The stomatogastric nervous system: Structure and function of a small neural network

Selverston, Allen I.; Russell, David F.; Miller, John P.

doi:10.1016/0301-0082(76)90008-3

Cited by 382 publications

(245 citation statements)

References 49 publications

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“…The stomatogastric nervous system was dissected as described by Selverston et al (1976) and placed in a preparation dish filled with Panulirus saline. The STG was desheathed, enclosed in a small (1 ml) pool of saline walled by Vaseline, and constantly superf used at 3 ml /min with oxygenated saline at 16 -17°C.…”

Section: Methodsmentioning

confidence: 99%

Monoamine Control of the Pacemaker Kernel and Cycle Frequency in the Lobster Pyloric Network

Ayali

Harris‐Warrick

1999

J. Neurosci.

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The monoamines dopamine (DA), serotonin (5HT), and octopamine (Oct) can each sculpt a unique motor pattern from the pyloric network in the stomatogastric ganglion (STG) of the spiny lobster Panulirus interruptus. In this paper we investigate the contribution of individual network components in determining the specific amine-induced cycle frequency. We used photoinactivation of identified neurons and pharmacological blockade of synapses to isolate the anterior burster (AB) and pyloric dilator (PD) neurons. Bath application of DA, 5HT, or Oct enhanced cycle frequency in an isolated AB neuron, with DA generating the most rapid oscillations and Oct the slowest. When an AB-PD or AB-2xPD subnetworks were tested, DA often reduced the ongoing cycle frequency, whereas 5HT and Oct both evoked similar accelerations in cycle frequency. However, in the intact pyloric network, both DA and Oct either reduced or did not alter the cycle frequency, whereas 5HT continued to enhance the cycle frequency as before. Our results show that the major target of 5HT in altering the pyloric cycle frequency is the AB neuron, whereas DA's effects on the AB-2xPD subnetwork are critical in understanding its modulation of the cycle frequency. Octopamine's effects on cycle frequency require an understanding of its modulation of the feedback inhibition to the AB-PD group from the lateral pyloric neuron, which constrains the pacemaker group to oscillate more slowly than it would alone. We have thus demonstrated that the relative importance of the different network components in determining the final cycle frequency is not fixed but can vary under different modulatory conditions.

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Section: Methodsmentioning

confidence: 99%

Monoamine Control of the Pacemaker Kernel and Cycle Frequency in the Lobster Pyloric Network

Ayali

Harris‐Warrick

1999

J. Neurosci.

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“…Standard procedures (Selverston et al, 1976;Harris-Warrick et al, 1992) were used to isolate the complete stomatogastric nervous system (the STG attached to the esophageal and paired commissural ganglia). The preparations were superf used during the dissection with cool, 13-15°C, pH 7.4 -7.5, normal saline containing (in mM): 479 NaC l, 13.7 KC l, 3.9 NaSO 4 , 10 MgSO 4 , 2 glucose, and 5.1 Trizma base acid.…”

Section: Methodsmentioning

confidence: 99%

“…All neurons were identified by their stereotypical axonal projections in identified nerves using conventional techniques (Selverston et al, 1976;Harris-Warrick et al, 1992).…”

Section: Methodsmentioning

confidence: 99%

Temporal Dynamics of Graded Synaptic Transmission in the Lobster Stomatogastric Ganglion

et al. 1997

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Synaptic transmission between neurons in the stomatogastric ganglion of the lobster Panulirus interruptus is a graded function of membrane potential, with a threshold for transmitter release in the range of Ϫ50 to Ϫ60 mV. We studied the dynamics of graded transmission between the lateral pyloric (LP) neuron and the pyloric dilator (PD) neurons after blocking action potential-mediated transmission with 0.1 M tetrodotoxin. We compared the graded IPSPs (gIPSPs) from LP to PD neurons evoked by square pulse presynaptic depolarizations with those potentials evoked by realistic presynaptic waveforms of variable frequency, amplitude, and duty cycle. The gIPSP shows frequency-dependent synaptic depression. The recovery from depression is slow, and as a result, the gIPSP is depressed at normal pyloric network frequencies. Changes in the duration of the presynaptic depolarization produce nonintuitive changes in the amplitude and time course of the postsynaptic responses, which are again frequency-dependent. Taken together, these data demonstrate that the measurements of synaptic efficacy that are used to understand neural network function are best made using presynaptic waveforms and patterns of activity that mimic those in the functional network. Key words: graded synaptic transmission; pyloric network; central pattern generation; oscillations; synaptic depression; inhibitionMost rhythmic movements are produced by central patterngenerating circuits (Marder and C alabrese, 1996). In many cases, the rhythmic movements are produced over a significant frequency range without appreciable alteration of the fundamental phase relationships or the character of the movement; e.g., an animal is allowed to breathe or to walk at different rates, slowly or quickly. Because circuit dynamics depend on both synaptic and intrinsic properties, it is interesting to ask how these dynamics are affected by changes in network frequency. In this paper we present the effects of frequency on the graded synaptic transmission between neurons of the pyloric circuit of the spiny lobster Panulirus interruptus.The pyloric network of the stomatogastric ganglion (STG) of P. interruptus is one of the best understood pattern-generating circuits. The connectivity among these neurons and their intrinsic membrane properties have been determined (Selverston and Miller, 1980;Eisen and Marder, 1982; Miller and Selverston, 1982a,b). Both in vivo and in vitro studies in a variety of crustacean species have shown that the triphasic pyloric rhythm operates over a frequency range from ϳ0.1 to ϳ2.5 Hz (Ayers and Selverston, 1979;Rezer and Moulins, 1983;Eisen and Marder, 1984;T urrigiano and Heinzel, 1992; Hooper, 1997a,b). One of the essential puzzles is how the pyloric rhythm can produce approximately the same motor pattern over such a wide frequency range. One possibility is that time-dependent changes in functional synaptic strength, such as facilitation and depression, play a critical role in maintaining network phase relationships as the frequency changes. This th...

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“…Nonetheless, there are numerous examples of convergent actions of modulators, in which several substances act on the same current (Dunlap and Fischbach, 1978;Jones, 1985;Christie and North, 1988;Nicoll et al, 1990;Bolshakov et al, 1993; Brezina et al, 1994a,b;van Tol-Steye et al, 1997;Sodickson and Bean, 1998). Convergent actions of modulators may appear to be redundant at the level of the single neuron but may not be redundant at the level of network behavior, if different substances activate different receptors on separate populations of target neurons.The crustacean stomatogastric ganglion (STG) contains the neurons responsible for producing the well described pyloric and gastric mill rhythms (Selverston et al, 1976;Harris-Warrick et al, 1992). The pyloric and gastric mill rhythms are modulated by a large number of peptides and amines that are present as circulating hormones and/or are released from modulatory projection and sensory neurons (Marder, 1987;Harris-Warrick et al, 1992;Christie et al, 1995;Marder et al, 1995;Marder and Calabrese, 1996).…”

mentioning

confidence: 99%

“…The crustacean stomatogastric ganglion (STG) contains the neurons responsible for producing the well described pyloric and gastric mill rhythms (Selverston et al, 1976;Harris-Warrick et al, 1992). The pyloric and gastric mill rhythms are modulated by a large number of peptides and amines that are present as circulating hormones and/or are released from modulatory projection and sensory neurons (Marder, 1987;Harris-Warrick et al, 1992;Christie et al, 1995;Marder et al, 1995;Marder and Calabrese, 1996).…”

mentioning

confidence: 99%

Multiple Peptides Converge to Activate the Same Voltage-Dependent Current in a Central Pattern-Generating Circuit

2000

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The stomatogastric ganglion of the crab, Cancer borealis, is modulated by Ͼ20 different substances, including numerous neuropeptides. One of these peptides, proctolin, activates an inward current that shows strong outward rectification (Golowasch and Marder, 1992). Decreasing the extracellular Ca 2ϩ concentration linearizes the current-voltage curve of the proctolin-induced current. We used voltage clamp to study the currents evoked by proctolin and five additional modulators [C. borealis tachykinin-related peptide Ia (CabTRP Ia), crustacean cardioactive peptide, red pigment-concentrating hormone, TNRNFLRFamide, and the muscarinic agonist pilocarpine] in stomatogastric ganglion neurons, both in the intact ganglion and in dissociated cell culture. Subtraction currents yielded proctolinlike current-voltage relationships for all six substances, and the current-voltage curves of all six substances showed linearization in low external Ca 2ϩ . The lateral pyloric neuron responded to all six modulators, but the ventricular dilator neuron only responded to a subset of them. Bath application of saturating concentrations of proctolin occluded the response to CabTRP and vice versa. N-(6-Aminohexyl)-5-chloro-1-napthalensulfonamide, a calmodulin inhibitor, increased the amplitude and altered the voltage dependence of the responses elicited by CabTRP and proctolin. Together, these data indicate that all six substances converge onto the same voltage-dependent current, although they activate different receptors. Therefore, differential network responses evoked by these substances may primarily depend on the receptor distribution on network neurons.Key words: stomatogastric ganglion; crab; Cancer borealis; proctolin; CCAP; RPCH; crab tachykinin-related peptide; FLRFamide-related peptides Nervous systems contain many neuropeptides and amines that modulate synaptic strength and cellular excitability (Nicoll et al., 1990;Kupfermann, 1991;Marder and Calabrese, 1996;Marder, 1998). Most voltage-dependent ion channels are subject to modulation by one or more substances, and many agonists modulate multiple membrane currents (Kaczmarek and Levitan, 1987;Levitan, 1988Levitan, , 1994 Hille, 1992Hille, , 1994Gudermann et al., 1997). In principle, the large number of different intrinsic and synaptic currents subject to modulation could provide the potential substrate for virtually infinite modifications of circuit behavior under different modulatory conditions. Nonetheless, there are numerous examples of convergent actions of modulators, in which several substances act on the same current (Dunlap and Fischbach, 1978;Jones, 1985;Christie and North, 1988;Nicoll et al., 1990;Bolshakov et al., 1993; Brezina et al., 1994a,b;van Tol-Steye et al., 1997;Sodickson and Bean, 1998). Convergent actions of modulators may appear to be redundant at the level of the single neuron but may not be redundant at the level of network behavior, if different substances activate different receptors on separate populations of target neurons.The crustacean stomatogast...

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The stomatogastric nervous system: Structure and function of a small neural network

Cited by 382 publications

References 49 publications

Monoamine Control of the Pacemaker Kernel and Cycle Frequency in the Lobster Pyloric Network

Monoamine Control of the Pacemaker Kernel and Cycle Frequency in the Lobster Pyloric Network

Temporal Dynamics of Graded Synaptic Transmission in the Lobster Stomatogastric Ganglion

Multiple Peptides Converge to Activate the Same Voltage-Dependent Current in a Central Pattern-Generating Circuit

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