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)

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.

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.

The effects of SDRNFLRFamide and TNRNFLRFamide on the motor patterns of the stomatogastric ganglion of the crab Cancer borealis

1993 ◽  
Vol 181 (1) ◽  
pp. 1-26 ◽  
Author(s):  
J. M. Weimann ◽  
E. Marder ◽  
B. Evans ◽  
R. L. Calabrese
Keyword(s):  
Nervous System ◽  
High Performance ◽  
Stomatogastric Ganglion ◽  
Moderate Activity ◽  
Activity Levels ◽  
Dependent Manner ◽  
Stomatogastric Nervous System ◽  
Cancer Borealis ◽  
Motor Patterns ◽  
Dose Dependent

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.

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
Keyword(s):  
Nervous System ◽  
Motor Neurons ◽  
Motor Pattern ◽  
Stomatogastric Ganglion ◽  
Red Pigment ◽  
Stomatogastric Nervous System ◽  
Two Phase ◽  
Motor Patterns ◽  
Neuronal Element

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.

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

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.

Hormonal Modulation of Two Coordinated Rhythmic Motor Patterns

2010 ◽  
Vol 104 (2) ◽  
pp. 654-664
Author(s):  
Debra E. Wood ◽  
Melissa Varrecchia ◽  
Michael Papernov ◽  
Denise Cook ◽  
Devon C. Crawford
Keyword(s):  
Motor Pattern ◽  
Projection Neuron ◽  
Frequency Regulation ◽  
Gastric Mill ◽  
Stomatogastric Nervous System ◽  
Motor Patterns ◽  
Rhythmic Motor ◽  
Hormonal Modulation ◽  
Frequency Relationship ◽  
Pyloric Rhythm

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.

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