Neuropeptides are ubiquitous chemical mediators: Using the stomatogastric nervous system as a model system
Freie Universität Berlin, Fachbereich Biologie, Chemie, Pharmazie, Neurobiologie, Königin-Luise-Straße 2830, D-14195 Berlin, Germany
*e-mail: skiebe{at}zedat.fu-berlin.de
Accepted March 12, 2001
![]() |
Summary |
---|
Key words: neuropeptide, neurohormone, modulation, crustacean, neural network, motor pattern generation.
![]() |
Introduction |
---|
To study peptides as neurotransmitters, it was important to study identified neurones containing neuropeptides or the effects of particular peptides on identified neurones embedded in small circuits of known function. Some invertebrate systems fulfilled these needs and have contributed to our understanding of peptide function. The mollusc Aplysia californica, for example, has been used to increase our knowledge about peptide co-transmission in studies of the actions of identified motoneurones containing known peptides (Weiss et al., 1993; Brezina and Weiss, 1997). Research on the mollusc Lymnaea stagnalis has demonstrated that two alternative mRNA transcripts of the gene coding for FMRFamide-related peptides are expressed in the CNS in a mutually exclusive manner, resulting in the differential distribution of distinct sets of neuropeptides in single neurones (Santama and Benjamin, 2000). In the insect Manduca sexta, sequential motor patterns were elicited by neuropetides released in a timed hierarchy (Gammie and Truman, 1997).
This review describes research on neuropeptides performed in another invertebrate system, the stomatogastric nervous system (STNS) of decapod crustaceans. This research has demonstrated that even small neural circuits are modulated by a large number of neuropeptides and has provided insights into mechanisms by which neuropeptides change motor patterns (Harris-Warrick et al., 1992; Marder and Weimann, 1992; Marder et al., 1994; Marder et al., 1997). The STNS is therefore an excellent model system demonstrating that peptides are strongly involved in the plasticity of neural networks. The goal of this review is to summarise our knowledge about the ubiquitous distribution of peptides within the STNS and to reassess the role of peptidergic neurones in the modulation of motor pattern generation in this model system.
![]() |
The stomatogastric nervous system |
---|
|
|
![]() |
Peptides in neurohaemal organs and neurohaemal release zones |
---|
|
![]() |
Peptides in the stomatogastric ganglion |
---|
Peptidergic cell bodies in the stomatogastric ganglion
The cell bodies of neurones that release peptides as transmitters within the STG are found either within the STG or projecting to the STG, mostly from the CoGs or the OG (Coleman et al., 1992). Although numerous antibodies against peptides have been used, evidence for peptidergic cell bodies within the adult STG was found only for the FMRFamide and allatostatin families (Fig.2A: a; Table1). Since only FLRFamides and no FMRFamides have been isolated from crustaceans (Trimmer et al., 1987; Mercier et al., 1993; Keller, 1992; Weimann et al., 1993), immunoreactivity detected using an antibody against FMRFamide will be referred to as FLRFamide-like immunoreactivity. The first peptidergic neurones noted were three FLRFamide-like immunoreactive cell bodies in the shrimp Palaemon serratus (Meyrand and Marder, 1991), and these were thought to be an exception. In Homarus americanus, 34 FLRFamide-like immunoreactive cell bodies were found in half the animals investigated with one antibody (Table1; Kilman et al., 1999), which were previously not found using a different antibody (Marder, 1987). Allatostatin-like immunoreactive neurones were found in two crayfish species (Cherax destructor and Procambarus clarkii) (Skiebe, 1999). Over the course of development, peptidergic cell bodies appear in the STG during some stages. In two lobster species (Homarus americanus and Homarus gammarus), FLRFamide- and proctolin-like immunoreactivity is expressed transiently, although the time window differs even in closely related species (Fig.2: d; Table1) (Fénelon et al., 1998; Fénelon et al., 1999; Kilman et al., 1999). The identity of none of these peptidergic neurones is known, either in the adult or in the embryonic or larval STG.
|
![]() |
Peptidergic interneurones projecting into the stomatogastric ganglion |
---|
|
One way to activate modulatory neurones with cell bodies in the CoG is by sensory input. In Homarus gammarus, the commissural gastric neurone (CG), which shows FLRFamide-like immunoreactivity (P. Meyrand, unpublished data), and the gastric inhibitor neurone (GI) are excited by the anterior gastric receptor (AGR, Fig.4) (Combes et al., 1999a; Combes et al., 1999b). AGR is a primary mechanoreceptor measuring the tension of a gastric mill muscle. It does not have ramifications in the STG but it projects through the STG to arborize in the CoGs. Depending on the firing frequency of AGR, one of two gastric mill motor patterns is elicited as a result of the different postsynaptic sensitivities of CG and GI to AGR. When AGR fires weakly, one gastric mill pattern is elicited. When AGR fires strongly, the second gastric mill pattern is elicited, demonstrating that feedback from a single mechanoreceptor is able to select different motor patterns (Combes et al., 1999b). This also demonstrates that different modulatory neurones can be co-activated and that pattern selection is dependent on the ensemble of modulatory neurones that are active. A second example of this is MCN1, which elicits a different gastric mill motor pattern when co-activated with CPN2 (Fig.4; Blitz and Nusbaum, 1997).
In seven species, a pair of neurones with cell bodies in the ivn was found that had axons projecting to the STG (Table1). These neurons are likely to contain histamine and/or FLRFamide-like peptides (Claiborne and Selverston, 1984a; Mulloney and Hall, 1991; Tierney et al., 1997; Kilman, 1998; Skiebe et al., 1999; Le Feuvre et al., 2000; Christie et al., 2000) and are referred to as ivn-through fibres (ivn-TF; Claiborne and Selverston, 1984a; Claiborne and Selverston, 1984b) or pyloric suppressor (PS) neurones (Cazalets et al., 1987; Cazalets et al., 1990). Both the ivn-TF in Panulirus interruptus and the PS neurones in Homarus gammarus elicit inhibitory effects on the pyloric rhythm of the STG. The inhibitory effect of the ivn-TF is frequency-dependent such that, at low frequencies, an excitatory action dominates, but this gives way to an inhibitory action at higher frequencies (Sigvardt and Mulloney, 1982; Claiborne and Selverston, 1984a; Claiborne and Selverston, 1984b), demonstrating that the effects of modulatory projection neurones can be frequency-dependent.
![]() |
Peptides present within the nerves of the stomatogastric nervous system |
---|
![]() |
Peptides and sensory neurones |
---|
![]() |
Peptides and stomach muscles |
---|
|
![]() |
Peptides and network function |
---|
|
It is not possible to discuss the effects of all peptides on the networks of the STG within the scope of this review (for reviews, see Harris-Warrick et al., 1992; Marder and Weimann, 1992; Marder et al., 2001). I will illustrate this research using studies of red pigment-concentrating hormone (RPCH). The presence of RPCH was demonstrated immunohistochemically in all four ganglia of the STNS (Nusbaum and Marder, 1988; Dickinson and Marder, 1989). Bath application of RPCH either to the CoGs and OG or to the STG activates a previously silent cardiac sac rhythm, but the rhythms differ with the site of application, demonstrating that a pattern-generating network can be modulated at more than one site and that the resultant modulations depend on the site of release of the modulator (Dickinson and Marder, 1989; Dickinson et al., 1993). RPCH is also able to fuse two pattern-generating networks as a result of enhancing the synaptic strength of the synapses between the two networks (Dickinson et al., 1990). That the modulatory history matters was shown by applying the two peptides sequentially. The likelihood that proctolin would initiate a cardiac sac rhythm was greatly enhanced if application of proctolin was preceded by an application of RPCH (Dickinson et al., 1997).
![]() |
Conclusions and future directions |
---|
To answer questions concerning cotransmission, either pharmacological separation of cotransmitter actions (Wood et al., 2000) or the effect of applying mixtures will have to be studied. For allatostatin and serotonin, the early data show that co-application causes a stronger reduction in the pyloric cycle frequency than either modulator alone (Marder et al., 1994). However, this might be different for co-localised peptides. In the example of proctolin and Cancer borealis tachykinin, which are co-localized in MCN1 (Blitz et al., 1999), both peptides competitively activate the same current (Swensen and Marder, 2000a). As this case suggests, to understand how a particular neurone elicits a unique motor pattern, not only will the postsynaptic neurons and currents have to be identified, but also co-application experiments will have to be compared with experiments using various stimulation patterns of the identified neurone.
To understand more about the role of peptides during development, it is necessary to determine the effects of bath-applied peptides, as has been started in Homarus americanus (Marder and Richards, 1999), to identify target neurones and individual peptidergic neurones and to study their effects from the cellular to the network level, as has been done in the adult. There is already evidence that embryonic neurones do not possess the same capacity to initiate large regenerative depolarisations as adult neurones (Casasnovas and Meyrand, 1995). It would be beneficial to include additional species (so far only Homarus americanus and Homarus gammarus have been investigated), since much can be learned by comparing species. The neurones of the crab Cancer borealis, for example, are much more flexible with respect to their membership in a particular motor pattern (Weimann et al., 1991) than those of lobsters.
Most of our knowledge concerning the peptide content of neurones is based on immunocytochemistry. In the case peptides such as proctolin and crustacean cardioactive peptide, which have the same amino acid sequence in all arthropod species investigated (Dircksen, 1994), immunocytochemistry provides strong evidence for the presence of the peptide. In the case of peptide families, immunocytochemistry can only be the first step since a given antibody might recognise all or only a subset of the members of a peptide family. Peptides must therefore be identified unambiguously at the level of a single neurone, as has been pioneered in molluscs (for reviews, see Jiménez and Burlingame, 1998; Li et al., 2000).
As a result of the abundant knowledge about the networks of the STG accumulated over the last 40 years and the ability to study identified peptidergic neurones, including sensory neurones, motoneurones and interneurones, both in the adult and during development, research on the STNS of decapod crustaceans will continue to increase our understanding of the role of peptides in the nervous system.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
Barker, D. L., Kushner, P. D. and Hooper, N. K. (1979). Synthesis of dopamine and octopamine in the crustacean stomatogastric nervous system. Brain Res. 161, 99113.[Medline]
Bartos, M. and Nusbaum, M. P. (1997). Intercircuit control of motor pattern modulation by presynaptic inhibition. J. Neurosci. 17, 22472256.
Beltz, B., Eisen, J. S., Flamm, R., Harris-Warrick, R., Hooper, S. and Marder, E. (1984). Serotonergic innervation and modulation of the stomatogastric ganglion of three decapod crustaceans (Panulirus interruptus, Homarus americanus and Cancer irroratus). J. Exp. Biol. 109, 3554.[Abstract]
Birmingham, J. T., Abbott, L. F. and Marder, E. (1998). Reconstruction of a stretch stimulus in the crab nervous system in different neuromodulatory conditions. Soc. Neurosci. Abstr. 24, 156.
Blitz, D. M., Christie, A. E., Coleman, M., Norris, B. J. and Nusbaum, M. P. (1999). Different proctolin neurons elicit distinct motor patterns from a multifunctional neuronal network. J. Neurosci. 19, 54495463.
Blitz, D. M., Christie, A. E., Marder, E. and Nusbaum, M. P. (1995). Distribution and effects of tachykinin-like peptides in the stomatogastric nervous system of the crab, Cancer borealis. J. Comp. Neurol. 354, 282294.[Medline]
Blitz, D. M. and Nusbaum, M. P. (1997). Motor pattern selection via inhibition of parallel pathways. J. Neurosci. 17, 49654975.
Blitz, D. M. and Nusbaum, M. P. (1999). Distinct functions for cotransmitters mediating motor pattern selection. J. Neurosci. 15, 67746783.
Brezina, V, and Weiss, K. R. (1997). Analysing the functional consequences of transmitter complexity. Trends Neurosci. 20, 538543.[Medline]
Brown, B. E. and Starrat, A. N. (1975). Isolation of proctolin, a myotropic peptide, from Periplaneta americana. J. Insect Physiol. 21, 18791881.
Casasnovas, B. and Meyrand, P. (1995). Functional differentiation of adult neural circuits from a single embryonic network. J. Neurosci. 15, 57035718.[Abstract]
Cazalets, J. R., Nagy, F. and Moulins, M. (1987). Suppressive control of a rhythmic central pattern generator by an identified modulatory neuron in crustacea. Neurosci. Lett. 81, 267272.[Medline]
Cazalets, J. R., Nagy, F. and Moulins, M. (1990). Suppressive control of the crustacean pyloric network by a pair of identified interneurons. I. Modulation of the motor pattern. J. Neurosci. 10, 448457.[Abstract]
Christie, A. E., Baldwin, D., Turrigiano, G., Graubard, K. and Marder, E. (1995a). Immunocytochemical localization of multiple cholecystokinin-like peptides in the stomatogastric ganglion of the crab Cancer borealis. J. Exp. Biol. 198, 263271.
Christie, A. E., Baldwin, D. H., Marder, E. and Graubard, K. (1997a). Organization of the stomatogastric neuropil of the crab, Cancer borealis, as revealed by modulator immunocytochemistry. Cell Tissue Res. 288, 135148.[Medline]
Christie, A. E., Hall, C., Oshinsky, M. and Marder, E. (1994). Buccalin-like and myomodulin-like peptides in the stomatogastric ganglion of the crab Cancer borealis. J. Exp. Biol. 193, 337343.
Christie, A. E., Lundquist, C. T., Nässel, D. R. and Nusbaum, M. P. (1997b). Two novel tachykinin-related peptides from the nervous system of the crab Cancer borealis. J. Exp. Biol. 200, 22792294.
Christie, A. E. and Nusbaum, M. P. (1995). Distribution and effects of corazonin-like and allatotropin-like peptides in the crab stomatogastric nervous system. Soc. Neurosci. Abstr. 21, 629.
Christie, A. E. and Nusbaum, M. P. (1999). Neuromodulation of neural network activity at an extraganglionic site. Soc. Neurosci. Abstr. 25, 1645.
Christie, A. E., Skiebe, P. and Marder, E. (1995b). Matrix of neuromodulators in neurosecretory structures of the crab Cancer borealis. J. Exp. Biol. 198, 24312439.
Christie, A. E., Stein, W., Quinlan, J. E. and Nusbaum, M. P. (2000). Histaminergic innervation of the crab stomatogastric system. Soc. Neurosci. Abstr. 26, 449.
Claiborne, B. J. and Selverston, A. I. (1984a). Histamine as a neurotransmitter in the stomatogastric nervous system of the spiny lobster. J. Neurosci. 4, 708721.[Abstract]
Claiborne, B. J. and Selverston, A. I. (1984b). Localization of stomatogastric IV neuron cell bodies in lobster brain. J. Comp. Physiol. A 154, 2732.
Coleman, M. J., Meyrand, P. and Nusbaum, M. P. (1995). A switch between two modes of synaptic transmission mediated by presynaptic inhibition. Nature 378, 502505.[Medline]
Coleman, M. J. and Nusbaum, M. P. (1994). Functional consequences of compartmentalization of synaptic input. J. Neurosci. 14, 65446552.[Abstract]
Coleman, M. J., Nusbaum, M. P., Cournil, I. and Claiborne, B. J. (1992). Distribution of modulatory inputs to the stomatogastric ganglion of the crab, Cancer borealis. J. Comp. Neurol. 325, 581594.[Medline]
Combes, D., Meyrand, P. and Simmers, J. (1999a). Motor pattern specification by dual descending pathways to a lobster rhythm-generating network. J. Neurosci. 19, 36103619.
Combes, D., Meyrand, P. and Simmers, J. (1999b). Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster. J. Neurosci. 19, 36203628.
Combes, D., Simmers, J. and Moulins, M. (1997). Conditional dendritic oscillators in a lobster mechanoreceptor neurone. J. Physiol., Lond. 499, 161177.[Abstract]
Cournil, I., Casasnovas, B., Helluy, S. M. and Beltz, B. S. (1995). Dopamine in the lobster Homarus gammarus. II. Dopamine-immunoreactive neurons and development of the nervous system. J. Comp. Neurol. 362, 116.[Medline]
Cournil, I., Helluy, S. M. and Beltz, B. S. (1994). Dopamine in the lobster Homarus gammarus. I. Comparative analysis of dopamine and tyrosine hydroxylase immunoreactivities in the nervous system of the juvenile. J. Comp. Neurol. 344, 455469.[Medline]
Cournil, I., Meyrand, P. and Moulins, M. (1990). Identification of all GABA immunoreactive neurones projecting to the lobster stomatogastric ganglion. J. Neurocytol. 19, 478493.[Medline]
De Wied, D. (1971). Long term effect of vassopressin on the maintenance of a conditioned avoidance response in rats. Nature 232, 5860.[Medline]
Dickinson, P. S., Fairfield, W. P., Hetling, J. R. and Hauptman, J. (1997). Neurotransmitter interactions in the stomatogastric system of the spiny lobster, one peptide alters the response of a central pattern generator to a second peptide. J. Neurophysiol. 77, 599610.
Dickinson, P. S. and Marder, E. (1989). Peptidergic modulation of a multioscillator system in the lobster. I. Activation of the cardiac sac motor pattern by the neuropeptides proctolin and red pigment-concentrating hormone. J. Neurophysiol. 61, 833844.
Dickinson, P. S., Mecsas, C., Hetling, J. and Terio, K. (1993). The neuropeptide red pigment-concentrating hormone affects rhythmic pattern generation at multiple sites. J. Neurophysiol. 69, 14751483.
Dickinson, P. S., Mecsas, C. and Marder, E. (1990). Neuropeptide fusion of two motor pattern generator circuits. Nature 344, 155158.[Medline]
Dickinson, P. S., Nagy, F. and Moulins, M. (1981). Interganglionic communication by spiking and nonspiking fibers in same neuron. J. Neurophysiol. 45, 11251138.
Dircksen, H. (1994). Distribution and physiology of crustacean cardioactive peptide in arthropods. In Perspectives in Comparative Endocrinology (ed. K. G. Davey, R. E. Peter and S. S. Tobe), pp. 139148. Ottawa: National Research Council of Canada.
Dircksen, H., Skiebe, P., Abel, B., Agricola, H., Buchner, K., Muren, J. E. and Nässel, D. R. (1999). Localization, structure and biological functions of a native allatostatin-like inhibitory neuropeptide of the crayfish, Orconectes limosus. Peptides 20, 695712.[Medline]
Fénelon, V. S., Casasnovas, B., Faumont, S. and Meyrand, P. (1998). Ontogenetic alteration in peptidergic expression within a stable neuronal population in lobster stomatogastric nervous system. J. Comp. Neurol. 399, 289305.[Medline]
Fénelon, V. S., Kilman, V. L., Meyrand, P. and Marder, E. (1999). Sequential development acquisition of neuromodulatory inputs to a central pattern-generating network. J. Comp. Neurol. 408, 335351.[Medline]
Fernlund, P. (1971). Chromactivating hormones of Pandalus borealis: isolation and purification of a light-adapting hormone. Biochim. Biophys. Acta 237, 519529.[Medline]
Fernlund, P. (1976). Structure of a light-adapting hormone from the shrimp, Pandalus borealis. Biochim. Biophys. Acta 439, 1725.[Medline]
Fernlund, P. and Josefsson, L. (1972). Crustacean color-change hormone: amino acid sequence and chemical synthesis. Science 177, 173175.[Medline]
Friend, B. J. (1976). Morphology and location of dense-core vesicles in the stomatogastric ganglion of the lobster, Panulirus interruptus. Cell Tissue Res. 175, 369390.[Medline]
Gammie, S. C. and Truman, J. W. (1997). Neuropeptide hierarchies and activation of sequential motor behaviors in the hawkmoth, Manduca sexta. J. Neurosci. 17, 43894397.
Goldberg, D., Nusbaum, M. P. and Marder, E. (1988). Substance P-like immunoreactivity in the stomatogastric nervous systems of the crab Cancer borealis and the lobsters Panulirus interruptus and Homarus americanus. Cell Tissue Res. 252, 515522.[Medline]
Golowasch, J. and Marder, E. (1992). Proctolin activates an inward current whose voltage dependence is modified by extracellular Ca2+. J. Neurosci. 12, 810817.[Abstract]
Harris-Warrick, R. M., Ayali, A., Baro, D. J., Johnson, B. R., Kim, M., Kloppenburg, P., Peck, J. H. and Tierney, A. J. (1998a). Potassium channels, amines and the control of a small neural network. In New Neuroethology on the Move: Proceedings of the 26th Gottingen Neurobiology Conference (ed. N. Elsner), pp. 87104. Stuttgart: Georg Thieme Verlag.
Harris-Warrick, R. M., Coniglio, L. M., Barazangi, N., Guckenheimer, J. and Gueron, S. (1995a). Dopamine modulation of transient potassium current evokes phase shifts in a central pattern generator network. J. Neurosci. 15, 342358.[Abstract]
Harris-Warrick, R. M., Coniglio, L. M., Levini, R. M., Gueron, S. and Guckenheimer, J. (1995b). Dopamine modulation of two subthreshold currents produces phase shifts in activity of an identified motoneuron. J. Neurophysiol. 74, 14041420.
Harris-Warrick R. M., Johnson, B. R., Peck, J. H., Kloppenburg, P., Ayali A. and Skarbinski, J. (1998b). Distributed effects of dopamine modulation in the crustacean pyloric network. Ann. N.Y. Acad. Sci. 860, 155167.
Harris-Warrick, R. M., Nagy, F. and Nusbaum, M. P. (1992). Neuromodulation of stomatogastric networks by identified neurons and transmitters. In Dynamic Biological Networks: The Stomatogastric Nervous System (ed. R. M. Harris-Warrick, E. Marder, A. I. Selverston and M. Moulins), pp. 87138. Cambridge, MA: MIT Press.
Heinzel, H. G. (1988). Gastric mill activity in the lobster. I. Spontaneous modes of chewing. J. Neurophysiol. 59, 528550.
Heinzel, H. G. and Selverston, A. I. (1988). Gastric mill activity in the lobster. III. Effects of proctolin on the isolated central pattern generator. J. Neurophysiol. 59, 566585.
Hökfelt, T. (1991). Neuropeptides in perspective: The last ten years. Neuron 7, 867879.[Medline]
Hooper, S. L. and Marder, E. (1984). Modulation of a central pattern generator by two neuropeptides, proctolin and FMRFamide. Brain Res. 305, 186191.[Medline]
Hooper, S. L. and Marder, E. (1987). Modulation of the lobster pyloric rhythm by the peptide proctolin. J. Neurosci. 7, 20972112.[Abstract]
Jiménez, C. R. and Burlingame, A. L. (1998). Ultramicroanalysis of peptide profiles in biological samples using MALDI mass spectrometry. Exp. Nephrol. 6, 421428.[Medline]
Jorge-Rivera, J. C. and Marder, E. (1996). TNRNFLRFamide and SDRNFLRFamide modulate muscles of the stomatogastric system of the crab Cancer borealis. J. Comp. Physiol. A 179, 741751.[Medline]
Jorge-Rivera, J. C. and Marder, E. (1997). Allatostatin decreases stomatogastric neuromuscular transmission in the crab Cancer borealis. J. Exp. Biol. 200, 29372946.
Jorge-Rivera, J. C., Sen, K., Birmingham, J. T., Abbott, L. F. and Marder, E. (1998). Temporal dynamics of convergent modulation at a crustacean neuromuscular junction. J. Neurophysiol. 80, 25592570.
Katz, P. S., Eigg, M. H. and Harris-Warrick, R. M. (1989). Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells. J. Neurophysiol. 62, 558570.
Katz, P. S. and Harris-Warrick, R. M. (1990). Actions of identified neuromodulatory neurons in a simple motor system. Trends Neurosci. 13, 367373.[Medline]
Katz, P. S. and Tazaki, K. (1992). Comparative and evolutionary aspects of the crustacean stomatogastric system. In Dynamic Biological Networks: The Stomatogastric Nervous System (ed. R. M. Harris-Warrick, E. Marder, A. I. Selverston and M. Moulins), pp. 221262. Cambridge, MA: MIT Press.
Keller, R. (1992). Crustacean neuropeptides: structure, functions and comparative aspects. Experientia 48, 439448.[Medline]
Kiehn, O. and Harris-Warrick, R. M. (1992a). Serotonergic stretch receptors induce plateau properties in a crustacean motor neuron by a dual-conductance mechanism. J. Neurophysiol. 68, 485495.
Kiehn, O. and Harris-Warrick, R. M. (1992b). 5-HT modulation of hyperpolarization-activated inward current and calcium-dependent outward current in a crustacean motor neuron. J. Neurophysiol. 68, 496508.
Kilman, V. L. (1998). Multiple roles of neuromodulators throughout life: An anatomical study of the crustacean stomatogastric nervous system. Thesis, Brandeis University, Waltham, Massachusetts, USA.
Kilman, V. L., Fénelon, V. S., Richards, K. S., Thirumalai, V., Meyrand, P. and Marder, E. (1999). Sequential development acquisition of cotransmitters in identified sensory neurons of the stomatogastric nervous system of the lobsters, Homarus americanus and Homarus gammarus. J. Comp. Neurol. 408, 318334.[Medline]
Kilman, V. L. and Marder, E. (1996). Ultrastructure of the stomatogastric ganglion of the crab, Cancer borealis. J. Comp. Neurol. 374, 362375.[Medline]
Kilman, V. L. and Marder, E. (1997). Extraganglionic neuropil-control of projection neurons or neurohemal organ? Soc. Neurosci. Abstr. 23, 477.
King, D. G. (1976). Organization of crustacean neuropil. I. Patterns of synaptic connections in lobster stomatogastric ganglion. J. Neurocytol. 5, 207237.[Medline]
Kloppenburg, P., Levini, R. M. and Harris-Warrick, R. M. (1999). Dopamine modulates two potassium currents and inhibits the intrinsic firing properties of an identified motor neuron in a central pattern generator network. J. Neurophysiol. 81, 2938.
Kushner, P. D. and Barker, D. L. (1983). A neurochemical description of the dopaminergic innervation of the stomatogastric ganglion of the spiny lobster. J. Neurobiol. 14, 1728.[Medline]
Le Feuvre, Y., Fénelon, V. S. and Meyrand, P. (1999). Central inputs mask multiple adult neural networks within a single embryonic network. Nature 402, 660664.[Medline]
Le Feuvre, Y., Fénelon, V. S., Simmers, J. A. and Meyrand, P. (2000). Characterisation of modulatory inputs involved in the repression of adult-like phenotypes in an embryonic nervous system. Soc. Neurosci. Abstr. 26, 453.
Li, L., Garden, R. W. and Sweedler, J. V. (2000). Single-cell MALDI: a new tool for direct peptide profiling. Trends Biotechnol. 18, 151160.[Medline]
Lingle, C. (1980). The sensitivity of decapod foregut muscles to acetylcholine and glutamate. J. Comp. Physiol. 138, 187199.
Marder, E. (1976). Cholinergic motor neurones in the stomatogastric system of the lobster. J. Physiol., Lond. 257, 6386.[Abstract]
Marder, E. (1987). Neurotransmitters and neuromodulators. In The Crustacean Stomatogastric System (ed. A. I. Selverston and M. Moulins), pp. 263300. Berlin, Heidelberg, New York: Springer Verlag.
Marder, E., Calabrese, R. L., Nusbaum, M. P. and Trimmer, B. (1987). Distribution and partial characterization of FMRFamide-like peptides in the stomatogastric nervous systems of the rock crab, Cancer borealis and the spiny lobster, Panulirus interruptus. J. Comp. Neurol. 259, 150163.[Medline]
Marder, E. and Hooper, S. L. (1985). Neurotransmitter modulation of the stomatogastric ganglion of decapod crustacean. In Model Neural Networks and Behaviour (ed. A. I. Selverston), pp. 319337. New York, London: Plenum Publishing Corporation.
Marder, E., Hooper, S. L. and Siwicki, K. K. (1986). Modulatory action and distribution of the neuropeptide proctolin in the crustacean stomatogastric nervous system. J. Comp. Neurol. 243, 454467.[Medline]
Marder, E., Jorge-Rivera, J. C., Kilman, V. L. and Weimann, J. M. (1997). Peptidergic modulation of synaptic transmission in a rhythmic motor system. Adv. Organ Biol. 2, 213233.
Marder, E. and Richards, K. S. (1999). Development of the peptidergic modulation of a rhythmic pattern generating network. Brain Res. 848, 3544.[Medline]
Marder, E., Skiebe, P. and Christie, A. E. (1994). Multiple modes of network modulation. Verh. Dt. Zool. Ges. 87, 177184.
Marder, E., Swensen, A. M., Blitz, D. M., Christie, A. E. and Nusbaum, M. P. (2001). Convergence and divergence of cotransmitter systems in the crab stomatogastric nervous system. In The Crustacean Nervous System (ed. K. Wiese). Berlin: Springer Verlag (in press).
Marder, E. and Weimann, J. M. (1992). Modulatory control of multiple task processing in the stomatogastric nervous system. In Neurobiology of Motor Program Selection (ed. J. Kien, C. McCrohan and B. Winlow), pp. 319. New York: Pergamon Press.
Maynard, D. M. and Dando, M. R. (1974). The structure of the stomatogastric neuromuscular system in Callinectes sapidus, Homarus americanus and Panulirus argus (Decapoda Crustacea). Phil. Trans. R. Soc. Lond. B 268, 161220.[Medline]
Maynard, E. A. (1971). Electron microscopy of stomatogastric ganglion in the lobster, Homarus americanus. Tissue & Cell 3, 137160.
Mercier, A. J., Orchard, I., TeBrugge, V. and Skerrett, M. (1993). Isolation of 2 FMRFamide-related peptides from crayfish pericardial organs. Peptides 14, 137143.[Medline]
Meyrand, P., Faumont, S., Simmers, J., Christie, A. E. and Nusbaum, M. P. (2000). Species-specific modulation of pattern-generating circuits. Eur. J. Neurosci. 12, 25852596.[Medline]
Meyrand, P. and Marder, E. (1991). Matching neural and muscle oscillators: control by FMRFamide-like peptides. J. Neurosci. 11, 11501161.[Abstract]
Mortin, L. I. and Marder, E. (1991). Differential distribution of ß-pigment dispersing hormone. (ß-PDH)-like immunoreactivity in the stomatogastric nervous system of five species of decapod crustaceans. Cell Tissue Res. 265, 1933.[Medline]
Mulloney, B. and Hall, W. M. (1991). Neurons with histamine-like immunoreactivity in the segmental and stomatogastric nervous system of the crayfish Pacifastacus leniusculus and the lobster Homarus americanus. Cell Tissue Res. 266, 197207.[Medline]
Nagy, F., Cardi, P. and Cournil, I. (1994). A rhythmic modulatory gating system in the stomatogastric nervous system of Homarus gammarus. I. Pyloric-related neurons in the commissural ganglia. J. Neurophysiol. 71, 24772489.
Nässel, D. R. (1993) Neuropeptides in the insect brain: a review. Cell Tissue Res. 273, 129.[Medline]
Nusbaum, M. P., Cournil, I., Golowasch, J. and Marder, E. (1989). Modulating rhythmic motor activity with a dual-transmitter neuron. In Neural Mechansims of Behavior (ed. J. Erber, R. Menzel, H.-J. Pflüger and D. Todt), p. 228. Stuttgart: Georg Thieme Verlag.
Nusbaum, M. P. and Marder, E. (1988). A neuronal role for a crustacean red pigment concentrating hormone-like peptide: neuromodulation of the pyloric rhythm in the crab Cancer borealis. J. Exp. Biol. 135, 165181.
Nusbaum, M. P. and Marder, E. (1989a). A modulatory proctolin-containing neuron (MPN). I. Identification and characterization. J. Neurosci. 9, 15911599.[Abstract]
Nusbaum, M. P. and Marder, E. (1989b). A modulatory proctolin-containing neuron (MPN). II. State-dependent modulation of rhythmic motor activity. J. Neurosci. 9, 16001607.[Abstract]
Orlov, J. (1928). Über den histologischen Bau der Ganglien des Mundmagennervensystems der Crustaceen. Z. Zellforsch. 8, 493541.
Patel, V. and Govind, C. K. (1997). Synaptic exocytosis of dense-core vesicles in the blue crab (Callinectes sapidus) stomach muscles. Cell Tissue Res. 289, 517526.[Medline]
Price, D. A. and Greenberg, M. J. (1977). Purification and characterization of a cardioexcitatory neuropeptide from the central ganglia of a bivalve mollusc. Prep. Biochem. 7, 261281.[Medline]
Richards, K. S. and Marder, E. (2000). The actions of crustacean cardioactive peptide on adult and developing stomatogastric ganglion motor patterns. J. Neurobiol. 44, 3144.[Medline]
Richards, K. S., Miller, W. L. and Marder, E. (1999). Maturation of lobster stomatogastric ganglion rhythmic activity. J. Neurophysiol. 82, 20062009.
Santama, N. and Benjamin, P. R. (2000). Gene expression and function of FMRFamide-related neuropeptides in the snail Lymnaea. Microsc. Res. Tech. 49, 547556.[Medline]
Scholz, N. L., Chang, E. S., Graubard, K. and Truman, J. W. (1998). The NO/cGMP pathway and the development of neural networks in postembryonic lobsters. J. Neurobiol. 34, 208226.[Medline]
Scholz, N. L., Goy, M. F., Truman, J. W. and Graubard, K. (1996). Nitric oxide and peptide neurohormones activate cGMP synthesis in the crab stomatogastric nervous system. J. Neurosci. 16, 16141622.[Abstract]
Schoofs, L., Veelaert, D., Vanden Broeck, J. and De Loof, A. (1997). Peptides in the locusts, Locusta migratoria and Schistocerca gregaria. Peptides 18, 145156.[Medline]
Sigvardt, K. A. and Mulloney, B. (1982). Properties of synapses made by IVN command-interneurones in the stomatogastric ganglion of the spiny lobster Panulirus interruptus. J. Exp. Biol. 97, 153168.[Abstract]
Skiebe, P. (1999). Allatostatin-like immunoreactivity within the stomatogastric nervous system and the pericardial organs of the crab Cancer pagurus, the lobster Homarus americanus and the crayfish Cherax destructor and Procambarus clarkii. J. Comp. Neurol. 403, 85105.[Medline]
Skiebe, P. (2000). A synaptotagmin antibody marks neurohemal release sites in the stomatogastric nervous system (STNS) of a decapod crustacean. Eur. J. Neurosci. 12, 451.
Skiebe, P., Dietel, C. and Schmidt, M. (1999). Immunocytochemical localization of FLRFamide-, proctolin- and CCAP-like peptides in the stomatogastric nervous system and neurohaemal structures of the crayfish, Cherax destructor. J. Comp. Neurol. 414, 511532.[Medline]
Skiebe, P. and Ganeshina, O. (2000). Synaptic neuropil in nerves of the crustacean stomatogastric nervous system: An immunocytochemical and electron microscopical study. J. Comp. Neurol. 420, 373397.[Medline]
Skiebe, P., Johnson, B. R. and Harris-Warrick, R. M. (2000). Allatostatin inhibits the activity of identified neurons within the stomatogastric ganglion of the crayfish Cherax destructor. Soc. Neurosci. Abstr. 26, 1579.
Skiebe, P. and Marder, E. (1994). Allatostatin modulates the pyloric and gastric rhythms of the crab, Cancer borealis. In Göttingen Neurobiology Report 1994 (ed. N. Elsner and H. Breer), p. 678. Stuttgart: Georg Thieme Verlag.
Skiebe, P. and Schneider, H. (1994). Allatostatin peptides in the crab stomatogastric nervous system: Inhibition of the pyloric rhythm and distribution of allatostatin-like immunoreactivity. J. Exp. Biol. 194, 195208.
Starrat, A. N. and Brown, B. E. (1975). Structure of the pentapeptide proctolin, a proposed neurotransmitter in insects. Life Sci. 17, 12531256.[Medline]
Stone, J. V., Mordue, W., Betley, K. E. and Morris, H. R. (1976). Structure of locust adipokinetic hormone, a neurohormone that regulates lipid utilization during flight. Nature 265, 207211.
Strand, F. L. (1999). Neuropeptides: Regulators of Physiological Processes. Cambridge, MA; London, UK: MIT Press.
Swensen, A. M. (2000). Network consequences of convergence modulation in the stomatogastric nervous system of the crab, Cancer borealis. Thesis, Brandeis University, Waltham, Massachusetts, USA.
Swensen, A. M., Golowasch, J., Christie, A. E., Coleman, M. J., Nusbaum, M. P. and Marder, E. (2000). GABA and responses to GABA in the stomatogastric ganglion of the crab Cancer borealis. J. Exp. Biol. 203, 20752092.
Swensen, A. M. and Marder, E. (2000a). Multiple peptides converge to activate the same voltage-dependent current in a central pattern generating circuit. J. Neurosci. 20, 67526759.
Swensen, A. M. and Marder, E. (2000b). Mechanism for differential effects of convergent modulators in the stomatogastric nervous system. Soc. Neurosci. Abstr. 26, 2175.
Tierney, A. J., Blanck, J. and Mercier, J. (1997). FMRFamide-like peptides in the crayfish (Procambarus clarkii) stomatogastric nervous system: distribution and effects on the pyloric motor pattern. J. Exp. Biol. 200, 32213233.
Tierney, A. J., Godleski, M. S. and Rattananont, P. (1999). Serotonin-like immunoreactivity in the stomatogastric nervous systems of crayfishes from four genera. Cell Tissue Res. 295, 537551.[Medline]
Trimmer, B. A., Kobierski, L. A. and Kravitz, E. A. (1987). Purification and characterization of immunoreactive substances from lobster nervous system: Isolation and sequence analysis of two closely related peptides. J. Comp. Neurol. 266, 1626.[Medline]
Turrigiano, G. G. and Selverston, A. I. (1989). Cholecystokinin-like peptide is a modulator of a crustacean central pattern generator. J. Neurosci. 9, 24862501.[Abstract]
Turrigiano, G. G. and Selverston, A. I. (1990). A cholecystokinin-like hormone activates a feeding-related neural circuit in lobster. Nature 344, 866868.[Medline]
Turrigiano, G. G. and Selverston, A. I. (1991). Distribution of cholecystokinin-like immunoreactivity within the stomatogastric nervous systems of four species of decapod Crustacea. J. Comp. Neurol. 305, 164176.[Medline]
Turrigiano, G. G., Van Wormhoudt, A., Ogden, L. and Selverston, A. I. (1994). Partial purification, tissue distribution and modulatory activity of a crustacean cholecystokinin-like peptide. J. Exp. Biol. 187, 181200.
Weimann, J. M., Marder, E., Evans, B. and Calabrese, R. L. (1993). The effects of SDRNFLRFNH2 and TNRNFLRFNH2 on the motor patterns of the stomatogastric ganglion of the crab Cancer borealis. J. Exp. Biol. 181, 126.
Weimann, J. M., Meyrand, P. and Marder, E. (1991). Neurons that form multiple pattern generators: Identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. J. Neurophysiol. 65, 111122.
Weimann, J. M., Skiebe, P., Heinzel, H.-G., Soto, C., Kopell, N., Jorge-Rivera, J. C. and Marder, E. (1997). Modulation of oscillator interactions in the crab stomatogastric ganglion by crustacean cardioactive peptide. J. Neurosci. 17, 17481760.
Weiss, K. R., Brezina, V., Cropper, E. C., Heierhorst, J., Hooper, S. L., Probst, W. C., Rosen, S. C., Vilim, F. S. and Kupfermann, I. (1993). Physiology and biochemistry of peptidergic cotransmission in Aplysia. J. Physiol., Paris 87, 141151.[Medline]
Wood, D. E., Stein, W. and Nusbaum, M. P. (2000). Projection neurons with shared cotransmitters elicit different motor patterns from the same neural circuit. J. Neurosci. 20, 89438953.
Zhang, B. and Harris-Warrick, R. M. (1995). Calcium-dependent plateau potentials in a crab stomatogastric ganglion motor neuron. I. Calcium current and its modulation by serotonin. J. Neurophysiol. 74, 19291937.