Activation of a Lobster Motor Rhythm-Generating Network by Disinhibition of Permissive Modulatory Inputs

1998 ◽  
Vol 80 (5) ◽  
pp. 2776-2780 ◽  
Author(s):  
Serge Faumont ◽  
John Simmers ◽  
Pierre Meyrand

Faumont, Serge, John Simmers, and Pierre Meyrand. Activation of a lobster motor rhythm-generating network by disinhibition of permissive modulatory inputs. J. Neurophysiol. 80: 2776–2780, 1998. Rhythm generation by the gastric motor network in the stomatogastric ganglion (STG) of the lobster Homarus gammarus is controlled by modulatory projection neurons from rostral commissural ganglia (CoGs); blocking action potential conduction in these inputs to the STG of a stomatogastric nervous system in vitro rapidly renders the gastric network silent. However, exposure of the CoGs to low Ca2+ saline to block chemical synapses activates a spontaneously silent gastric network or enhances an ongoing gastric rhythm. A similar permissive effect was observed when picrotoxin was also superfused on these ganglia. We conclude that in the CoGs continuous synaptic inhibition is exerted on modulatory projection neuron(s) and that release from this inhibition allows strong activation of the gastric network.

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)


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.


2019 ◽  
Vol 121 (3) ◽  
pp. 950-972 ◽  
Author(s):  
Dawn M. Blitz ◽  
Andrew E. Christie ◽  
Aaron P. Cook ◽  
Patsy S. Dickinson ◽  
Michael P. Nusbaum

Microcircuit modulation by peptides is well established, but the cellular/synaptic mechanisms whereby identified neurons with identified peptide transmitters modulate microcircuits remain unknown for most systems. Here, we describe the distribution of GYRKPPFNGSIFamide (Gly1-SIFamide) immunoreactivity (Gly1-SIFamide-IR) in the stomatogastric nervous system (STNS) of the crab Cancer borealis and the Gly1-SIFamide actions on the two feeding-related circuits in the stomatogastric ganglion (STG). Gly1-SIFamide-IR localized to somata in the paired commissural ganglia (CoGs), two axons in the nerves connecting each CoG with the STG, and the CoG and STG neuropil. We identified one Gly1-SIFamide-IR projection neuron innervating the STG as the previously identified modulatory commissural neuron 5 (MCN5). Brief (~10 s) MCN5 stimulation excites some pyloric circuit neurons. We now find that bath applying Gly1-SIFamide to the isolated STG also enhanced pyloric rhythm activity and activated an imperfectly coordinated gastric mill rhythm that included unusually prolonged bursts in two circuit neurons [inferior cardiac (IC), lateral posterior gastric (LPG)]. Furthermore, longer duration (>30 s) MCN5 stimulation activated a Gly1-SIFamide-like gastric mill rhythm, including prolonged IC and LPG bursting. The prolonged LPG bursting decreased the coincidence of its activity with neurons to which it is electrically coupled. We also identified local circuit feedback onto the MCN5 axon terminals, which may contribute to some distinctions between the responses to MCN5 stimulation and Gly1-SIFamide application. Thus, MCN5 adds to the few identified projection neurons that modulate a well-defined circuit at least partly via an identified neuropeptide transmitter and provides an opportunity to study peptide regulation of electrical coupled neurons in a functional context. NEW & NOTEWORTHY Limited insight exists regarding how identified peptidergic neurons modulate microcircuits. We show that the modulatory projection neuron modulatory commissural neuron 5 (MCN5) is peptidergic, containing Gly1-SIFamide. MCN5 and Gly1-SIFamide elicit similar output from two well-defined motor circuits. Their distinct actions may result partly from circuit feedback onto the MCN5 axon terminals. Their similar actions include eliciting divergent activity patterns in normally coactive, electrically coupled neurons, providing an opportunity to examine peptide modulation of electrically coupled neurons in a functional context.


2007 ◽  
Vol 293 (2) ◽  
pp. R901-R910 ◽  
Author(s):  
Stephen M. Johnson ◽  
Liana M. Wiegel ◽  
David J. Majewski

The role of pacemaker properties in vertebrate respiratory rhythm generation is not well understood. To address this question from a comparative perspective, brain stems from adult turtles were isolated in vitro, and respiratory motor bursts were recorded on hypoglossal (XII) nerve rootlets. The goal was to test whether burst frequency could be altered by conditions known to alter respiratory pacemaker neuron activity in mammals (e.g., increased bath KCl or blockade of specific inward currents). While bathed in artificial cerebrospinal fluid (aCSF), respiratory burst frequency was not correlated with changes in bath KCl (0.5–10.0 mM). Riluzole (50 μM; persistent Na+ channel blocker) increased burst frequency by 31 ± 5% ( P < 0.05) and decreased burst amplitude by 42 ± 4% ( P < 0.05). In contrast, flufenamic acid (FFA, 20–500 μM; Ca2+-activated cation channel blocker) reduced and abolished burst frequency in a dose- and time-dependent manner ( P < 0.05). During synaptic inhibition blockade with bicuculline (50 μM; GABAA channel blocker) and strychnine (50 μM; glycine receptor blocker), rhythmic motor activity persisted, and burst frequency was directly correlated with extracellular KCl (0.5–10.0 mM; P = 0.005). During synaptic inhibition blockade, riluzole (50 μM) did not alter burst frequency, whereas FFA (100 μM) abolished burst frequency ( P < 0.05). These data are most consistent with the hypothesis that turtle respiratory rhythm generation requires Ca2+-activated cation channels but not pacemaker neurons, which thereby favors the group-pacemaker model. During synaptic inhibition blockade, however, the rhythm generator appears to be transformed into a pacemaker-driven network that requires Ca2+-activated cation channels.


1997 ◽  
Vol 200 (24) ◽  
pp. 3221-3233 ◽  
Author(s):  
A J Tierney ◽  
J Blanck ◽  
J Mercier

Whole-mount immunocytochemistry was used to map the location of FMRFamide-like peptides in the crayfish (Procambarus clarkii) stomatogastric nervous system. This system contains the pyloric and gastric mill central pattern generators, which receive modulatory inputs from projection neurons with somata located primarily in other ganglia of the stomatogastric nervous system. Our studies revealed stained somata in the commissural and esophageal ganglia. A pair of stained somata was located in the inferior ventricular nerve, and another pair of somata was located in the stomatogastric nerve where it is joined by the two superior esophageal nerves. The stomatogastric ganglion contained no stained somata, but the neuropil was brightly stained and 2-4 axons projected laterally in small nerves directly from the ganglion. These results indicate that FMRFamide or related peptides may act as neuromodulators in the crayfish stomatogastric nervous system. To test this hypothesis, we studied the effects of FMRFamide and four related peptides (DF2, NF1, F1 and LMS) on the pyloric motor pattern. DF2, NF1 and F1 all excited certain pyloric cells, especially the lateral pyloric (LP) and ventricular dilator (VD) neurons, and enhanced pyloric cycling frequency in most actively rhythmic preparations. FMRFamide had no detectable effects on pyloric cells, and LMS had inhibitory effects, causing disruption of the pyloric rhythm in actively cycling preparations and reducing tonic activity in non-rhythmic preparations.


2000 ◽  
Vol 203 (14) ◽  
pp. 2075-2092 ◽  
Author(s):  
A.M. Swensen ◽  
J. Golowasch ◽  
A.E. Christie ◽  
M.J. Coleman ◽  
M.P. Nusbaum ◽  
...  

The multifunctional neural circuits in the crustacean stomatogastric ganglion (STG) are influenced by many small-molecule transmitters and neuropeptides that are co-localized in identified projection neurons to the STG. We describe the pattern of gamma-aminobutyric acid (GABA) immunoreactivity in the stomatogastric nervous system of the crab Cancer borealis and demonstrate biochemically the presence of authentic GABA in C. borealis. No STG somata show GABA immunoreactivity but, within the stomatogastric nervous system, GABA immunoreactivity co-localizes with several neuropeptides in two identified projection neurons, the modulatory proctolin neuron (MPN) and modulatory commissural neuron 1 (MCN1). To determine which actions of these neurons are evoked by GABA, it is necessary to determine the physiological actions of GABA on STG neurons. We therefore characterized the response of each type of STG neuron to focally applied GABA. All STG neurons responded to GABA. In some neurons, GABA evoked a picrotoxin-sensitive depolarizing, excitatory response with a reversal potential of approximately −40 mV. This response was also activated by muscimol. In many STG neurons, GABA evoked inhibitory responses with both K(+)- and Cl(−)-dependent components. Muscimol and beta-guanidinopropionic acid weakly activated the inhibitory responses, but many other drugs, including bicuculline and phaclofen, that act on vertebrate GABA receptors were not effective. In summary, GABA is found in projection neurons to the crab STG and can evoke both excitatory and inhibitory actions on STG neurons.


1981 ◽  
Vol 90 (1) ◽  
pp. 231-251
Author(s):  
F. NAGY ◽  
M. MOULINS

1. In the lobster Jasus lalandii the activity of the oesophageal nervous system (monitored through the firing of its main motor neuron, OD1) is modulated by a pair of proprioceptors, the posterior stomach receptors (PSRs). 2. The in vitro preparation used consisted of the oesophageal nervous system, the suboesophageal ganglion and the two PSRs, which provide the only source of sensory input. 3. Stimulation of a PSR activates only the oesophageal oscillator located in the ipsilateral commissural ganglion. 4. When spike conduction is blocked in the ipsilateral connective, the stimulation of a PSR activates the contralateral oesophageal oscillator. Inputs from each PSR project to the different parts of the distributed oesophageal network (in the two commissural ganglia and the oesophageal ganglion), but at a given time only one of the PSRs' projections is effective. 5. The relative efficacy of the PSRs' projections is controlled by the oesophageal motor network itself and requires that the superior oesophageal nerves be intact (sons). 6. The PSRs' inputs are integrated in the suboesophageal ganglion before reaching the oesophageal network. However, this premotor step is not involved in the control of the unilaterality of PSRs' effects. 7. The PSRs are stimulated by at least two different rhythmical muscular sequences of the foregut (the gastric mill sequence and the cardiac sac sequence) and provide a source of rhythmical inputs to the CNS. 8. The oesophageal nervous system exhibits a periodically varying sensitivity to the PSRs' inputs, which is illustrated by a phase-response curve. 9. Each oesophageal oscillator can be entrained by the rhythmical PSRs' inputs over a range of period. This range includes the period of the spontaneous gastric rhythm. 10. It is proposed that the PSRs enable the oesophageal and the gastric mill rhythms to be coordinated through a peripheral loop. The participation of PSRs in the coordination of different motor sequences of the foregut is discussed.


2003 ◽  
Vol 469 (2) ◽  
pp. 153-169 ◽  
Author(s):  
Andrew E. Christie ◽  
Wolfgang Stein ◽  
John E. Quinlan ◽  
Mark P. Beenhakker ◽  
Eve Marder ◽  
...  

2004 ◽  
Vol 91 (1) ◽  
pp. 78-91 ◽  
Author(s):  
Mark P. Beenhakker ◽  
Dawn M. Blitz ◽  
Michael P. Nusbaum

Sensory neurons enable neural circuits to generate behaviors appropriate for the current environmental situation. Here, we characterize the actions of a population (about 60) of bilaterally symmetric bipolar neurons identified within the inner wall of the cardiac gutter, a foregut structure in the crab Cancer borealis. These neurons, called the ventral cardiac neurons (VCNs), project their axons through the crab stomatogastric nervous system to influence neural circuits associated with feeding. Brief pressure application to the cardiac gutter transiently modulated the filtering motor pattern (pyloric rhythm) generated by the pyloric circuit within the stomatogastric ganglion (STG). This modulation included an increased speed of the pyloric rhythm and a concomitant decrease in the activity of the lateral pyloric neuron. Furthermore, 2 min of rhythmic pressure application to the cardiac gutter elicited a chewing motor pattern (gastric mill rhythm) generated by the gastric mill circuit in the STG that persisted for ≤30 min. These sensory actions on the pyloric and gastric mill circuits were mimicked by either ventral cardiac nerve or dorsal posterior esophageal nerve stimulation. VCN actions on the STG circuits required the activation of projection neurons in the commissural ganglia. A subset of the VCN actions on these projection neurons appeared to be direct and cholinergic. We propose that the VCN neurons are mechanoreceptors that are activated when food stored in the foregut applies an outward force, leading to the long-lasting activation of projection neurons required to initiate chewing and modify the filtering of chewed food.


1998 ◽  
Vol 201 (10) ◽  
pp. 1615-1626 ◽  
Author(s):  
D R Nässel ◽  
M Eckert ◽  
J E Muren ◽  
H Penzlin

Nine tachykinin-related peptides (TRPs) have been isolated from the brain and intestine of the cockroach Leucophaea maderae. In the present investigation, two of the nine TRPs, LemTRP 1 and 5, were tested for their ability to stimulate contractions in the foregut of the cockroaches L. maderae and Periplaneta americana in vitro. The two LemTRPs and the related locust peptide locustatachykinin I (LomTK I) induced contractions in the foregut of P. americana in a dose-dependent manner, but had no myostimulatory action in L. maderae. A half-maximal response for the LemTRPs and LomTK I was obtained at 5x10(-9)mol l-1. In both species, the neuropeptide proctolin stimulated foregut contractions. Using an antiserum to LomTK I, we demonstrated that in both species there are LomTK-like-immunoreactive (LomTK-LI) cell bodies and fibers within the ganglia and nerves of the stomatogastric nervous system. However, correlated with the species-specific action of the TRPs, we found efferent LomTK-LI nerve fibers supplying muscle fibers in the foregut of P. americana, but not in L. maderae. In both cockroach species, there is a rich supply of proctolin-immunoreactive fibers to the foregut muscle. Some of the LomTK-LI fibers supplying the P. americana foregut muscle contain co-localized proctolin immunoreactivity. These fibers appear to be derived from a large cell body in the frontal ganglion which also displayed co-localized immunoreactivities. Since TRP-containing neurons are restricted to the nerves and ganglia of the stomatogastric nervous system both in P. americana and L. maderae, TRPs may be involved in the control of foregut movements in both species, but in P. americana the control may be more complex with the additional peripherally projecting LomTK-LI neurons.


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