scholarly journals Actions of a histaminergic/peptidergic projection neuron on rhythmic motor patterns in the stomatogastric nervous system of the crabCancer borealis

2003 ◽  
Vol 469 (2) ◽  
pp. 153-169 ◽  
Author(s):  
Andrew E. Christie ◽  
Wolfgang Stein ◽  
John E. Quinlan ◽  
Mark P. Beenhakker ◽  
Eve Marder ◽  
...  
2010 ◽  
Vol 104 (2) ◽  
pp. 654-664
Author(s):  
Debra E. Wood ◽  
Melissa Varrecchia ◽  
Michael Papernov ◽  
Denise Cook ◽  
Devon C. Crawford

Neuromodulation is well known to provide plasticity in pattern generating circuits, but few details are available concerning modulation of motor pattern coordination. We are using the crustacean stomatogastric nervous system to examine how co-expressed rhythms are modulated to regulate frequency and maintain coordination. The system produces two related motor patterns, the gastric mill rhythm that regulates protraction and retraction of the teeth and the pyloric rhythm that filters food. These rhythms have different frequencies and are controlled by distinct mechanisms, but each circuit influences the rhythm frequency of the other via identified synaptic pathways. A projection neuron, MCN1, activates distinct versions of the rhythms, and we show that hormonal dopamine concentrations modulate the MCN1 elicited rhythm frequencies. Gastric mill circuit interactions with the pyloric circuit lead to changes in pyloric rhythm frequency that depend on gastric mill rhythm phase. Dopamine increases pyloric frequency during the gastric mill rhythm retraction phase. Higher gastric mill rhythm frequencies are associated with higher pyloric rhythm frequencies during retraction. However, dopamine slows the gastric mill rhythm frequency despite the increase in pyloric frequency. Dopamine reduces pyloric circuit influences on the gastric mill rhythm and upregulates activity in a gastric mill neuron, DG. Strengthened DG activity slows the gastric mill rhythm frequency and effectively reduces pyloric circuit influences, thus changing the frequency relationship between the rhythms. Overall dopamine shifts dependence of frequency regulation from intercircuit interactions to increased reliance on intracircuit mechanisms.


Author(s):  
Eve Marder

The crustacean stomatogastric nervous system has become one of the premier preparations used for the study of the mechanisms underlying the generation of rhythmic motor patterns. The stomatogastric ganglion (STG) contains about 30 neurons, most of which are motor neurons that innervate more than 40 sets of striated muscles that move the animal’s stomach. Descending projection neurons from the two commissural ganglia (CoGs) and the single oesophageal ganglion (OG) are important for the generation of the motor patterns produced by the STG. Identified sensory neurons project either into the CoGs to activate descending modulatory neurons, or directly into the STG.


1989 ◽  
Vol 61 (4) ◽  
pp. 833-844 ◽  
Author(s):  
P. S. Dickinson ◽  
E. Marder

1. The cardiac sac motor pattern consists of slow and irregular impulse bursts in the motor neurons [cardiac sac dilator 1 and 2 (CD1 and CD2)] that innervate the dilator muscles of the cardiac sac region of the crustacean foregut. 2. The effects of the peptides, proctolin and red pigment-concentrating hormone (RPCH), on the cardiac sac motor patterns produced by in vitro preparations of the combined stomatogastric nervous system [the stomatogastric ganglion (STG), the paired commissural ganglia (CGs), and the oesophageal ganglion (OG)] were studied. 3. Bath applications of either RPCH or proctolin activated the cardiac sac motor pattern when this motor pattern was not already active and increased the frequency of the cardiac sac motor pattern in slowly active preparations. 4. The somata of CD1 and CD2 are located in the esophageal and stomatogastric ganglia, respectively. Both neurons project to all four of the ganglia of the stomatogastric nervous system. RPCH elicited cardiac sac motor patterns when applied to any region of the stomatogastric nervous system, suggesting a distributed pattern generating network with multiple sites of modulation. 5. The anterior median (AM) neuron innervates the constrictor muscles of the cardiac sac. The AM usually functions as a part of the gastric mill pattern generator. However, when the cardiac sac is activated by RPCH applied to the stomatogastric ganglion, the AM neuron becomes active in antiphase with the cardiac sac dilator bursts. This converts the cardiac sac motor pattern from a one-phase rhythm to a two-phase rhythm. 6. These data show that a neuropeptide can cause a neuronal element to switch from being solely a component of one neuronal circuit to functioning in a second one as well. This example shows that peptidergic "reconfiguration" of neuronal networks can produce substantial changes in the behavior of associated neurons.


Author(s):  
Aaron P. Cook ◽  
Michael P. Nusbaum

Studies elucidating modulation of microcircuit activity in isolated nervous systems have revealed numerous insights regarding neural circuit flexibility, but this approach limits the link between experimental results and behavioral context. To bridge this gap, we studied feeding behavior-linked modulation of microcircuit activity in the isolated stomatogastric nervous system (STNS) of male Cancer borealis crabs. Specifically, we removed hemolymph from a crab that was unfed for ≥24 h ('unfed' hemolymph) or fed 15 min - 2 h before hemolymph removal ('fed' hemolymph). After feeding, the first significant foregut emptying occurred >1 h later and complete emptying required ≥6 h. We applied the unfed or fed hemolymph to the stomatogastric ganglion (STG) in an isolated STNS preparation from a separate, unfed crab to determine its influence on the VCN (ventral cardiac neuron)-triggered gastric mill (chewing)- and pyloric (filtering of chewed food) rhythms. Unfed hemolymph had little influence on these rhythms, but fed hemolymph from each examined time-point (15 min, 1- or 2 h post-feeding) slowed one or both rhythms without weakening circuit neuron activity. There were also distinct parameter changes associated with each time-point. One change unique to the 1 h time-point (i.e. reduced activity of one circuit neuron during the transition from the gastric mill retraction to protraction phase) suggested the fed hemolymph also enhanced the influence of a projection neuron which innervates the STG from a ganglion isolated from the applied hemolymph. Hemolymph thus provides a feeding state-dependent modulation of the two feeding-related motor patterns in the C. borealis STG.


2008 ◽  
Vol 99 (6) ◽  
pp. 3104-3122 ◽  
Author(s):  
Kristina J. Rehm ◽  
Adam L. Taylor ◽  
Stefan R. Pulver ◽  
Eve Marder

The stomatogastric nervous system (STNS) of the embryonic lobster is rhythmically active prior to hatching, before the network is needed for feeding. In the adult lobster, two rhythms are typically observed: the slow gastric mill rhythm and the more rapid pyloric rhythm. In the embryo, rhythmic activity in both embryonic gastric mill and pyloric neurons occurs at a similar frequency, which is slightly slower than the adult pyloric frequency. However, embryonic motor patterns are highly irregular, making traditional burst quantification difficult. Consequently, we used spectral analysis to analyze long stretches of simultaneous recordings from muscles innervated by gastric and pyloric neurons in the embryo. This analysis revealed that embryonic gastric mill neurons intermittently produced pauses and periods of slower activity not seen in the recordings of the output from embryonic pyloric neurons. The slow activity in the embryonic gastric mill neurons increased in response to the exogenous application of Cancer borealis tachykinin-related peptide 1a (CabTRP), a modulatory peptide that appears in the inputs to the stomatogastric ganglion (STG) late in larval development. These results suggest that the STG network can express adult-like rhythmic behavior before fully differentiated adult motor patterns are observed, and that the maturation of the neuromodulatory inputs is likely to play a role in the eventual establishment of the adult motor patterns.


1993 ◽  
Vol 181 (1) ◽  
pp. 1-26 ◽  
Author(s):  
J. M. Weimann ◽  
E. Marder ◽  
B. Evans ◽  
R. L. Calabrese

TNRNFLRFamide was isolated and sequenced from the stomatogastric nervous system of the crab Cancer borealis by reverse-phase high performance liquid chromatography followed by automated Edman degradation. An SDRNFLRFamide-like peptide that exactly co-migrated with SDRNFLRFamide was also observed. The effects of TNRNFLRFamide and SDRNFLRFamide on the gastric and pyloric rhythms of the stomatogastric nervous system of the crab Cancer borealis were studied. Both peptides activated pyloric rhythms in quiescent preparations in a dose-dependent manner with a threshold between 10(−11) and 10(−10) mol l-1. Both peptides increased the pyloric rhythm frequency of preparations showing moderate activity levels and had relatively little effect on preparations that showed strong pyloric rhythms prior to peptide application. Both peptides evoked gastric mill activity in preparations without existing gastric rhythms. The activation of the gastric rhythm is associated with activation of oscillatory properties in the dorsal gastric neurone. The induction of gastric rhythms by these peptides was accompanied by switches from pyloric-timed activity to gastric-timed activity by several stomatogastric ganglion neurones. Application of these peptides provides direct experimental control of circuit modification in the stomatogastric nervous system.


2001 ◽  
Vol 204 (12) ◽  
pp. 2035-2048 ◽  
Author(s):  
Petra Skiebe

SUMMARYThe stomatogastric nervous system (STNS) controls the movements of the foregut and the oesophagus of decapod crustaceans and is a good example for demonstrating that peptides are ubiquitously distributed chemical mediators in the nervous system. The stomatogastric ganglion (STG), one of the four ganglia of the STNS, contains the most intensively investigated neuronal circuits. The other ganglia, including the two commissural ganglia (CoGs) and the oesophageal ganglion (OG), are thought to be modulatory control centres. Peptides reach the STNS either as neurohormones or are released as transmitters. Peptide neurohormones can be released either from neurohaemal organs or from local neurohaemal release zones located on the surface of nerves and connectives. There were thought to be no peptidergic neurones with cell bodies in the STG itself. However, some have recently been described in adults of four species, in addition to a transient expression of peptides during development in two species. None of these peptidergic neurones has been investigated physiologically, in contrast to peptidergic neurones that project to the STG and have cell bodies in either the CoGs or the OG. It has been shown that neurones containing the same peptide elicit different motor patterns, that the peptide transmitter and the classical transmitter are not necessarily co-released and that the effect of a peptidergic neurone depends on its firing frequency and on which other modulatory neurones are co-active. The activity of modulatory projection neurones can be elicited by sensory neurones, and their activity can depend on the firing frequency of the sensory neurone. In addition to being found within the neuropile of ganglia, peptides are present in neuropile patches located within the nerves of the STNS, suggesting that these nerves can integrate as well as transfer information. Furthermore, sensory neurones and muscles exhibit peptide-like immunoreactivity and are modulated by peptides. Bath-applied peptides elicit peptide-specific motor patterns within the STG by targeting subsets of neurones. This divergence is contrasted by a convergence at the level of currents: five different peptides modulate a single current. Peptides not only induce motor patterns but can also switch the alliance of neurones from one network to another or are able to fuse different networks. In general, peptides are the most abundant group of modulators within the STNS; they are ubiquitously present, indicating that they play multiple roles in the plasticity of neural networks.


2009 ◽  
Vol 102 (5) ◽  
pp. 2866-2879 ◽  
Author(s):  
Ulrike B. S. Hedrich ◽  
Carmen R. Smarandache ◽  
Wolfgang Stein

Sensorimotor integration is known to occur at the level of motor circuits as well as in upstream interneurons that regulate motor activity. Here we show, using the crab stomatogastric nervous system (STNS) as a model, that different sensory systems affect the same set of projection neurons. However, they have qualitatively different effects on their activities (excitation vs. inhibition), and these differences contribute to the selection of motor patterns from multifunctional circuits. We compare the actions of the proprioceptive anterior gastric receptor (AGR) and the inferior ventricular (IV) neurons, which relay chemosensory information from the brain to the STNS, on modulatory commissural neurons 1 and 5 (MCN1 and MCN5) and commissural projection neuron 2 (CPN2) and their resulting actions on the gastric mill central pattern generating circuit in the stomatogastric ganglion. When stimulated, AGR and the IV neurons affect all three projection neurons but elicit distinct gastric mill rhythms. The effects of both sensory pathways on the projection neurons differ in the type of excitation provided to CPN2 and MCN5 (electrical vs. chemical) and the effect on MCN1 (direct inhibition by AGR vs. polysynaptic excitation by the IV neurons). The latter is functionally important because a restoration of MCN1 activity during the AGR rhythm made it more similar to that elicited by IV neuron stimulation. Our results thus support the hypothesis that sensory pathways activate different combinations of projection neurons to select distinct outputs from the same neuronal circuit.


1994 ◽  
Vol 72 (4) ◽  
pp. 1451-1463 ◽  
Author(s):  
B. J. Norris ◽  
M. J. Coleman ◽  
M. P. Nusbaum

1. In the isolated stomatogastric nervous system of the crab Cancer borealis (Fig. 1), the muscarinic agonist oxotremorine elicits several distinct gastric mill motor patterns from neurons in the stomatogastric ganglion (STG; Fig. 2). Selection of a particular gastric mill rhythm is determined by activation of distinct projection neurons that influence gastric mill neurons within the STG. In this paper we identify one such neuron, called commissural projection neuron 2 (CPN2), whose rhythmic activity is integral in producing one form of the gastric mill rhythm. 2. There is a CPN2 soma and neuropilar arborization in each commissural ganglion (CoG). The CPN2 axon projects through the superior esophageal nerve (son) and the stomatogastric nerve (stn) to influence neurons in the STG (Figs. 3 and 4A). 3. CPN2 activity influences most of the gastric mill neurons in the STG. Specifically, CPN2 excites gastric mill neurons GM and LG (gastric mill and lateral gastric, respectively) and inhibits the dorsal gastric (DG), anterior median (AM), medial gastric (MG), and inferior cardiac (IC) neurons (Figs. 5 and 6). CPN2 also indirectly inhibits gastric mill neurons Int1 and VD (interneuron 1 and ventricular dilator neuron, respectively) through its activation of LG. The CPN2 excitatory effects are mediated at least partly via discrete excitatory postsynaptic potentials (EPSPs; Fig. 4B), whereas its inhibitory effects are produced via smooth hyperpolarizations. 4. Within the CoG, CPN2 receives excitatory synaptic input from the anterior gastric receptor neuron (AGR), a gastric mill proprioceptive sensory neuron (Fig. 7) and inhibitory synaptic input from the gastric mill interneuron, Int1 (Fig. 8). 5. During one form of the gastric mill rhythm, CPN2 fires rhythmically in time with the gastric mill motor pattern, whereas it is silent or fires weakly during other gastric mill rhythms (Fig. 9). 6. When CPN2 rhythmic activity is suppressed during a CPN2-influenced gastric mill rhythm, the gastric mill rhythm continues, but the pattern is altered (Fig. 10). Moreover, transiently stimulating CPN2 during any ongoing gastric mill motor pattern can reset the timing of that rhythm (Fig. 11). 7. Tonic activity in CPN2 is insufficient to elicit a gastric mill rhythm (Fig. 12). Phasic activity in CPN2 can elicit a gastric mill rhythm only in preparations in which gastric mill neurons are already in an excited state (Figs. 12 and 13). 8. CPN2 recruitment plays a pivotal role in determining the final form of the gastric mill rhythm.(ABSTRACT TRUNCATED AT 400 WORDS)


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