scholarly journals When complex neuronal structures may not matter

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Adriane G Otopalik ◽  
Alexander C Sutton ◽  
Matthew Banghart ◽  
Eve Marder
Keyword(s):  
Morphological Variability ◽  
Gastric Mill ◽  
Neuron Type ◽  
Recording Site ◽  
Cancer Borealis ◽  
Physiological Properties ◽  
Branching Patterns ◽  
Identified Neuron ◽  
Channel Expression ◽  
Reversal Potentials

Much work has explored animal-to-animal variability and compensation in ion channel expression. Yet, little is known regarding the physiological consequences of morphological variability. We quantify animal-to-animal variability in cable lengths (CV = 0.4) and branching patterns in the Gastric Mill (GM) neuron, an identified neuron type with highly-conserved physiological properties in the crustacean stomatogastric ganglion (STG) of Cancer borealis. We examined passive GM electrotonic structure by measuring the amplitudes and apparent reversal potentials (Erevs) of inhibitory responses evoked with focal glutamate photo-uncaging in the presence of TTX. Apparent Erevs were relatively invariant across sites (mean CV ± SD = 0.04 ± 0.01; 7–20 sites in each of 10 neurons), which ranged between 100–800 µm from the somatic recording site. Thus, GM neurons are remarkably electrotonically compact (estimated λ > 1.5 mm). Electrotonically compact structures, in consort with graded transmission, provide an elegant solution to observed morphological variability in the STG.

The Pharmacological Profile of the Acetylcholine Response of a Crustacean Muscle

1980 ◽  
Vol 88 (1) ◽  
pp. 147-160
Author(s):  
EVE MARDER ◽  
DANIÈLE PAUPARDIN-TRITSCH
Keyword(s):  
Acetylcholinesterase Activity ◽  
Gastric Mill ◽  
Muscarinic Agonists ◽  
Pharmacological Profile ◽  
Cancer Borealis ◽  
Cancer Irroratus ◽  
Pharmacological Analysis ◽  
Crustacean Muscle ◽  
Cancer Pagurus ◽  
High Concentrations

A pharmacological analysis was made of the depolarizing acetylcholine (ACh) response found on the gastric mill 1 muscles of the crabs Cancer pagurus, Cancer irroratus and Cancer borealis. Acetylcholine, carbamylcholine, trimethylammonium, nicotine, and dimethyl-4-phenyl-piperazinium were effective in producing contractures and depolarizations in these muscles. No response to decamethonium, suberyldicholine, acetyl-β-methylcholine, carbamyl-β-methylcholine, pilocarpine and oxotremorine could be detected. High concentrations of muscarinic agonists (10−4 to 10−3 M) potentiated and prolonged the ACh iontophoretic response. When the acetylcholinesterase activity was inhibited with neostigmine, or when the response was elicited with carbamylcholine, muscarinic agonists partially inhibited the response. ACh responses were most effectively blocked by vertebrate nicotinic ganglionic antagonists, including dihydro-β-erythroidine, pempidine, and mecamylamine. α-Bungarotoxin was without effect on the ACh response.

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.

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.

Auditory Interneurones in the Metathoracic Ganglion of the Grasshopper Chorthippus Biguttulus: I. Morphological and Physiological Characterization

1991 ◽  
Vol 158 (1) ◽  
pp. 391-410 ◽  
Author(s):  
ANDREAS STUMPNER ◽  
BERNHARD RONACHER
Keyword(s):  
White Noise ◽  
Dynamic Range ◽  
Lucifer Yellow ◽  
Physiological Characterization ◽  
Acoustic Stimuli ◽  
Physiological Properties ◽  
Metathoracic Ganglion ◽  
Branching Patterns ◽  
Dependent Inhibition ◽  
Chorthippus Biguttulus

1. Auditory intemeurones originating in the metathoracic ganglion of females of the grasshopper Chorthippus biguttulus can be classified as local (SN), bisegmental (BSN), T-shaped (TN) and ascending neurones (AN). A comparison of branching patterns and physiological properties indicates that auditory interneurones of C. biguttulus are homologous with those described for the locust. 2. Eighteen types of auditory neurones are morphologically characterized on the basis of Lucifer Yellow staining. All of them branch bilaterally in the metathoracic ganglion. Smooth dendrites, from which postsynaptic potentials (PSPs) can be recorded, predominate on the side ipsilateral to the soma. If ‘beaded’ branches exist, they predominate contralaterally. The ascending axon runs contralaterally to the soma, except in T-fibres. 3. Auditory receptors respond tonically. The dynamic range of their intensity-response curve covers 20–25 dB. Local, bisegmental and T-shaped neurones are most sensitive to stimulation ipsilateral to the soma. The responses of SN1 and TNI to white-noise stimuli are similar to those of receptors, while phasic-tonic responses are found in SN4, SN5, SN7 and BSN1. The bisegmental neurones receive side-dependent inhibition that corresponds to a 20–30dB attenuation. One local element (SN6) is predominantly inhibited by acoustic stimuli. 4. Ascending neurones are more sensitive to contralateral stimulation (i.e. on their axon side). Only one of them (AN6) responds tonically to white-noise stimuli at all intensities; others exhibit a tonic discharge only at low or at high intensities.One neurone (AN12) responds with a phasic burst over a wide intensity range. The most directional neurones (AN1, AN2) are excited by contralateral stimuli and (predominantly) inhibited by ipsilateral stimuli. Three ascending neurones (AN13-AN15) are spontaneously active and are inhibited by acoustic stimuli. 5. All auditory intemeurones, except SN5, are more sensitive to pure tones below 10 kHz than to ultrasound.

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.

scholarly journals Two central pattern generators from the crab, Cancer borealis, respond robustly and differentially to extreme extracellular pH

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Jessica A Haley ◽  
David Hampton ◽  
Eve Marder
Keyword(s):  
Ion Channels ◽  
Network Performance ◽  
Central Pattern Generators ◽  
Extracellular Ph ◽  
Cancer Borealis ◽  
Environmental Perturbation ◽  
Cardiac Ganglia ◽  
Physiological Properties ◽  
Potential Difficulty ◽  
Pattern Generators

The activity of neuronal circuits depends on the properties of the constituent neurons and their underlying synaptic and intrinsic currents. We describe the effects of extreme changes in extracellular pH – from pH 5.5 to 10.4 – on two central pattern generating networks, the stomatogastric and cardiac ganglia of the crab, Cancer borealis. Given that the physiological properties of ion channels are known to be sensitive to pH within the range tested, it is surprising that these rhythms generally remained robust from pH 6.1 to pH 8.8. The pH sensitivity of these rhythms was highly variable between animals and, unexpectedly, between ganglia. Animal-to-animal variability was likely a consequence of similar network performance arising from variable sets of underlying conductances. Together, these results illustrate the potential difficulty in generalizing the effects of environmental perturbation across circuits, even within the same animal.

scholarly journals Coupling between fast and slow oscillator circuits in Cancer borealis is temperature-compensated

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Daniel Powell ◽  
Sara A Haddad ◽  
Srinivas Gorur-Shandilya ◽  
Eve Marder
Keyword(s):  
Integer Number ◽  
Temperature Sensitive ◽  
Gastric Mill ◽  
Temperature Dependent ◽  
Cancer Borealis ◽  
Cycle Frequency ◽  
Temperature Changes ◽  
Wide Range ◽  
Similar Temperature ◽  
Increasing Temperature

Coupled oscillatory circuits are ubiquitous in nervous systems. Given that most biological processes are temperature-sensitive, it is remarkable that the neuronal circuits of poikilothermic animals can maintain coupling across a wide range of temperatures. Within the stomatogastric ganglion (STG) of the crab, Cancer borealis, the fast pyloric rhythm (~1 Hz) and the slow gastric mill rhythm (~0.1 Hz) are precisely coordinated at ~11°C such that there is an integer number of pyloric cycles per gastric mill cycle (integer coupling). Upon increasing temperature from 7°C to 23°C, both oscillators showed similar temperature-dependent increases in cycle frequency, and integer coupling between the circuits was conserved. Thus, although both rhythms show temperature-dependent changes in rhythm frequency, the processes that couple these circuits maintain their coordination over a wide range of temperatures. Such robustness to temperature changes could be part of a toolbox of processes that enables neural circuits to maintain function despite global perturbations.

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