Peptidergic modulation of a multioscillator system in the lobster. I. Activation of the cardiac sac motor pattern by the neuropeptides proctolin and red pigment-concentrating hormone

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):  
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.


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.


1997 ◽  
Vol 78 (6) ◽  
pp. 3210-3221 ◽  
Author(s):  
Bruce R. Johnson ◽  
Ronald M. Harris-Warrick

Johnson, Bruce R. and Ronald M. Harris-Warrick. Amine modulation of glutamate responses from pyloric motor neurons in lobster stomatogastric ganglion. J. Neurophysiol. 78: 3210–3221, 1997. The amines dopamine (DA), serotonin (5-HT), and octopamine (Oct) each elicit a distinctive motor pattern from a quiescent pyloric network in the lobster stomatogastric ganglion (STG). We previously have demonstrated that these amines alter the synaptic strength at multiple, distributed sites within the pyloric network that could contribute to the amine-induced motor patterns. Here, we examined the postsynaptic contribution to these changes in synaptic strength by determining how the amines modify responses of pyloric motor neurons to glutamate (Glu), one of the network transmitters, applied iontophoretically into the STG neuropil. Dopamine reduced the Glu responses of the pyloric dilator (PD), ventricular dilator (VD), and inferior cardiac (IC) neurons and enhanced the Glu responses of the lateral pyloric (LP) and pyloric constrictor (PY) neurons. The only effect of 5-HT was to reduce the Glu response of the VD neuron. Oct enhanced the Glu responses of the LP and PY neurons but did not affect the PD, VD, and IC responses. We also examined amine effects on the depolarizing responses to iontophoresed acetylcholine (ACh) in the PD and VD and found that they paralleled the amine effects on Glu responses in these neurons. This suggests that amine modulation of PD and VD responses to Glu and ACh may be explained by general changes in the ionic conductance of these neurons. We compare our results with our earlier work describing amine effects on synaptic strength and input resistance to show that amines act at both pre- and postsynaptic sites to modify graded synaptic transmission in the pyloric network.


1992 ◽  
Vol 68 (5) ◽  
pp. 1693-1707 ◽  
Author(s):  
G. Wittenberg ◽  
W. B. Kristan

1. Mechanical stimulation of the leech, Hirudo medicinalis, elicits withdrawal behavior that has two components: local bending in the segment stimulated and shortening in outlying segments. Local bending is characterized by excitation of longitudinal muscle on one side of the segment and inhibition on the other side. In shortening, all longitudinal muscles are excited. We wished to understand how these distinct motor patterns are produced by a nervous system with segmentally iterated neurons, a configuration that places some limitations on the complexity of connection patterns. 2. We searched for neurons in the segmental nervous system that subserved shortening behavior, expecting to find at least one interneuron in each segment that was involved in shortening behavior exclusively. We found instead that all interneurons involved in shortening are also involved in local bending, and no individual interneuron can completely account for shortening. 3. The motor output caused by individual identified interneurons is not entirely consistent with the shortening motor output pattern. For instance, one interneuron, cell 115, has the same pattern of motor effects from segment to segment, causing excitation of dorsal excitatory motor neurons and inhibition of ventral excitatory motor neurons. These effects would cause dorsal local bending, not shortening, in a few segments. Only one interneuron, cell 125, has motor effects that would cause shortening. 4. Individual interneurons were hyperpolarized while single sensory cells were stimulated, to quantify the contributions of individual interneurons to the observed motor pattern. Interneurons 115 and 125, and the inhibitory motor neuron, cell 1, were found to have significant roles in producing the shortening motor output. 5. A quantitative estimate of the role of each interneuron type showed that the identified interneurons account for most of the excitation of dorsal motor neurons, but for very little of the excitation of ventral motor neurons. This predicts that at least one additional interneuron type remains to be identified, one that would provide excitation to ventral motor neurons in several segments. 6. A back-propagation trained neural network model was constructed to predict the connections of the as yet unidentified interneurons. To match the known properties of interneurons, it was necessary to include a segmental similarity constraint in the training algorithm for segmentally iterated model neurons. The modeled networks predicted that there are at least two kinds of interneurons yet to be found. Also, the modeling showed that interneurons can have input and output patterns that differ very little from segment to segment but yet produce major differences in the motor output.


2006 ◽  
Vol 95 (6) ◽  
pp. 3617-3632 ◽  
Author(s):  
Dirk Bucher ◽  
Adam L. Taylor ◽  
Eve Marder

Neuronal firing patterns can contain different temporal information. It has long been known that the fast pyloric and the slower gastric motor patterns in the stomatogastric ganglion of decapod crustaceans interact. However, the bidirectional influences between the pyloric rhythm and the gastric mill rhythm have not been quantified in detail from preparations that spontaneously express both patterns in vitro. We found regular and stable spontaneous gastric and pyloric activity in 71% of preparations of the isolated stomatogastric nervous system of the lobster, Homarus americanus. The gastric [cycle period: 10.96 ± 2.67 (SD) s] and pyloric (cycle period: 1.35 ± 0.18 s) patterns showed bidirectional interactions and coordination. Gastric neuron firing showed preferred phases within the reference frame of the pyloric cycle. The relative timing and burst parameters of the pyloric neurons systematically changed within the reference frame of the gastric cycle. The gastric rhythm showed a tendency to run at cycle periods that were integer multiples of the pyloric periods, but coupling and coordination between the two rhythms were variable. We used power spectra to quantify the gastric and pyloric contributions to the firing pattern of each individual neuron. This provided us with a way to analyze the firing pattern of each gastric and pyloric neuron type individually without reference to either gastric or pyloric phase. Possible functional consequences of these network interactions for motor output are discussed.


1994 ◽  
Vol 194 (1) ◽  
pp. 195-208 ◽  
Author(s):  
P Skiebe ◽  
H Schneider

The effects of four Diploptera punctata allatostatin peptides on the stomatogastric nervous system of the crab Cancer borealis were studied. All of the peptides had similar actions on the activity of neurons involved in rhythmic movements of the pyloric region of the stomach, decreasing the frequency of the pyloric rhythm in a dose-dependent manner. Diploptera allatostatin 3 (D-AST-3) was slightly more effective than the others. The absolute change in the frequency of the pyloric rhythm depended on the starting frequency, demonstrating that the effect of D-AST-3 depends on the preceding physiological state of the preparation. The largest decreases were observed when the starting frequency was slower than 0.8 Hz. Whole-mount immunocytochemistry with anti-Diploptera allatostatin 1 antibodies demonstrated the presence of allatostatin-like peptides in the paired commissural ganglia, the unpaired oesophageal ganglion and the stomatogastric ganglion, and in their connecting and motor nerves. Dense processes were labeled in the stomatogastric ganglion, 12-19 cell bodies and neuropil staining were found in each commissural ganglion, two cell bodies were stained in the oesophageal ganglion and two pairs of cell bodies, the gastropyloric receptor neurons, were stained in peripheral nerves.


1998 ◽  
Vol 79 (3) ◽  
pp. 1396-1408 ◽  
Author(s):  
Stefan Clemens ◽  
Denis Combes ◽  
Pierre Meyrand ◽  
John Simmers

Clemens, Stefan, Denis Combes, Pierre Meyrand, and John Simmers. Long-term expression of two interacting motor pattern-generating networks in the stomatogastric system of freely behaving lobster. J. Neurophysiol. 79: 1396–1408, 1998. Rhythmic movements of the gastric mill and pyloric regions of the crustacean foregut are controlled by two stomatogastric neuronal networks that have been intensively studied in vitro. By using electromyographic recordings from the European lobster, Homarus gammarus, we have monitored simultaneously the motor activity of pyloric and gastric mill muscles for ≤3 mo in intact and freely behaving animals. Both pyloric and gastric mill networks are almost continuously active in vivo regardless of the presence of food. In unfed resting animals kept under “natural-like” conditions, the pyloric network expresses the typical triphasic pattern seen in vitro but at considerably slower cycle periods (2.5–3.5 s instead of 1–1.5 s). Gastric mill activity occurs at mean cycle periods of 20–50 s compared with 5–10 s in vitro but may suddenly stop for up to tens of minutes, then restart without any apparent behavioral reason. When conjointly active, the two networks express a strict coupling that involves certain but not all motor neurons of the pyloric network. The posterior pyloric constrictor muscles, innervated by a total of 8 pyloric (PY) motor neurons, are influenced by the onset of each gastric mill medial gastric/lateral gastric(MG/LG) neuron powerstroke burst, and for one cycle, PY neuron bursts may attain >300% of their mean duration. However, the duration of activity in the lateral pyloric constrictor muscle, innervated by the unique lateral pyloric (LP) motor neuron, remains unaffected by this perturbation. During this period after gastric perturbation, LP neuron and PY neurons thus express opposite burst-to-period relationships in that LP neuron burst duration is independent of the ongoing cycle period, whereas PY neuron burst duration changes with period length. In vitro the same type of gastro-pyloric interaction is observed, indicating that it is not dependent on sensory inputs. Moreover, this interaction is intrinsic to the stomatogastric ganglion itself because the relationship between the two networks persists after suppression of descending inputs to the ganglion. Intracellular recordings reveal that thisgastro-pyloric interaction originates from the gastric MG and LG neurons of the gastric network, which inhibit the pyloric pacemaker ensemble. As a consequence, the pyloric PY neurons, which are inhibited by the pyloric dilator (PD) neurons of the pyloric pacemaker group, extend their activity during the time that PD neuron is held silent. Moreover, there is evidence for a pyloro-gastric interaction, apparently rectifying, from the pyloric pacemakers back to the gastric MG/LG neuron group.


1987 ◽  
Vol 58 (3) ◽  
pp. 584-597 ◽  
Author(s):  
B. Mulloney ◽  
L. D. Acevedo ◽  
A. G. Bradbury

1. The swimmeret system can be excited by perfusing the neuropeptide proctolin through the isolated ventral nerve cord of the crayfish. Previously silent preparations begin to generate a characteristic motor pattern, the swimmeret rhythm, in the nerves that innervate the swimmerets. The response to proctolin is dose dependent and reversible. The threshold concentration of proctolin perfused through the ventral artery is approximately 10(-8) M. The EC50 is 1.6 X 10(-6) M. 2. Proctolin-induced motor patterns have periods and phases similar to those of spontaneously generated motor patterns. The durations of the bursts of impulses in power-stroke motor neurons generated in the presence of proctolin are, however, significantly longer than those that occur during spontaneous activity. 3. DL-Octopamine inhibits the swimmeret system, both when the system is spontaneously active and when it has been excited by proctolin. The inhibition by octopamine is dose dependent and reversible. The threshold for inhibition is approximately 10(-6) M, and the EC50 is approximately 5 X 10(-5) M. 4. Octopamine's effect is mimicked by its agonists, synephrine and norepinephrine. Synephrine has a lower threshold concentration than does octopamine, but norepinephrine is much less effective than octopamine. 5. Octopamine's inhibition is partially blocked by an antagonist, phentolamine. 6. Phentolamine also blocks inhibition of the swimmeret system by inhibitory command interneurons. This block is dose dependent and can be partially overcome by stimulating the command interneurons at higher frequencies. 7. Perfusion with 11 other suspected crustacean neurotransmitters and transmitter analogues did not similarly excite or inhibit the swimmeret system, so we suggest that proctolin and octopamine are transmitters used by the neurons that normally control expression of the swimmeret rhythm.


2015 ◽  
Vol 113 (6) ◽  
pp. 1921-1940 ◽  
Author(s):  
D. Ryczko ◽  
J. Knüsel ◽  
A. Crespi ◽  
S. Lamarque ◽  
A. Mathou ◽  
...  

In tetrapods, limb and axial movements are coordinated during locomotion. It is well established that inter- and intralimb coordination show considerable variations during ongoing locomotion. Much less is known about the flexibility of the axial musculoskeletal system during locomotion and the neural mechanisms involved. Here we examined this issue in the salamander Pleurodeles waltlii, which is capable of locomotion in both aquatic and terrestrial environments. Kinematics of the trunk and electromyograms from the mid-trunk epaxial myotomes were recorded during four locomotor behaviors in freely moving animals. A similar approach was used during rhythmic struggling movements since this would give some insight into the flexibility of the axial motor system. Our results show that each of the forms of locomotion and the struggling behavior is characterized by a distinct combination of mid-trunk motor patterns and cycle durations. Using in vitro electrophysiological recordings in isolated spinal cords, we observed that the spinal networks activated with bath-applied N-methyl-d-aspartate could generate these axial motor patterns. In these isolated spinal cord preparations, the limb motor nerve activities were coordinated with each mid-trunk motor pattern. Furthermore, isolated mid-trunk spinal cords and hemicords could generate the mid-trunk motor patterns. This indicates that each side of the cord comprises a network able to generate coordinated axial motor activity. The roles of descending and sensory inputs in the behavior-related changes in axial motor coordination are discussed.


2019 ◽  
Author(s):  
Kritika S. Katiyar ◽  
Laura A. Struzyna ◽  
Suradip Das ◽  
D. Kacy Cullen

AbstractThe central feature of peripheral motor axons is their remarkable lengths as they project from a motor neuron residing in the spinal cord to an often-distant target muscle. However, to date in vitro models have not replicated this central feature owing to challenges in generating motor axon tracts beyond a few millimeters in length. To address this, we have developed a novel combination of micro-tissue engineering and mechanically assisted growth techniques to create long-projecting centimeter-scale motor axon tracts. Here, primary motor neurons were isolated from the spinal cords of rats and induced to form engineered micro-spheres via forced aggregation in custom micro-wells. This three-dimensional micro-tissue yielded healthy motor neurons projecting dense, fasciculated axonal tracts. Within our custom-built mechanobioreactors, motor neuron culture conditions, neuronal/axonal architecture, and mechanical growth conditions were systematically optimized to generate parameters for robust and efficient “stretch-growth” of motor axons. We found that axons projecting from motor neuron aggregates were able to respond to axon displacement rates at least 10 times greater than that tolerated by axons projecting from dissociated motor neurons. The growth and structural characteristics of these stretch-grown motor axons were compared to benchmark stretch-grown axons from sensory dorsal root ganglion neurons, revealing similar axon densities yet increased motor axon fasciculation. Finally, motor axons were integrated with myocytes and then stretch-grown to create novel long-projecting axonal-myocyte constructs that better recreate characteristic dimensions of native nerve-muscle anatomy. This is the first demonstration of mechanical elongation of spinal cord motor axons and may have applications as anatomically inspired in vitro testbeds or as tissue engineered “living scaffolds” for targeted axon tract reconstruction following nervous system injury or disease.Significance StatementWe have developed novel axon tracts of unprecedented lengths spanning either two discrete populations of neurons or a population of neurons and skeletal myocytes. This is the first demonstration of “stretch-grown” motor axons that recapitulate the structure of spinal motor neurons in vivo by projecting long axons from a pool of motor neurons to distant targets, and may have applications as anatomically inspired in vitro test beds to study mechanisms of axon growth, development, and neuromuscular function in anatomically accurate axo-myo constructs; as well as serve as “living scaffolds” in vivo for targeted axon tract reconstruction following nervous system trauma.


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