Organization of the stomatogastric neuropil of the crab, Cancer borealis, as revealed by modulator immunocytochemistry

Christie, Andrew E.; Baldwin, David H.; Marder, Eve; Graubard, Katherine

doi:10.1007/s004410050801

Cited by 44 publications

(37 citation statements)

References 42 publications

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“…of the M PNs, we were able to conclude that these neurons are not immunoreactive for serotonin or histamine (Beltz et al, 1984;Katz et al, 1989;Christie, 1995) or TN RN FLRFamide, CabTRP Ia, red pigment-concentrating hormone-like, allatostatin-like, buccalin-like, myomodulin-like, or cholecystokinin-like peptides Goldberg et al, 1988;Nusbaum and Marder, 1988;Christie et al, 1994Christie et al, , 1995Christie et al, , 1997cSkiebe and Schneider, 1994).…”

Section: Mpn Cotransmitter Complementmentioning

confidence: 89%

“…We also paired intracellular LY fills of MCN1 SNAX with FMRFamide immunocytochemistry and determined that MCN1 SNAX is not FMRFamide immunoreactive (n ϭ 4). Christie et al (1997c) demonstrated that MCN1 SNAX also exhibits no cholecystokinin-like immunoreactivity. MCN1 SNAX is not serotonergic, because all of the serotonin (5-HT) immunoreactivity within the crab STG arises from the arbors of identified sensory neurons (Katz et al, 1989).…”

Section: Mcn1 Cotransmitter Complementmentioning

confidence: 99%

“…Note: In many of the images shown here, there appears to be incomplete colocalization of dye and immunoreactivity. This is because nearly all modulator immunoreactivity in the neuropil is confined to varicose swellings present on the smalldiameter terminal branches and is not always found within processes that connect these varicosities (Christie et al, 1997c).…”

Section: Mpn Cotransmitter Complementmentioning

confidence: 99%

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Different Proctolin Neurons Elicit Distinct Motor Patterns from a Multifunctional Neuronal Network

et al. 1999

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Distinct motor patterns are selected from a multifunctional neuronal network by activation of different modulatory projection neurons. Subsets of these projection neurons can contain the same neuromodulator(s), yet little is known about the relative influence of such neurons on network activity. We have addressed this issue in the stomatogastric nervous system of the crab Cancer borealis. Within this system, there is a neuronal network in the stomatogastric ganglion (STG) that produces many versions of the pyloric and gastric mill rhythms. These different rhythms result from activation of different projection neurons that innervate the STG from neighboring ganglia and modulate STG network activity. Three pairs of these projection neurons contain the neuropeptide proctolin. These include the previously identified modulatory proctolin neuron and modulatory commissural neuron 1 (MCN1) and the newly identified modulatory commissural neuron 7 (MCN7). We document here that each of these neurons contains a unique complement of cotransmitters and that each of these neurons elicits a distinct version of the pyloric motor pattern. Moreover, only one of them (MCN1) also elicits a gastric mill rhythm. The MCN7-elicited pyloric rhythm includes a pivotal switch by one STG network neuron from playing a minor to a major role in motor pattern generation. Therefore, modulatory neurons that share a peptide transmitter can elicit distinct motor patterns from a common target network.

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Section: Mpn Cotransmitter Complementmentioning

confidence: 89%

Section: Mcn1 Cotransmitter Complementmentioning

confidence: 99%

Section: Mpn Cotransmitter Complementmentioning

confidence: 99%

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Different Proctolin Neurons Elicit Distinct Motor Patterns from a Multifunctional Neuronal Network

et al. 1999

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“…Although extensive neuroanatomical and immunocytochemical work has demonstrated complex and rich patterns of colocalization for amines and peptides, how these substances modulate specific functional circuits remains relatively unknown. The stomatogastric nervous system contains ϳ20 different identified modulatory substances (Marder and Weimann, 1992;Marder et al, 1995;Christie et al, 1997a;Abbott and Marder, 1998), each of which can alter the STG motor patterns. The effects of serotonin (Kiehn and HarrisWarrick, 1992a,b;Zhang and Harris-Warrick, 1995), dopamine (Harris-Warrick et al, 1995a,b;Kloppenburg et al, 1999), and the peptide proctolin (Golowasch and Marder, 1992) have been characterized, but until now, the biophysical actions of most of the modulatory substances found in inputs to the STG were unknown.…”

Section: Discussionmentioning

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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“…It was purified based on its myotropic actions on the insect hindgut, and was subsequently found to have wide distribution throughout the arthropods (2)(3)(4). In the crab Cancer, proctolin has potent effects on defined neural circuits within the stomatogastric system (5) and at the neuromuscular junction (6).…”

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confidence: 99%

Identification and characterization of a G protein-coupled receptor for the neuropeptide proctolin in Drosophila melanogaster

Johnson

Garczynski

Park

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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Proctolin is a bioactive neuropeptide that modulates interneuronal and neuromuscular synaptic transmission in a wide variety of arthropods. We present several lines of evidence to propose that the orphan G protein-coupled receptor CG6986 of Drosophila is a proctolin receptor. When expressed in mammalian cells, CG6986 confers second messenger activation after proctolin application, with an EC 50 of 0.3 nM. In competition-based studies, the CG6986 receptor binds proctolin with high affinity (IC50 ‫؍‬ 4 nM). By microarray analysis, CG6986 transcript is consistently detected in head mRNA of different genotypes, and under different environmental conditions. By blot analysis, anti-CG6986 antibodies detect a band in tissue homogenates similar to the predicted size of the protein. Proctolin receptor immunosignals are found in the hindgut, heart, and in distinct neuronal populations of the CNS; such patterns correlate with previous demonstrations of proctolin biological activity, and in several instances, with areas of proctolin peptide immunosignals. The identification of a bona fide proctolin receptor provides the basis for a mechanistic analysis of this critical synaptic modulator.T he pentapeptide proctolin (RYLPT) was the first neuropeptide to be isolated and sequenced from insects (1). It was purified based on its myotropic actions on the insect hindgut, and was subsequently found to have wide distribution throughout the arthropods (2-4). In the crab Cancer, proctolin has potent effects on defined neural circuits within the stomatogastric system (5) and at the neuromuscular junction (6). In insects, proctolin is a major peptide cotransmitter and it modulates contractions of both somatic and visceral muscles (7,8). Proctolin-like immunosignals are found within a small number of neurons in the larval CNS of Drosophila and these include efferents to bodywall muscles, heart, and viscera (9).The mechanisms of actions of proctolin have also been investigated. Proctolin elevates levels of inositol trisphosphate (IP 3 ) and cAMP, and increases calcium entry through voltagegated ion channels (10-13). Several studies have suggested the existence of multiple proctolin receptor subtypes based on binding studies and activities of proctolin (14, 15) or its structural analogues (16-19). However, more recent studies (15,20,21) of proctolin binding support a model featuring a single proctolin receptor. The identification of a specific proctolin receptor will help address issues regarding possibilities of multiple receptors, the precise nature of proctolin-dependent signaling pathways, and phylogenetic differences in proctolin signaling. The significance of such studies is substantial because proctolin exerts such a widespread role as a synaptic modulator in arthropod physiology.Analysis of the completed Drosophila genomic sequences (22, 23) identified Ͼ100 genes encoding G protein-coupled receptors (GPCRs). Further analysis indicated that 44 such receptors are likely to have peptide ligands and that the majority of these are derive...

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Organization of the stomatogastric neuropil of the crab, Cancer borealis, as revealed by modulator immunocytochemistry

Cited by 44 publications

References 42 publications

Different Proctolin Neurons Elicit Distinct Motor Patterns from a Multifunctional Neuronal Network

Different Proctolin Neurons Elicit Distinct Motor Patterns from a Multifunctional Neuronal Network

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

Identification and characterization of a G protein-coupled receptor for the neuropeptide proctolin in Drosophila melanogaster

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