Rapid Dopaminergic Signaling by Interneurons That Contain Markers for Catecholamines and GABA in the Feeding Circuitry of Aplysia

2005 ◽  
Vol 93 (4) ◽  
pp. 2142-2156 ◽  
Author(s):  
Manuel Díaz-Ríos ◽  
Mark W. Miller
Keyword(s):  
Motor Neurons ◽  
Receptor Agonist ◽  
Input Resistance ◽  
Pattern Generator ◽  
Feeding Behaviors ◽  
Motor Programs ◽  
Pharmacological Tests ◽  
Specific Manner ◽  
Rapid Signaling ◽  
Functional Output

Consummatory feeding behaviors in Aplysia californica are controlled by a polymorphic central pattern generator (CPG) circuit. Previous investigations have demonstrated colocalization of markers for GABA and catecholamines within two interneurons, B20 and B65, that participate in configuring the functional output of this CPG. This study examined the contributions of GABA and dopamine (DA) to rapid synaptic signaling from B20 and B65 to follower cells that implement their specification of motor programs. Pharmacological tests did not substantiate the participation of GABA in the mediation of the excitatory postsynaptic potentials (EPSPs) from either B20 or B65. However, GABA and the GABAB receptor agonist baclofen were found to modify these signals in a target-specific manner. Several observations indicated that DA acts as the neurotransmitter mediating fast EPSPs from B20 to two radula closer motor neurons B8 and B16. In both motor neurons, application of DA produced depolarizing responses associated with decreased input resistance and increased excitation. B20-evoked EPSPs in both follower cells were occluded by exogenous dopamine and blocked by the DA antagonist sulpiride. While dopamine occlusion and sulpiride block of convergent signaling to B8 from B65 resembled that of B20, both of these actions were less potent on the rapid signaling from B65 to the multifunctional and widely acting interneuron B4/5. These findings indicate that dopamine mediates divergent (B20 to B16 and B8) and convergent (B20 and B65 to B8) rapid EPSPs from two influential CPG interneurons in which it is colocalized with GABA-like immunoreactivity.

Tight or Loose Coupling Between Components of the Feeding Neuromusculature of Aplysia?

2005 ◽  
Vol 94 (1) ◽  
pp. 531-549 ◽  
Author(s):  
Yuriy Zhurov ◽  
Klaudiusz R. Weiss ◽  
Vladimir Brezina
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Neuromuscular System ◽  
Loose Coupling ◽  
Tight Coupling ◽  
Feeding Behaviors ◽  
Motor Programs ◽  
Firing Patterns ◽  
Functional Behavior ◽  
Tightly Coupled

Like other complex behaviors, the cyclical, rhythmic consummatory feeding behaviors of Aplysia—biting, swallowing, and rejection of unsuitable food—are produced by a complex neuromuscular system: the animal's buccal mass, with numerous pairs of antagonistic muscles, controlled by the firing of numerous motor neurons, all driven by the motor programs of a central pattern generator (CPG) in the buccal ganglia. In such a complex neuromuscular system, it has always been assumed that the activities of the various components must necessarily be tightly coupled and coordinated if successful functional behavior is to be produced. However, we have recently found that the CPG generates extremely variable motor programs from one cycle to the next, and so very variable motor neuron firing patterns and contractions of individual muscles. Here we show that this variability extends even to higher-level parameters of the operation of the neuromuscular system such as the coordination between entire antagonistic subsystems within the buccal neuromusculature. In motor programs elicited by stimulation of the esophageal nerve, we have studied the relationship between the contractions of the accessory radula closer (ARC) muscle, and the firing patterns of its motor neurons B15 and B16, with those of its antagonist, the radula opener (I7) muscle, and its motor neuron B48. There are two separate B15/B16-ARC subsystems, one on each side of the animal, and these are indeed very tightly coupled. Tight coupling can, therefore, be achieved in this neuromuscular system where required. Yet there is essentially no coupling at all between the contractions of the ARC muscles and those of the antagonistic radula opener muscle. We interpret this result in terms of a hypothesis that ascribes a higher-order benefit to such loose coupling in the neuromusculature. The variability, emerging in the successive feeding movements made by the animal, diversifies the range of movements and thereby implements a trial-and-error search through the space of movements that might be successful, an optimal strategy for the animal in an unknown, rapidly changing feeding environment.

scholarly journals Cell-selective modulation of the Drosophila neuromuscular system by a neuropeptide

2015 ◽  
Vol 113 (5) ◽  
pp. 1631-1643 ◽  
Author(s):  
Kiel G. Ormerod ◽  
Jacob L. Krans ◽  
A. Joffre Mercier
Keyword(s):  
Motor Neurons ◽  
Input Resistance ◽  
Muscle Cells ◽  
Fruit Fly ◽  
Physiological Properties ◽  
Selective Modulation ◽  
Specific Manner ◽  
A Cell ◽  
Evoked Contractions

Neuropeptides can modulate physiological properties of neurons in a cell-specific manner. The present work examines whether a neuropeptide can also modulate muscle tissue in a cell-specific manner using identified muscle cells in third-instar larvae of fruit flies. DPKQDFMRFa, a modulatory peptide in the fruit fly Drosophila melanogaster, has been shown to enhance transmitter release from motor neurons and to elicit contractions by a direct effect on muscle cells. We report that DPKQDFMRFa causes a nifedipine-sensitive drop in input resistance in some muscle cells (6 and 7) but not others (12 and 13). The peptide also increased the amplitude of nerve-evoked contractions and compound excitatory junctional potentials (EJPs) to a greater degree in muscle cells 6 and 7 than 12 and 13. Knocking down FMRFamide receptor (FR) expression separately in nerve and muscle indicate that both presynaptic and postsynaptic FR expression contributed to the enhanced contractions, but EJP enhancement was mainly due to presynaptic expression. Muscle ablation showed that DPKQDFMRFa induced contractions and enhanced nerve-evoked contractions more strongly in muscle cells 6 and 7 than cells 12 and 13. In situ hybridization indicated that FR expression was significantly greater in muscle cells 6 and 7 than 12 and 13. Taken together, these results indicate that DPKQDFMRFa can elicit cell-selective effects on muscle fibers. The ability of neuropeptides to work in a cell-selective manner on neurons and muscle cells may help explain why so many peptides are encoded in invertebrate and vertebrate genomes.

Synaptic regulation of cellular properties and burst oscillations of neurons in gastric mill system of spiny lobsters, Panulirus interruptus

1984 ◽  
Vol 52 (1) ◽  
pp. 54-73 ◽  
Author(s):  
D. F. Russell ◽  
D. K. Hartline
Keyword(s):  
Motor Neurons ◽  
Pattern Generator ◽  
Stomatogastric Ganglion ◽  
Gastric Mill ◽  
Panulirus Interruptus ◽  
Synaptic Regulation ◽  
Gastric Cells ◽  
Current Pulses ◽  
Regenerative Property ◽  
Stimulation Of

The properties of neurons in the stomatogastric ganglion (STG) participating in the pattern generator for the gastric mill rhythm were studied by intracellular current injection under several conditions: during ongoing gastric rhythms, in the nonrhythmic isolated STG, after stimulation of the nerve carrying central nervous system (CNS) inputs to the STG, or under Ba2+ or Sr2+. Slow regenerative depolarizations during ongoing rhythms were demonstrated in the anterior median, cardiopyloric, lateral cardiac, gastropyloric, and continuous inhibitor (AM, CP, LC, GP, and CI) neurons according to criteria such as voltage dependency, burst triggering, and termination by brief current pulses, etc. Experiments showed that regenerative-like behavior was not due to synaptic network interactions. The slow regenerative responses were abolished by isolating the stomatogastric ganglion but could be reestablished by stimulating the input nerve. This indicates that certain CNS inputs synaptically induce the regenerative property in specific gastric neurons. Slow regenerative depolarizations were not demonstrable in gastric mill (GM) motor neurons. Their burst oscillations and firing rate were instead proportional to injected current. CNS inputs evoked a prolonged depolarization in GM motor neurons, apparently by a nonregenerative mechanism. All the gastric cells showed prolonged regenerative potentials under 0.5-1.5 mM Ba2+. We conclude that the gastric neurons of the STG can be divided into three types according to their properties: those with a regenerative capability, a repetitively firing type, and a nonregenerative "proportional" type. The cells are strongly influenced by several types of CNS inputs, including "gastric command fibers."

scholarly journals Functional Genetic Screen to Identify Interneurons Governing Behaviorally Distinct Aspects of Drosophila Larval Motor Programs

2016 ◽  
Author(s):  
Matt Q. Clark ◽  
Stephanie J. McCumsey ◽  
Sereno Lopez-Darwin ◽  
Ellie S. Heckscher ◽  
Chris Q. Doe
Keyword(s):  
Motor Neurons ◽  
Animal Behavior ◽  
Motor Program ◽  
Genetic Screen ◽  
Muscle Contractions ◽  
Specific Expression ◽  
Motor Programs ◽  
Secondary Screen ◽  
Forward Locomotion ◽  
Sparse Pattern

AbstractDrosophila larval crawling is an attractive system to study patterned motor output at the level of animal behavior. Larval crawling consists of waves of muscle contractions generating forward or reverse locomotion. In addition, larvae undergo additional behaviors including head casts, turning, and feeding. It is likely that some neurons are used in all these behaviors (e.g. motor neurons), but the identity (or even existence) of neurons dedicated to specific aspects of behavior is unclear. To identify neurons that regulate specific aspects of larval locomotion, we performed a genetic screen to identify neurons that, when activated, could elicit distinct motor programs. We used 165 Janelia CRM-Gal4 lines – chosen for sparse neuronal expression – to express the warmth-inducible neuronal activator TrpA1 and screened for locomotor defects. The primary screen measured forward locomotion velocity, and we identified 63 lines that had locomotion velocities significantly slower than controls following TrpA1 activation (28°C). A secondary screen was performed on these lines, revealing multiple discrete behavioral phenotypes including slow forward locomotion, excessive reverse locomotion, excessive turning, excessive feeding, immobile, rigid paralysis, and delayed paralysis. While many of the Gal4 lines had motor, sensory, or muscle expression that may account for some or all of the phenotype, some lines showed specific expression in a sparse pattern of interneurons. Our results show that distinct motor programs utilize distinct subsets of interneurons, and provide an entry point for characterizing interneurons governing different elements of the larval motor program.

Modulation of Fictive Feeding by Dopamine and Serotonin inAplysia

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

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

Intrinsic and Extrinsic Modulation of a Single Central Pattern Generating Circuit

2000 ◽  
Vol 84 (3) ◽  
pp. 1186-1193 ◽  
Author(s):  
Peter T. Morgan ◽  
Ray Perrins ◽  
Philip E. Lloyd ◽  
Klaudiusz R. Weiss
Keyword(s):  
Neural Circuits ◽  
Central Pattern Generators ◽  
Motor Program ◽  
Pattern Generator ◽  
Motor Programs ◽  
Appetitive Behavior ◽  
Protraction Phase ◽  
Pattern Generators ◽  
Rhythmic Behaviors ◽  
Appetitive Behaviors

Intrinsic and extrinsic neuromodulation are both thought to be responsible for the flexibility of the neural circuits (central pattern generators) that control rhythmic behaviors. Because the two forms of modulation have been studied in different circuits, it has been difficult to compare them directly. We find that the central pattern generator for biting in Aplysia is modulated both extrinsically and intrinsically. Both forms of modulation increase the frequency of motor programs and shorten the duration of the protraction phase. Extrinsic modulation is mediated by the serotonergic metacerebral cell (MCC) neurons and is mimicked by application of serotonin. Intrinsic modulation is mediated by the cerebral peptide-2 (CP-2) containing CBI-2 interneurons and is mimicked by application of CP-2. Since the effects of CBI-2 and CP-2 occlude each other, the modulatory actions of CBI-2 may be mediated by CP-2 release. Although the effects of intrinsic and extrinsic modulation are similar, the neurons that mediate them are active predominantly at different times, suggesting a specialized role for each system. Metacerebral cell (MCC) activity predominates in the preparatory (appetitive) phase and thus precedes the activation of CBI-2 and biting motor programs. Once the CBI-2s are activated and the biting motor program is initiated, MCC activity declines precipitously. Hence extrinsic modulation prefacilitates biting, whereas intrinsic modulation occurs during biting. Since biting inhibits appetitive behavior, intrinsic modulation cannot be used to prefacilitate biting in the appetitive phase. Thus the sequential use of extrinsic and intrinsic modulation may provide a means for premodulation of biting without the concomitant disruption of appetitive behaviors.

5-Hydroxytryptamine Responses in Immature Rat Rostral Ventrolateral Medulla Neurons In Vitro

1998 ◽  
Vol 80 (3) ◽  
pp. 1033-1041 ◽  
Author(s):  
L. L. Hwang ◽  
N. J. Dun
Keyword(s):  
Receptor Antagonist ◽  
Receptor Agonist ◽  
Reversal Potential ◽  
Input Resistance ◽  
Rostral Ventrolateral Medulla ◽  
Ventrolateral Medulla ◽  
Immature Rat ◽  
Apparent Change ◽  
Biphasic Responses

Hwang, L. L. and N. J. Dun. 5-Hydroxytryptamine responses in immature rat rostral ventrolateral medulla neurons in vitro. J. Neurophysiol. 80: 1033–1041, 1998. Whole cell patch recordings were made from rostral ventrolateral medulla (RVLM) neurons of brainstem slices from 8- to 12-day-old rats. By superfusion or pressure ejection to RVLM neurons, 5-hydroxytryptamine (5-HT) elicited three types of membrane potential changes: a slow hyperpolarization (5-HTH), a slow depolarization (5-HTD) and a biphasic response, which persisted in a tetrodotoxin (TTX, 0.3 μM)-containing solution. 5-HTH were accompanied by a decrease of input resistance in the majority of responsive neurons. Hyperpolarization reduced and depolarization increased the 5-HTH; the mean reversal potential was −92.3 mV in 3.1 mM and shifted to −69.3 mV in 7 mM [K+]o. Barium (Ba2+, 0.1 mM) but not tetraethylammonium (TEA, 10 mM) suppressed 5-HTH. The 5-HT1A receptor agonist (±)-8-hydroxy-dipropylamino-tetralin (8-OH-DPAT; 5–50 μM) hyperpolarized RVLM neurons. The 5-HT1A antagonist pindobind-5-HT1A (PBD; 1–3 μM) and the 5-HT2/5-HT1 receptor antagonist spiperone (1–10 μM) suppressed 5-HTH and the hyperpolarizing phase of biphasic responses; the 5-HT2 receptor antagonist ketanserin (3 μM) was without significant effect. 5-HTD were associated with an increase or no apparent change of input resistance in RVLM neurons. Hyperpolarization of the membrane decreased or caused no apparent change in 5-HTD. 5-HTD were reduced in an elevated [K+]o (7.0 mM) solution and >60% in a low Na+ (26 mM) solution and were not significantly changed in a low Cl− (6.7 mM) or Ca2+-free/high Mg2+ (10.9 mM) solution. The 5-HT2 receptor agonist α-methyl-5-HT (50 μM) depolarized RVLM neurons, and the 5-HT2 antagonist ketanserin (1–10 μM) attenuated the 5-HTD and the depolarizing phase of biphasic responses, whereas the 5-HT1A receptor antagonist PBD (2 μM) was without effect. Inclusion of the hydrolysis resistant guanine nucleotide GDP-β-S in patch solution significantly reduced the 5-HTH as well as the 5-HTD. The present study shows that, in the immature rat RVLM neurons, 5-HT causes a slow hyperpolarization and depolarization probably by interacting with 5-HT1A and 5-HT2 receptors, which are G-proteins coupled. 5-HTH may involve an increase of an inwardly rectifying K+ conductance, and 5-HTD appear to be caused by a decrease of K+ conductance and/or increase of nonselective cation conductance.

Afferent-Induced Changes in Rhythmic Motor Programs in the Feeding Circuitry of Aplysia

2004 ◽  
Vol 92 (4) ◽  
pp. 2312-2322 ◽  
Author(s):  
Avniel N. Shetreat-Klein ◽  
Elizabeth C. Cropper
Keyword(s):  
Sensory Neurons ◽  
Motor Neurons ◽  
Rhythmic Activity ◽  
Motor Program ◽  
Firing Frequency ◽  
Afferent Activity ◽  
Motor Programs ◽  
Rhythmic Motor ◽  
Induced Changes ◽  
The Impact

A manipulation often used to determine whether a neuron plays a role in the generation of a motor program involves injecting current into the cell during rhythmic activity to determine whether activity is modified. We perform this type of manipulation to study the impact of afferent activity on feeding-like motor programs in Aplysia. We trigger biting-like programs and manipulate sensory neurons that have been implicated in producing the changes in activity that occur when food is ingested, i.e., when bites are converted to bite-swallows. Sensory neurons that are manipulated are the radula mechanoafferent B21 and the retraction proprioceptor B51. Data suggest that both cells are peripherally activated during radula closing/retraction when food is ingested. We found that phasic subthreshold depolarization of a single sensory neuron can significantly prolong radula closing/retraction, as determined by recording both from interneurons (e.g., B64), and motor neurons (e.g., B15 and B8). Additionally, afferent activity produces a delay in the onset of the subsequent radula opening/protraction, and increases the firing frequency of motor neurons. These are the changes in activity that are seen when food is ingested. These results add to the growing data that implicate B21 and B51 in bite to bite-swallow conversions and indicate that afferent activity is important during feeding in Aplysia.

Fast Synaptic Connections From CBIs to Pattern-Generating Neurons in Aplysia: Initiation and Modification of Motor Programs

2003 ◽  
Vol 89 (4) ◽  
pp. 2120-2136 ◽  
Author(s):  
Itay Hurwitz ◽  
Irving Kupfermann ◽  
Klaudiusz R. Weiss
Keyword(s):  
Central Pattern Generator ◽  
Motor Pattern ◽  
Aplysia Californica ◽  
Pattern Generator ◽  
Synaptic Connections ◽  
Motor Patterns ◽  
Motor Programs ◽  
Postsynaptic Potentials ◽  
Buccal Ganglia ◽  
Very High

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.

scholarly journals Output variability across animals and levels in a motor system

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Angela Wenning ◽  
Brian J Norris ◽  
Cengiz Günay ◽  
Daniel Kueh ◽  
Ronald L Calabrese
Keyword(s):  
Life History ◽  
Central Pattern Generator ◽  
Motor Neurons ◽  
Motor System ◽  
Motor Pattern ◽  
Pattern Generator ◽  
Phase Relations ◽  
The Other ◽  
Output Variability ◽  
Rhythmic Behaviors

Rhythmic behaviors vary across individuals. We investigated the sources of this output variability across a motor system, from the central pattern generator (CPG) to the motor plant. In the bilaterally symmetric leech heartbeat system, the CPG orchestrates two coordinations in the bilateral hearts with different intersegmental phase relations (Δϕ) and periodic side-to-side switches. Population variability is large. We show that the system is precise within a coordination, that differences in repetitions of a coordination contribute little to population output variability, but that differences between bilaterally homologous cells may contribute to some of this variability. Nevertheless, much output variability is likely associated with genetic and life history differences among individuals. Variability of Δϕ were coordination-specific: similar at all levels in one, but significantly lower for the motor pattern than the CPG pattern in the other. Mechanisms that transform CPG output to motor neurons may limit output variability in the motor pattern.

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