Maturation of Lobster Stomatogastric Ganglion Rhythmic Activity

1999 ◽  
Vol 82 (4) ◽  
pp. 2006-2009 ◽  
Author(s):  
Kathryn S. Richards ◽  
William L. Miller ◽  
Eve Marder

The stomatogastric ganglion of the adult lobster, Homarus americanus generates extremely regular pyloric rhythms with a characteristic period of 0.5–1.5 Hz. To study the changes in the pyloric rhythm during embryonic and larval development, we recorded excitatory junctional potentials evoked by lateral pyloric (LP) neuron activity. Early in development the motor discharge of the LP neuron was often irregular, preventing use of conventional analysis methods that rely on extracting burst times to calculate cycle frequency and its variability. Instead, cycle frequency was determined for the LP neuron from the peak of the power spectrum obtained from the occurrence times of excitatory junctional potentials in the p1 muscle. The ratio of the power in the peak to the power from 0 to 3 Hz was used as a relative measure of the regularity of the rhythm. Throughout embryonic and the first larval stage, LP neuron activity is slow, irregular, and only weakly periodic. The regularity of the rhythm increased during midlarval stages, and both the frequency and regularity increased considerably by the postlarval stage LIV.

2016 ◽  
Vol 115 (5) ◽  
pp. 2434-2445 ◽  
Author(s):  
Lin Zhu ◽  
Allen I. Selverston ◽  
Joseph Ayers

The hyperpolarization-activated inward cationic current ( Ih) is known to regulate the rhythmicity, excitability, and synaptic transmission in heart cells and many types of neurons across a variety of species, including some pyloric and gastric mill neurons in the stomatogastric ganglion (STG) in Cancer borealis and Panulirus interruptus. However, little is known about the role of Ih in regulating the gastric mill dynamics and its contribution to the dynamical bifurcation of the gastric mill and pyloric networks. We investigated the role of Ih in the rhythmic activity and cellular excitability of both the gastric mill neurons (medial gastric, gastric mill) and pyloric neurons (pyloric dilator, lateral pyloric) in Homarus americanus. Through testing the burst period between 5 and 50 mM CsCl, and elimination of postinhibitory rebound and voltage sag, we found that 30 mM CsCl can sufficiently block Ih in both the pyloric and gastric mill neurons. Our results show that Ih maintains the excitability of both the pyloric and gastric mill neurons. However, Ih regulates slow oscillations of the pyloric and gastric mill neurons differently. Specifically, blocking Ih diminishes the difference between the pyloric and gastric mill burst periods by increasing the pyloric burst period and decreasing the gastric mill burst period. Moreover, the phase-plane analysis shows that blocking Ih causes the trajectory of slow oscillations of the gastric mill neurons to change toward the pyloric sinusoidal-like trajectories. In addition to regulating the pyloric rhythm, we found that Ih is also essential for the gastric mill rhythms and differentially regulates these two dynamics.


1998 ◽  
Vol 201 (17) ◽  
pp. 2465-2479 ◽  
Author(s):  
S Harzsch ◽  
J Miller ◽  
J Benton ◽  
RR Dawirs ◽  
B Beltz

The mode of embryonic and larval development and the ethology of metamorphosis in the spider crab and the American lobster are very different, and we took advantage of this to compare neuronal development in the two species. The goals of this study were to discover whether the differences in the maturation of the neuromuscular system in the pereopods and the metamorphic changes of motor behavior between the two species are reflected at the level of the developing nervous system ('neurometamorphosis'). Furthermore, we wanted to broaden our understanding of the mechanisms that govern neuronal development in arthropods. Proliferation of neuronal stem cells in thoracic neuromeres 4-8 of the lobster Homarus americanus and the crab Hyas araneus was monitored over the course of embryonic and larval development using the in vivo incorporation of bromodeoxyuridine (BrdU). Neuropil structure was visualized using an antibody against Drosophila synapsin. While proliferation of neuronal precursors has ceased when embryogenesis is 80 % complete (E80%) in the lobster thoracic neuromeres, proliferation of neuroblasts in the crab persists throughout embryonic development and into larval life. The divergent temporal patterns of neurogenesis in the two crustacean species can be correlated with differences in larval life style and in the degree of maturation of the thoracic legs during metamorphic development. Several unusual aspects of neurogenesis reported here distinguish these crustaceans from other arthropods. Lobsters apparently lack a postembryonic period of proliferation in the thoracic neuromeres despite the metamorphic remodeling that takes place in the larval stages. In contrast, an increase in mitotic activity towards the end of embryonic development is found in crabs, and neuroblast proliferation persists throughout the process of hatching into the larval stages. In both E20% lobster embryos and mid-embryonic crabs, expression of engrailed was found in a corresponding set of neurons and putative glial cells at the posterior neuromere border, suggesting that these cells have acquired similar specific identities and might, therefore, be homologous. None of the BrdU-labeled neuroblasts (typically 6-8 per hemineuromere over a long period of embryogenesis) was positive for engrailed at this and subsequent stages. Our findings are discussed in relation to the spatial and temporal patterns of neurogenesis in insects.


2014 ◽  
Vol 112 (11) ◽  
pp. 2946-2958 ◽  
Author(s):  
Sonal Shruti ◽  
David J. Schulz ◽  
Kawasi M. Lett ◽  
Eve Marder

Gap junctions are intercellular channels that allow for the movement of small molecules and ions between the cytoplasm of adjacent cells and form electrical synapses between neurons. In invertebrates, the gap junction proteins are coded for by the innexin family of genes. The stomatogastric ganglion (STG) in the crab Cancer borealis contains a small number of identified and electrically coupled neurons. We identified Innexin 1 ( Inx1), Innexin 2 (Inx2), Innexin 3 (Inx3), Innexin 4 ( Inx4), Innexin 5 (Inx5), and Innexin 6 ( Inx6) members of the C. borealis innexin family. We also identified six members of the innexin family from the lobster Homarus americanus transcriptome. These innexins show significant sequence similarity to other arthropod innexins. Using in situ hybridization and reverse transcriptase-quantitative PCR (RT-qPCR), we determined that all the cells in the crab STG express multiple innexin genes. Electrophysiological recordings of coupling coefficients between identified pairs of pyloric dilator (PD) cells and PD-lateral posterior gastric (LPG) neurons show that the PD-PD electrical synapse is nonrectifying while the PD-LPG synapse is apparently strongly rectifying.


1984 ◽  
Vol 51 (6) ◽  
pp. 1375-1393 ◽  
Author(s):  
J. S. Eisen ◽  
E. Marder

During motor activity of the pyloric system of the lobster stomatogastric ganglion, there are rhythmic alternations between activity in the pyloric dilator (PD) and pyloric (PY) motor neurons. We studied the phase relations between PD motor neuron activity and PY motor neuron activity in preparations cycling at a wide range of frequencies and after altering the activity of the PD neurons. The PY neurons fall into two classes, early (PE) and late (PL) (21), distinguished by the different phases in the pyloric cycle at which they fire. The phase at which PE neurons fired and the phase at which PL neurons fired was independent of pyloric cycle frequency over a range of frequencies from 0.5 to 2.25 Hz. The anterior burster (AB) interneuron is electrically coupled to the PD motor neurons. Together the AB and PD neurons form the pacemaker for the pyloric system. Synchronous depolarization of the AB and PD neurons evokes a complex inhibitory post-synaptic potential (IPSP) in PY neurons. This IPSP has two components: an early, AB neuron-derived component and a late, PD neuron-derived component. Deletion of the PD neurons from the pyloric circuit by photoinactivation removed the PD-evoked component of the pacemaker-evoked IPSP. This resulted in a decrease in the duration of the IPSP evoked by pacemaker depolarization and a significant advance in the firing phase of PY neurons. Bath application of dopamine was used to hyperpolarize and inhibit the PD neurons (30), causing them to release less neurotransmitter. As a consequence, the duration of the IPSP evoked by pacemaker depolarization was decreased and the firing phase of the PY neurons was significantly advanced. Stimulation of the inferior ventricular nerve (IVN) produces a slow excitation of the PD neurons (30), causing them to release more neurotransmitter. Consequently, the duration of the IPSP evoked by pacemaker depolarization was increased and the firing phase of the PY neurons was significantly retarded for several cycles of pyloric activity following IVN stimulation. Thus, modulation of the strength of PD-evoked inhibition in PY neurons is responsible for altering the firing phase of the PY neurons with respect to the pyloric pacemaker. We suggest that frequency of the pyloric output and the phase relations of the elements within the pyloric cycle can be regulated independently. The potential implications of these data for modulation of synaptic efficacy in other preparations are discussed.


Development ◽  
1959 ◽  
Vol 7 (1) ◽  
pp. 22-38
Author(s):  
Arthur Hughes

Among the Amphibia there are numerous examples of the suppression to a varying extent of a larval stage in the life-history. In such instances the animal is freed by various means from the necessity of passing its early phases of development in open water. This evolutionary trend has nowhere proceeded further than in the Anuran genus Eleutherodactylus, which is distributed through the Caribbean and the adjacent mainlands. In Eleutherodactylus, development is direct and wholly embryonic, and many larval features have been suppressed. In 1871 was published the first description of a West Indian frog which laid eggs in air, and from which young frogs with fully formed limbs were hatched (Bello y Espinosa, 1871). Since that time some twenty papers have been published on the embryology of different species of the genus, mainly in recent years by Dr. W. Gardner Lynn and his collaborators.


2008 ◽  
Vol 99 (6) ◽  
pp. 3104-3122 ◽  
Author(s):  
Kristina J. Rehm ◽  
Adam L. Taylor ◽  
Stefan R. Pulver ◽  
Eve Marder

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.


2013 ◽  
Vol 109 (10) ◽  
pp. 2451-2465 ◽  
Author(s):  
Alex H. Williams ◽  
Molly A. Kwiatkowski ◽  
Adam L. Mortimer ◽  
Eve Marder ◽  
Mary Lou Zeeman ◽  
...  

The cardiac ganglion (CG) of Homarus americanus is a central pattern generator that consists of two oscillatory groups of neurons: “small cells” (SCs) and “large cells” (LCs). We have shown that SCs and LCs begin their bursts nearly simultaneously but end their bursts at variable phases. This variability contrasts with many other central pattern generator systems in which phase is well maintained. To determine both the consequences of this variability and how CG phasing is controlled, we modeled the CG as a pair of Morris-Lecar oscillators coupled by electrical and excitatory synapses and constructed a database of 15,000 simulated networks using random parameter sets. These simulations, like our experimental results, displayed variable phase relationships, with the bursts beginning together but ending at variable phases. The model suggests that the variable phasing of the pattern has important implications for the functional role of the excitatory synapses. In networks in which the two oscillators had similar duty cycles, the excitatory coupling functioned to increase cycle frequency. In networks with disparate duty cycles, it functioned to decrease network frequency. Overall, we suggest that the phasing of the CG may vary without compromising appropriate motor output and that this variability may critically determine how the network behaves in response to manipulations.


1995 ◽  
Vol 198 (4) ◽  
pp. 917-930 ◽  
Author(s):  
R A Satterlie ◽  
T P Norekian

Swim acceleration in Clione limacina can occur via central inputs to pattern generator interneurons and motor neurons and through peripheral inputs to the swim musculature. In the previous paper, peripheral modulation of the swim muscles was shown to increase wing contractility. In the present paper, central inputs are described that trigger an increase in swim frequency and an increase in motor neuron activity. In dissected preparations, spontaneous acceleration from slow to fast swimming included an increase in the cycle frequency, a baseline depolarization in the swim interneurons and an increase in the intensity of motoneuron firing. Similar effects could be elicited by bath application of 10(-5) mol l-1 serotonin. Two clusters of cerebral serotonin-immunoreactive interneurons were found to produce acceleration of swimming accompanied by changes in neuronal activity. Posterior cluster neurons triggered an increase in swim frequency, depolarization of the swim interneurons, an increase in general excitor motoneuron activity and activation of type 12 interneurons and pedal peripheral modulatory neurons. Cells from the anterior cerebral cluster also increased swim frequency, increased activity in the swim motoneurons and activated type 12 interneurons, pedal peripheral modulatory neurons and the heart excitor neuron. The time course of action of the anterior cluster neurons did not greatly outlast the duration of spike activity, while that of the posterior cluster neurons typically outlasted burst duration. It appears that the two discrete clusters of serotonin-immunoreactive neurons have similar, but not identical, effects on swim neurons, raising the possibility that the two serotonergic cell groups modulate the same target cells through different cellular mechanisms.


2020 ◽  
Author(s):  
Lane Yoder

AbstractThe stomatogastric ganglion (STG) is a group of about 30 neurons that resides on the stomach in decapod crustaceans. Its two central pattern generators (CPGs) control the chewing action of the gastric mill and the peristaltic movement of food through the pylorus to the gut. The STG has been studied extensively because it has properties that are common to all nervous systems and because of the small number of neurons and other features that make it convenient to study. So many details are known that the STG is considered a classic test case in neuroscience for the reductionist strategy of explaining the emergence of macro-level phenomena from micro-level data. In spite of the intense scrutiny the STG has received, how it generates its rhythmic patterns of bursts remains unknown.The novel neural networks presented here model the pyloric CPG of the American lobster (Homarus americanus). Each model’s connectivity is explicit, and its operation depends only on minimal neuron capabilities of excitation and inhibition. One type of model CPGs, flip-flop ring oscillators, is apparently new to engineering, making it an example of neuroscience and logic circuit design informing each other. Several testable predictions are given here, and STG phenomena are shown to support several predictions of neural flip-flops that were given in a previous paper on short-term memory.The model CPGs are not the same as the more complex pyloric CPG. But they show how neurons can be connected to produce oscillations, and there are enough similarities in significant features that they may be considered first approximations, or perhaps simplified versions, of STG architecture. The similarities include 1) mostly inhibitory synapses; 2) pairs of cells with reciprocal, inhibitory inputs, complementary outputs that are approximately 180 degrees out of phase, and state changes occurring with the high output changing first; 3) cells that have reciprocal, inhibitory inputs with more than one other cell; and 4) six cells that produce coordinated oscillations with the same period, four phases distributed approximately uniformly over the period, and half of the burst durations approximately 1/4 of the period and the other half 3/8. These variables cannot be controlled independently in the design, suggesting a similar architecture in the models and the STG.Some of the neural network designs can be derived from electronic logic circuit designs simply by moving each negation symbol from one end of a connection to the other. This does not change the logic of the network, but it changes each logic gate to one that can be implemented with a single neuron.


1992 ◽  
Vol 67 (2) ◽  
pp. 341-349 ◽  
Author(s):  
J. Golowasch ◽  
F. Buchholtz ◽  
I. R. Epstein ◽  
E. Marder

1. The behavior of the mathematical model for the lateral pyloric (LP) neuron of the crustacean stomatogastric ganglion (STG) developed in the previous paper was further studied. 2. The action of proctolin, a neuromodulatory peptide that acts directly on the LP neuron, was modeled. The effect of the proctolin-activated current (iproc) on the model neuron mimics the effects of proctolin on the isolated biological LP neuron. The depolarization and increased frequency of firing seen when iproc is activated are associated with changes in the relative contributions of the delayed rectifier (id) and the Ca(2+)-activated outward current (io(Ca] to the repolarization phase of the action potential. 3. The effects of turning off the A-current (iA) in the model were compared with those obtained by pharmacologically blocking iA in the biological neuron. iA appears to regulate action-potential frequency as well as postinhibitory rebound activity. 4. The role of iA on the rhythmic activity of the cell was studied by modifying several of its parameters while periodically activating a simulated synaptically activated conductance, isyn. 5. The effects of manipulations of the maximal conductances (g) for id and io(Ca) were studied. id strongly influences action-potential frequency, whereas io(Ca) strongly influences action-potential duration. 6. Modifications of the maximal conductance of the inward Ca2+ current (iCa) were compared with the effects of blocking iCa in the real cell. 7. The role of the hyperpolarization-activated inward current (ih) during ongoing rhythmic activity was assessed by periodically activating isyn while modifying ih.


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