Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system

1991 ◽  
Vol 65 (1) ◽  
pp. 111-122 ◽  
Author(s):  
J. M. Weimann ◽  
P. Meyrand ◽  
E. Marder
Keyword(s):  
Motor Neurons ◽  
Activity Patterns ◽  
Gastric Mill ◽  
Cancer Borealis ◽  
Motor Patterns ◽  
Pyloric Network ◽  
Lateral Posterior ◽  
Pattern Generators ◽  
Rhythmic Behaviors ◽  
Pyloric Rhythm

1. The stomatogastric ganglion (STG) of decapod crustaceans has been characterized by its production of two motor patterns, the gastric mill rhythm and the pyloric rhythm. The period of the gastric rhythm is typically 5-10 s, whereas the period of the pyloric rhythm is approximately 1 s. 2. In the STG of the crab, Cancer borealis, we find routinely that many motor neurons are active in time with both the pyloric and gastric rhythms. We rigorously identified the motor neurons according to the muscles they innervate. Some neurons usually classified as members of the pyloric network can be active in time with the gastric rhythm. All of the gastric motor neurons except the dorsal gastric (DG) neuron can generate pyloric-timed firing patterns. 3. Two motor neurons innervate muscles found in several different regions of the stomach. The inferior cardiac (IC) neuron, usually considered part of the pyloric network, innervates cardiac sac, gastric mill, and pyloric muscles. The lateral posterior gastric (LPG) neurons innervate muscles of both the gastric mill and the pyloric chamber. 4. These data show that the gastric and pyloric networks in the crab are not separate groups of neurons that independently generate two different rhythmic behaviors. Rather, these neurons together provide a synaptically connected pool of neurons from which many different pattern-generating circuits can be assembled, under different physiological conditions.

Endogenous Motor Neuron Properties Contribute to a Program-Specific Phase of Activity in the Multifunctional Feeding Central Pattern Generator of Aplysia

2007 ◽  
Vol 98 (1) ◽  
pp. 29-42 ◽  
Author(s):  
Geidy E. Serrano ◽  
Clarissa Martínez-Rubio ◽  
Mark W. Miller
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Central Pattern Generators ◽  
Ingestive Behavior ◽  
Membrane Properties ◽  
Motor Patterns ◽  
Effector System ◽  
Bilateral Pair ◽  
Pattern Generators ◽  
Specific Phase

Multifunctional central pattern generators (CPGs) are circuits of neurons that can generate manifold actions from a single effector system. This study examined a bilateral pair of pharyngeal motor neurons, designated B67, that participate in the multifunctional feeding network of Aplysia californica. Fictive buccal motor programs (BMPs) were elicited with four distinct stimulus paradigms to assess the activity of B67 during ingestive versus egestive patterns. In both classes of programs, B67 fired during the phase of radula protraction and received a potent inhibitory postsynaptic potential (IPSP) during fictive radula retraction. When programs were ingestive, the retraction phase IPSP exhibited a depolarizing sag and was followed by a postinhibitory rebound (PIR) that could generate a postretraction phase of impulse activity. When programs were egestive, the depolarizing sag potential and PIR were both diminished or were not present. Examination of the membrane properties of B67 disclosed a cesium-sensitive depolarizing sag, a corresponding Ih-like current, and PIR in its responses to hyperpolarizing pulses. Direct IPSPs originating from the influential CPG retraction phase interneuron B64 were also found to activate the sag potential and PIR of B67. Dopamine, a modulator that can promote ingestive behavior in this system, enhanced the sag potential, Ih-like current, and PIR of B67. Finally, a pharyngeal muscle contraction followed the radula retraction phase of ingestive, but not egestive motor patterns. It is proposed that regulation of the intrinsic properties of this motor neuron can contribute to generating a program-specific phase of motor activity.

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.

scholarly journals Episodic Bouts of Activity Accompany Recovery of Rhythmic Output By a Neuromodulator- and Activity-Deprived Adult Neural Network

2003 ◽  
Vol 90 (4) ◽  
pp. 2720-2730 ◽  
Author(s):  
Jason A. Luther ◽  
Alice A. Robie ◽  
John Yarotsky ◽  
Christopher Reina ◽  
Eve Marder ◽  
...  
Keyword(s):  
Neural Network ◽  
Neuronal Network ◽  
Recovery Process ◽  
Stomatogastric Ganglion ◽  
Cancer Borealis ◽  
Pyloric Network ◽  
Underlying Mechanisms ◽  
Over Time ◽  
Phase Relationships ◽  
Pyloric Rhythm

The pyloric rhythm of the stomatogastric ganglion of the crab, Cancer borealis, slows or stops when descending modulatory inputs are acutely removed. However, the rhythm spontaneously resumes after one or more days in the absence of neuromodulatory input. We recorded continuously for days to characterize quantitatively this recovery process. Activity bouts lasting 40–900 s began several hours after removal of neuromodulatory input and were followed by stable rhythm recovery after 1–4 days. Bout duration was not related to the intervals (0.3–800 min) between bouts. During an individual bout, the frequency rapidly increased and then decreased more slowly. Photoablation of back-filled neuromodulatory terminals in the stomatogastric ganglion (STG) neuropil had no effect on activity bouts or recovery, suggesting that these processes are intrinsic to the STG neuronal network. After removal of neuromodulatory input, the phase relationships of the components of the triphasic pyloric rhythm were altered, and then over time the phase relationships moved toward their control values. Although at low pyloric rhythm frequency the phase relationships among pyloric network neurons depended on frequency, the changes in frequency during recovery did not completely account for the change in phase seen after rhythm recovery. We suggest that activity bouts represent underlying mechanisms controlling the restructuring of the pyloric network to allow resumption of an appropriate output after removal of neuromodulatory input.

Long-Term Expression of Two Interacting Motor Pattern-Generating Networks in the Stomatogastric System of Freely Behaving Lobster

1998 ◽  
Vol 79 (3) ◽  
pp. 1396-1408 ◽  
Author(s):  
Stefan Clemens ◽  
Denis Combes ◽  
Pierre Meyrand ◽  
John Simmers
Keyword(s):  
Motor Neurons ◽  
Motor Pattern ◽  
Burst Duration ◽  
Cycle Period ◽  
Gastric Mill ◽  
Pyloric Network ◽  
Freely Behaving ◽  
Stomatogastric System

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.

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.

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.

Interneuronal and motor patterns during crawling behavior of semi-intact leeches.

1997 ◽  
Vol 200 (9) ◽  
pp. 1369-1381 ◽  
Author(s):  
A P Baader
Keyword(s):  
Motor Neurons ◽  
Behavior Pattern ◽  
Activity Patterns ◽  
Medicinal Leech ◽  
Intracellular Recordings ◽  
Motor Patterns ◽  
Potential Oscillations ◽  
Different Types ◽  
Inhibitory Motor Neurons ◽  
Membrane Potential Oscillations

Semi-intact tethered preparations were used to characterize neuronal activity patterns in midbody ganglia of the medicinal leech during crawling. Extra- and intracellular recordings were obtained from identified interneurons and from motor neurons of the longitudinal and circular muscles during crawling episodes. Coordinated activities of nine excitatory and inhibitory motor neurons of the longitudinal and circular muscles were recorded during the appropriate phases of crawling. Thus, during crawling, the leech uses motor output components known to contribute to other types of behavior, such as swimming or the shortening/local bending reflex. Interneurons with identified functions in these other types of behavior exhibit membrane potential oscillations that are in phase with the behavior pattern. Therefore, the recruitment of neuronal network elements during several types of behavior occurs not only at the motor neuron level but also involves interneurons. This applies even to some interneurons that were previously thought to have dedicated functions (such as cells 204 and 208 and the S cell). The function of neuronal circuitries in producing different types of behavior with a limited number of neurons is discussed.

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.

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.

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