Dual modulatory effects on feedback from a proprioceptor in the crustacean stomatogastric nervous system

2021 ◽  
Author(s):  
Davis Grininger ◽  
John T. Birmingham
Keyword(s):  
Nervous System ◽  
Inhibitory Action ◽  
Muscle Contractions ◽  
Proprioceptive Feedback ◽  
Gastric Mill ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Muscle Stretch ◽  
Excitatory Action ◽  
Central Network

Neuromodulatory actions that change the properties of proprioceptors or the muscle movements to which they respond necessarily affect the feedback provided to the central network. Here we further characterize the responses of the gastropyloric receptor 1 (GPR1) and gastropyloric receptor 2 (GPR2) neurons in the stomatogastric nervous system of the crab Cancer borealis to movements and contractions of muscles, and we report how neuromodulation modifies those responses. We observed that the GPR1 response to contractions of the gastric mill 4 (gm4) muscle was absent, or nearly so, when the neuron was quiescent but robust when it was spontaneously active. We also found that the effects of four neuromodulatory substances (GABA, serotonin, proctolin and TNRNFLRFamide) on the GPR1 response to muscle stretch were similar to those previously reported for GPR2. Finally, we showed that an excitatory action on gm4 due to proctolin combined with an inhibitory action on GPR2 due to GABA can allow for larger muscle contractions without increased proprioceptive feedback.

scholarly journals Long-Lasting Activation of Rhythmic Neuronal Activity by a Novel Mechanosensory System in the Crustacean Stomatogastric Nervous System

2004 ◽  
Vol 91 (1) ◽  
pp. 78-91 ◽  
Author(s):  
Mark P. Beenhakker ◽  
Dawn M. Blitz ◽  
Michael P. Nusbaum
Keyword(s):  
Nervous System ◽  
Neural Circuits ◽  
Motor Pattern ◽  
Projection Neurons ◽  
Gastric Mill ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Pressure Application ◽  
Mechanosensory System ◽  
Pyloric Rhythm

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.

Spectral Analyses Reveal the Presence of Adult-Like Activity in the Embryonic Stomatogastric Motor Patterns of the Lobster, Homarus americanus

2008 ◽  
Vol 99 (6) ◽  
pp. 3104-3122 ◽  
Author(s):  
Kristina J. Rehm ◽  
Adam L. Taylor ◽  
Stefan R. Pulver ◽  
Eve Marder
Keyword(s):  
Nervous System ◽  
Rhythmic Activity ◽  
Homarus Americanus ◽  
Gastric Mill ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Motor Patterns ◽  
Similar Frequency ◽  
Rhythmic Behavior ◽  
Slow Activity

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.

Recruitment of a projection neuron determines gastric mill motor pattern selection in the stomatogastric nervous system of the crab, Cancer borealis

1994 ◽  
Vol 72 (4) ◽  
pp. 1451-1463 ◽  
Author(s):  
B. J. Norris ◽  
M. J. Coleman ◽  
M. P. Nusbaum
Keyword(s):  
Nervous System ◽  
Synaptic Input ◽  
Motor Pattern ◽  
Rhythmic Activity ◽  
Projection Neuron ◽  
Projection Neurons ◽  
Muscarinic Agonist ◽  
Gastric Mill ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis

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)

Distribution and effects of tachykinin-like peptides in the stomatogastric nervous system of the crab,Cancer borealis

1995 ◽  
Vol 354 (2) ◽  
pp. 282-294 ◽  
Author(s):  
Dawn M. Blitz ◽  
Andrew E. Christie ◽  
Eve Marder ◽  
Michael P. Nusbaum
Keyword(s):  
Nervous System ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis

Nervous Control of Gut Movements in Lophius

1980 ◽  
Vol 60 (1) ◽  
pp. 19-30 ◽  
Author(s):  
J. Z. Young
Keyword(s):  
Nervous System ◽  
Autonomic Nervous System ◽  
Inhibitory Action ◽  
Sympathetic Nerves ◽  
The Other ◽  
Sufficient Data ◽  
Nervous Control ◽  
Autonomic Nervous ◽  
Hand Control ◽  
Excitatory Action

There are not sufficient data available to allow any general statements about the earlier stages of evolution of the autonomic nervous system and of its various transmitter mechanisms. In the previous paper (Young, 1980) it was shown that control of the stomach of elasmobranchs is largely by the inhibitory action of the sympathetic nerves, probably mediated by 5-HT. In teleostean fishes on the other hand control seems to be mainly by the cholinergic excitatory action of the vagus, especially in the more advanced (acanthopterygian) groups (Grove & Campbell, 1979a, b; Fänge & Grove, 1979).

scholarly journals Similarities and differences in circuit responses to applied Gly1-SIFamide and peptidergic (Gly1-SIFamide) neuron stimulation

2019 ◽  
Vol 121 (3) ◽  
pp. 950-972 ◽  
Author(s):  
Dawn M. Blitz ◽  
Andrew E. Christie ◽  
Aaron P. Cook ◽  
Patsy S. Dickinson ◽  
Michael P. Nusbaum
Keyword(s):  
Activity Patterns ◽  
Projection Neuron ◽  
Projection Neurons ◽  
Gastric Mill ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Axon Terminals ◽  
Motor Circuits ◽  
Commissural Neuron ◽  
Functional Context

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.

Feeding State-Dependent Modulation of Feeding-Related Motor Patterns

2021 ◽  
Author(s):  
Aaron P. Cook ◽  
Michael P. Nusbaum
Keyword(s):  
Neural Circuit ◽  
Projection Neuron ◽  
Neuron Activity ◽  
Gastric Mill ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Motor Patterns ◽  
State Dependent ◽  
Reduced Activity ◽  
Time Point

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.

GABA and responses to GABA in the stomatogastric ganglion of the crab Cancer borealis

2000 ◽  
Vol 203 (14) ◽  
pp. 2075-2092 ◽  
Author(s):  
A.M. Swensen ◽  
J. Golowasch ◽  
A.E. Christie ◽  
M.J. Coleman ◽  
M.P. Nusbaum ◽  
...  
Keyword(s):  
Nervous System ◽  
Gaba Receptors ◽  
Reversal Potential ◽  
Stomatogastric Ganglion ◽  
Projection Neurons ◽  
Gamma Aminobutyric Acid ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Excitatory Response ◽  
Commissural Neuron

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.

Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. II. Rapid nicotinic and prolonged modulatory effects on neurons in the stomatogastric ganglion

1989 ◽  
Vol 62 (2) ◽  
pp. 571-581 ◽  
Author(s):  
P. S. Katz ◽  
R. M. Harris-Warrick
Keyword(s):  
Motor Neurons ◽  
Preceding Paper ◽  
Stomatogastric Ganglion ◽  
Cell Group ◽  
Muscarinic Antagonists ◽  
Gastric Mill ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Mechanical Coupling ◽  
Plateau Potential

1. The gastropyloric receptor (GPR) cells, which are described in the preceding paper, are a set of proprioceptive cells in the crabs Cancer borealis and Cancer irroratus that contain serotonin (5-hydroxytryptamine, 5-HT) and choline acetyltransferase. These cells have a variety of synaptic effects on cells in the stomatogastric ganglion (STG). We used pharmacologic methods to distinguish the effects that were due to acetylcholine (ACh) from those that could be due to serotonin. 2. The GPR cells evoke excitatory postsynaptic potentials (EPSPs) in two gastric mill motor neurons [lateral and dorsal gastric (LG and DG)] in the stomatogastric ganglion. The EPSPs exhibit nicotinic pharmacology, indicating that they may be due to the release of ACh from the GPR cells. 3. A train of GPR action potentials induces plateau potential properties in the DG motor neuron. This plateau potential induction is not blocked by nicotinic or muscarinic antagonists, suggesting it might be due to serotonin released from the GPR cells. Bath-applied serotonin induces a tonic depolarization of DG with high-intensity spiking. 4. In the accompanying paper, it is shown that DG-evoked muscle contraction leads to the excitation of GPR2 through mechanical coupling of the muscles. Because GPR2 also excites DG, a positive feedback loop exists between GPR2 and DG. This reflex loop may be involved in the control of the medial tooth of the gastric mill. 5. GPR stimulation initiates or enhances rhythmic pyloric cycling. This is due at least in part to a direct enhancement of bursting in the pyloric dilator/anterior burster (PD/AB) pacemaker cell group and can outlast the period of GPR stimulation by up to 1 min. GPR-induced PD burst enhancement continues in the presence of nicotinic and muscarinic antagonists, indicating that the effect is probably not due to the release of ACh. Bath application of serotonin mimicks the neuromodulatory effect of GPR stimulation on the PD/AB group by inducing or enhancing bursting. 6. Thus the GPR cells elicit at least three different synaptic actions in the stomatogastric ganglion: 1) classical, fast nicotinic cholinergic EPSPs that may be important for reflex functions in the gastric mill; 2) noncholinergic, cycle-by-cycle plateau potential induction that might be critical for the timing and operation of the gastric mill, and 3) prolonged, noncholinergic burst enhancement in pyloric neurons that is mimicked by serotonin, lasts many cycles, and may act to assure that the pyloric central pattern generator (CPG) is activated and cycling strongly.

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