABSTRACT
The patterning of feeding and the quantity eaten in Aplysia californica with ad libitum food access cannot be explained by the effects of three variables previously shown to control the patterning of consummatory feeding responses and the quantity eaten in animals hand-fed individual meals. Feeding in ad libitum conditions is regulated primarily by varying the time between feeding bouts rather than by modulating bout lengths or the efficacy of consummatory movements within a bout. Aplysia with steady-state food access are in a newly characterized feeding state in which they are relatively unresponsive to food. They eat very little (1-4% of the time), and the quantity eaten is unrelated to the quantity of food in the anterior gut. The steady state can be maintained by the presence of food, even if animals do not contact food. The chemosensory rhinophores signal the presence of food that maintains the steady state. Up to 24 h without food is needed for animals to recover from the inhibition of feeding by steady-state presence of food. Recovery from the steady state is partially governed by postingestion stimuli as shown by a faster recovery in animals that have not been in contact with food. Inhibition of feeding during the steady-state is mediated in part via humoral factors because bathing the cerebral and buccal ganglia in hemolymph from animals in the steady state inhibits the ability to elicit buccal motor programs via a cholinomimetic thought to simulate stimulation of the lips with food. After food deprivation that is sufficiently long so that the steady-state decays, animals eat a large meal the size and dynamics of which are consistent with regulation via the three variables previously identified. This large meal is modulated by pheromones secreted by conspecifics even in sexually immature Aplysia.
Subject(s)
Aplysia/physiology , Appetite/physiology , Eating/physiology , Feeding Behavior/physiology , Food Deprivation/physiology , Hunger/physiology , Satiation/physiology , Animals , Time FactorsABSTRACT
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.
Subject(s)
Action Potentials/physiology , Aplysia/physiology , Feeding Behavior/physiology , Interneurons/physiology , Neural Inhibition/physiology , Presynaptic Terminals/physiology , Animals , Biological Clocks/physiology , In Vitro TechniquesABSTRACT
Growing evidence suggests that different forms of complex motor acts are constructed through flexible combinations of a small number of modules in interneuronal networks. It remains to be established, however, whether a module simply controls groups of muscles and functions as a computational unit for use in multiple behaviors (behavior independent) or whether a module controls multiple salient features that define one behavior and is used primarily for that behavior (behavior specific). We used the Aplysia feeding motor network to examine the two proposals by studying the functions of identifiable interneurons. We identified three types of motor programs that resemble three types of behaviors that Aplysia produce: biting, swallowing, and rejection. Two ingestive programs (biting, swallowing) are defined by two movement parameters of the feeding apparatus (the radula): one is the same in both programs (phasing of radula closure motoneurons relative to radula protraction-retraction), whereas the other parameter (protraction duration) is different in the two programs. In each program, these two parameters were specified together by an individual neuron, but the neurons in each were different (B40 for biting, B30 for swallowing). These findings support the existence of behavior-specific modules. Furthermore, neuron B51 was found to mediate a phase that can be flexibly added on to both ingestive and egestive-rejection programs, suggesting that B51 may be a behavior-independent module. The functional interpretation of the role played by these modules is supported by the patterns of synaptic connectivity that they make. Thus, both behavior-specific and behavior-independent modules are used to construct complex behaviors.
Subject(s)
Aplysia/physiology , Feeding Behavior/physiology , Interneurons/physiology , Motor Neurons/physiology , Movement/physiology , Nerve Net/physiology , Animals , Cluster Analysis , Deglutition/physiology , Ganglia, Invertebrate/physiology , Mastication/physiology , Models, NeurologicalABSTRACT
Nitric oxide (NO) is widely used in neural circuits giving rise to learning and memory. NO is an unusual neurotransmitter in its modes of release and action. Is its association with learning and memory related to its unusual properties? Reviewing the literature might allow the formulation of a general principle on how NO and memory are related. However, other than confirming that there is indeed a strong association between NO and memory, no simple rules emerge on the role of NO in learning and memory. The effects of NO are not associated with a particular stage or form of memory and are highly dependent on species, strain, and behavior or training paradigm. Nonetheless, a review does provide hints on why NO is associated with learning and memory. Unlike transmitters acting via receptors expressed only in neurons designed to respond to the transmitter, NO is a promiscuous signal that can affect a wide variety of neurons, via many molecular mechanisms. In circuits giving rise to learning and memory, it may be useful to signal some events via a promiscuous messenger having widespread effects. However, each circuit will use the promiscuous signal in a different way, to achieve different ends.
Subject(s)
Memory/physiology , Neuronal Plasticity/physiology , Nitric Oxide/physiology , Animals , Behavior, Animal , Models, Neurological , Nerve Net/physiology , Synaptic Transmission/physiologyABSTRACT
Mediation of mother-infant interactions by the brain-gut peptide cholecystokinin (CCK) was examined by observing behavior of Otsuka Long-Evans Tokushima Fatty (OLETF) rats, which lack functional CCKA receptors because of a genetic abnormality. OLETF (n = 10) and control (Long-Evans Tokushima Otsuka [LETO] n = 10) dams interacted with 1 pup of each line on Postpartum Days 6-9. OLETF pups received more body and anogenital licking and emitted substantially more ultrasonic vocalizations than LETO pups. OLETF dams carried pups less frequently and showed a nursing position more frequently than LETO dams. No significant Pup X Dam Line interactions or line differences in dams' activity were detected. The results provide convergent validity to previous pharmacological studies implicating CCK mediation of both infant and maternal behavior.
Subject(s)
Brain/metabolism , Maternal Behavior/physiology , Object Attachment , Receptors, Cholecystokinin/metabolism , Animals , Dopamine/metabolism , Female , Nucleus Accumbens/metabolism , Pregnancy , Random Allocation , Rats , Reinforcement, PsychologyABSTRACT
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.
Subject(s)
Aplysia/physiology , Feeding Behavior/physiology , Nerve Net/physiology , Neurons/physiology , Action Potentials/physiology , Animals , Behavior, Animal , Digestive System Physiological Phenomena , Feedback , Ganglia, Invertebrate/cytology , Ganglia, Invertebrate/physiology , Motor Activity , Nerve Net/cytology , Neural Inhibition , Neural Networks, Computer , Neurons/classificationABSTRACT
Consummatory feeding movements in Aplysia californica are organized by a central pattern generator (CPG) in the buccal ganglia. Buccal motor programs similar to those organized by the CPG are also initiated and controlled by the cerebro-buccal interneurons (CBIs), interneurons projecting from the cerebral to the buccal ganglia. To examine the mechanisms by which CBIs affect buccal motor programs, we have explored systematically the synaptic connections from three of the CBIs (CBI-1, CBI-2, CBI-3) to key buccal ganglia CPG neurons (B31/B32, B34, and B63). The CBIs were found to produce monosynaptic excitatory postsynaptic potentials (EPSPs) with both fast and slow components. In this report, we have characterized only the fast component. CBI-2 monosynaptically excites neurons B31/B32, B34, and B63, all of which can initiate motor programs when they are sufficiently stimulated. However, the ability of CBI-2 to initiate a program stems primarily from the excitation of B63. In B31/B32, the size of the EPSPs was relatively small and the threshold for excitation was very high. In addition, preventing firing in either B34 or B63 showed that only a block in B63 firing prevented CBI-2 from initiating programs in response to a brief stimulus. The connections from CBI-2 to the buccal ganglia neurons showed a prominent facilitation. The facilitation contributed to the ability of CBI-2 to initiate a BMP and also led to a change in the form of the BMP. The cholinergic blocker hexamethonium blocked the fast EPSPs induced by CBI-2 in buccal ganglia neurons and also blocked the EPSPs between a number of key CPG neurons within the buccal ganglia. CBI-2 and B63 were able to initiate motor patterns in hexamethonium, although the form of a motor pattern was changed, indicating that non-hexamethonium-sensitive receptors contribute to the ability of these cells to initiate bursts. By contrast to CBI-2, CBI-1 excited B63 but inhibited B34. CBI-3 excited B34 and not B63. The data indicate that CBI-1, -2, and -3 are components of a system that initiates and selects between buccal motor programs. Their behavioral function is likely to depend on which combination of CBIs and CPG elements are activated.
Subject(s)
Interneurons/physiology , Motor Neurons/physiology , Neural Pathways/physiology , Synapses/physiology , Action Potentials/drug effects , Action Potentials/physiology , Animals , Aplysia , Excitatory Postsynaptic Potentials/drug effects , Excitatory Postsynaptic Potentials/physiology , Ganglionic Blockers/pharmacology , Hexamethonium/pharmacology , Mouth/innervation , Movement/physiologyABSTRACT
The buccal ganglia of Aplysia contain a central pattern generator (CPG) that organizes the rhythmic movements of the radula and buccal mass during feeding. Many of the cellular and synaptic elements of this CPG have been identified and characterized. However, the roles that specific cellular and synaptic properties play in generating patterns of activity are not well understood. To examine these issues, the present study developed computational models of a portion of this CPG and used simulations to investigate processes underlying the initiation of patterned activity. Simulations were done with the SNNAP software package. The simulated network contained two neurons, B31/B32 and B63. The development of the model was guided and constrained by the available current-clamp data that describe the properties of these two protraction-phase interneurons B31/B32 and B63, which are coupled via electrical and chemical synapses. Several configurations of the model were examined. In one configuration, a fast excitatory postsynaptic potential (EPSP) from B63 to B31/B32 was implemented in combination with an endogenous plateau-like potential in B31/B32. In a second configuration, the excitatory synaptic connection from B63 to B31/B32 produced both fast and slow EPSPs in B31/B32 and the plateau-like potential was removed from B31/B32. Simulations indicated that the former configuration (i.e., electrical and fast chemical coupling in combination with a plateau-like potential) gave rise to a circuit that was robust to changes in parameter values and stochastic fluctuations, that closely mimicked empirical observations, and that was extremely sensitive to inputs controlling the onset of a burst. The coupling between the two simulated neurons served to amplify exogenous depolarizations via a positive feedback loop and the subthreshold activation of the plateau-like potential. Once a burst was initiated, the circuit produced the program in an all-or-none fashion. The slow kinetics of the simulated plateau-like potential played important roles in both initiating and maintaining the burst activity. Thus the present study identified cellular and network properties that contribute to the ability of the simulated network to integrate information over an extended period before a decision is made to initiate a burst of activity and suggests that similar mechanisms may operate in the buccal ganglia in initiating feeding movements.