© 2001 by The Society for Integrative and Comparative Biology
NO/cGMP Signaling and the Flexible Organization of Motor Behavior in Crustaceans1
1 University of Washington, Department of Zoology, Seattle, Washington 98195-1800
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The basic elements of the NO/cGMP signaling pathway have been identified in the nervous systems of animals from nearly all of the major phyla. In crustaceans, the NO/cGMP pathway is associated with certain fundamental neuronal processes, including sensory integration and the organization and production of motor behavior. Here I review the evidence for NO synthesis and action in crustacean neural networks, with an emphasis on the rhythmic motor circuits of the crab stomatogastric ganglion (STG). In the STG, NO appears to be released as an orthograde transmitter from descending projection neurons. NO's receptor, a cytopasmic isoform of guanylate cyclase (sGC), is expressed in a subset of the cells that participate in the gastric mill and pyloric central pattern generating networks. In spontaneously-active, in vitro preparations of the STG, pharmacological inhibitors of the NO/cGMP pathway cause the two rhythmic motor patterns to collapse into a single conjoint rhythm. Parallel motor output is restored when the ganglion is returned to normal saline. Although precise mechanisms have yet to be determined, these data suggest that NO and cGMP play an important role in the functional organization of STG networks. The STG, as well as other crustacean models, provides a promising context for studying the physiological and behavioral aspects of NO-mediated signaling in the nervous system.
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INTRODUCTION |
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Nitric oxide (NO) is a versatile and evolutionarily ancient (Colasanti et al., 1997
) neuronal messenger. Although NO-mediated signaling has been extensively studied in the mammalian nervous system, much of what we know about NO's diverse functions in the brain has also come from research on invertebrate model systems (reviewed by Jacklet, 1997; Muller, 1997; Bicker, 1998; Scholz and Truman, 2000). In the short time since NO was discovered in molluscs (Elofsson et al., 1993; Gelperin, 1994) and arthropods (Elphick et al., 1993; Johansson and Carlberg, 1994), there has been a rapid increase in the number of studies investigating NO-mediated signaling in animals from nearly all of the major invertebrate phyla (Jacklet, 1997). These parallel studies have implicated NO in several important processes, including neural development (Lin and Leise, 1996; Truman et al., 1996; Gibbs and Truman, 1998), olfaction (Gelperin, 1994; Muller and Bicker, 1994), vision (Elphick et al., 1996), motor control (Moroz et al., 1993; Elphick et al. 1995), network plasticity (Scholz et al., 2001), and learning and memory (Robertson et al., 1994; Muller, 1996).
This review will highlight recent NO research in decapod crustaceans, with an emphasis on the stomatogastric ganglion (STG) and NO's role in the specification of rhythmic motor networks. Stomatogastric circuits have been intensively studied for more than 30 years (Maynard, 1972), providing a great deal of insight into the neurophysiological mechanisms that give rise to patterned motor behavior (Harris-Warrick et al., 1992a). Neural network plasticity, or the process by which functional circuits can be reconfigured to meet the changing behavioral needs of the animal, is a hallmark of this system (Dickinson, 1995). Neuromodulators play an important role in this process by evoking changes in the cellular and synaptic properties of stomatogastric neurons. These changes, in turn, can lead to subtle modifications of an active rhythm or wholesale shifts in motor production. The stomatogastric nervous system thus provides an excellent context for investigating potential neuromodulatory functions for NO and cGMP in well-defined, flexible neural circuits.
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EVIDENCE FOR A CRUSTACEAN NOS |
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The enzyme nitric oxide synthase (NOS) produces NO stoichiometrically from the conversion of L-arginine to L-citrulline. In crustaceans, a NOS was first characterized in the brain of the crayfish Pacifastacus leniusculus (Johansson and Carlberg, 1994
). Similar to constitutively-expressed isoforms in other species, crayfish NOS is calcium/calmodulin-dependent and its activity is sensitive to conventional inhibitors (Johansson and Carlberg, 1994; Lee et al., 2000). NADPH-diaphorase histochemistry, which labels putative NOS-containing neurons in many different species (Jacklet, 1997), provides evidence that NO-producing neurons are predominantly associated with the integration of chemosensory information in the brain. In P. leniusculus, diaphorase staining is present in olfactory receptor neurons (Johansson and Carlberg, 1994; Johansson et al., 1996) as well as the olfactory midbrain (Johansson and Carlberg, 1994; Johansson and Mellon, 1998). Similar patterns of diaphorase staining have been observed in the brain of another crayfish, Cambarellus montezumae (Talavera et al., 1995).
The quality of NADPH-diaphorase staining in the crustacean nervous system is relatively poor when compared to insects and molluscs. For example, the diaphorase technique labels numerous neurons in ventral ganglia of developing hawkmoth (Manduca sexta) larvae (Zayas et al., 2000). However, it does not label cells in the nervous systems of pre-metamorphic lobsters (Homarus americanus) (Scholz et al., 1998). This is the case even when Manduca and Homarus nerve cords are processed for NADPH-diaphorase histochemistry together (N. L. Scholz, unpublished observations). The reason for this is not clear, but it may reflect an unusual sensitivity of crustacean NOS isoforms to paraformaldehyde or glutaraldehyde fixation (e.g., Matsumoto et al., 1993). In any case, the absence of reliable NADPH-d staining in many parts of the nervous system has made the identification of NO-releasing neurons in crustaceans somewhat more difficult than in other invertebrate models.
Recent evidence from immunoblotting experiments suggests that the crustacean nervous system may contain more than one NOS. Western blots probed with a universal NOS (uNOS) antibody, which detects Drosophila NOS (Gibbs and Truman, 1998), reveal two NOS-like proteins (
155 and 135 kD) in extracts from the brain and stomatogastric nervous system of the crab Cancer productus (Scholz et al., 2001). In addition, a 138 kD NOS-immunoreactive protein has been identified in the eyestalk ganglia and sinus gland of the crayfish P. clarkii (Lee et al., 2000).
In wholemount preparations of the developing lobster nervous system, the uNOS antibody labels several cells in the brain and ventral nerve cord (Scholz et al., 1998). NOS-immunoreactivity is especially prominent in two pairs of large interneurons in the brain. These cells, which project to the olfactory neuropil in the deutocerebrum, appear to be the same neurons that are NADPH-diaphorase positive in the crayfish midbrain (Johansson and Mellon, 1998).
Putative NO-producing neurons have also been visualized using citrulline immunocytochemistry. Both citrulline and NO are produced stoichiometrically from L-arginine, and in mammals citrulline accumulation in neurons has been shown to faithfully reflect NOS activity (Eliasson et al., 1997). In the crab stomatogastric nervous system, citrulline is present in a pair of projection neurons that send axons to the synaptic neuropil of the STG (Fig. 1; Scholz et al., 2001). Citrulline immunoreactivity is restricted to the distal axons and terminals of these neurons, which may reflect a targeting of the active NOS enzyme. By contrast, the somata of the projection neurons do not label with the citrulline antibody. This has made it difficult to identify the location of these cells in anterior ganglia.
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In summary, several independent lines of evidence have shown that one or more NOS enzymes are expressed in the crustacean nervous system. However, it has been difficult to identify individual NO-releasing neurons via NADPH-diaphorase histochemistry or NOS immunocytochemistry. Future studies would therefore benefit from a molecular characterization of the crustacean NOS gene(s), as accomplished in other invertebrates such as Lymnaea (Korneev et al., 1998
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PATTERNS OF SGC EXPRESSION IN CRUSTACEAN NEURONS |
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Soluble guanylate cyclase (sGC) is an important receptor for NO in the nervous system (Denninger and Marletta, 1999
). Among crustaceans, a biochemical characterization of sGC enzymes in the lobster H. americanus has shown that two different cytoplasmic forms are enriched in the nervous system (Prabhakar et al., 1997). The first form is activated by NO and resembles NO-sensitive sGC in the mammalian nervous system. The second form is NO-insensitive, and may be a homolog of the MsGC-ß3 cyclase that was recently identified in the moth Manduca sexta (Nighorn et al., 1999). A function for the latter enzyme has not yet been determined.
Identifying which neurons in the brain express an NO-sensitive sGC (and are therefore possible targets for endogenous NO) has been an important step in deciphering functional roles for NO/cGMP signaling. Cyclic GMP immunocytochemistry (de Vente et al., 1987) has been used extensively to this end. When the nervous system is exposed to NO-releasing compounds (e.g., sodium nitroprusside), sGC activation leads to an accumulation of intracellular cGMP in NO-sensitive cells. These increases are detectable by cGMP immunocytochemistry, and this technique has been used as an indirect marker for visualizing sGC-expressing neurons in a diversity of animals, including mammals (Southam and Garthwaite, 1993), insects (Truman et al., 1996), and molluscs (Koh and Jacklet, 1999). In lobsters, NO-sensitive neurons have been mapped throughout the brain and ventral nerve cord (Prabhakar et al., 1997; Scholz et al., 1998). In crabs, NO-responsive cells have been found in the STG (Scholz et al., 1996, 2001).
The distribution and functional significance of sGC enzyme activity has been explored most extensively in the stomatogastric networks of C. productus. Nitric oxide donors stimulate a 10 to 20-fold increase in cGMP when applied to in vitro preparations of the stomatogastric nervous system (Fig. 2; Scholz et al., 1996). As revealed by cGMP immunocytochemistry, these increases arise from the activation of sGC in neurons from the commissural, oesophageal, and stomatogastric ganglia. However, the STG contains the largest proportion of NO-sensitive cells. As shown in Figure 3, approximately 13 of the 30 cells in the ganglion show consistent NO-induced cGMP immunoreactivity (Scholz et al., 1996, 2001). Importantly, cGMP synthesis is blocked by pretreatment with 1H-(1,2,4)oxadiazolo(4,3-a)-quinoxalin-1-one (ODQ), a selective inhibitor of NO-sensitive sGC enzymes (Garthwaite et al., 1995). The STG therefore contains a substantial complement of NO-sensitive, sGC-expressing neurons. These cells may be targets for NO produced by descending projection neurons (Fig. 1).
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NO/CGMP SIGNALING CONTRIBUTES TO NETWORK PARTITIONING AND NEURONAL SWITCHING IN THE STG |
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This section will focus on neuromodulatory functions for NO and cGMP in the crustacean STG, beginning with a brief overview of gastric mill and pyloric motor pattern production. See Harris-Warrick et al. (1992a)
for a more extensive review of stomatogastric circuits and Marder and Calabrese (1996) for a review of mechanisms of pattern generation in oscillatory neural networks.
In decapod crustaceans, motor output from the stomatogastric nervous system drives the rhythmic movements of the esophagus, cardiac sac, gastric mill, and pyloric regions of the animal's foregut (Selverston et al., 1976). The networks which underlie these four basic rhythms are distributed throughout the paired commissural ganglia, the oesophageal ganglion, and the STG (schematic diagram in Fig. 4). Much of the previous work in this system has focused on the STG, which contains 30 neurons and all of the cells that produce the gastric mill and pyloric motor behaviors. These two oscillatory networks serve different functions in the intact animal. Whereas gastric mill neurons drive the rhythmic grinding movements of the medial and paired lateral teeth that make up the gastric mill, pyloric neurons direct the filtering movements of the pyloric chamber. However, food moves back and forth between these two regions of the foregut and there is considerable interaction between the two underlying motor circuits (e.g., Heinzel et al., 1993).
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When the stomatogastric nervous system is isolated in vitro, the STG continues to generate both motor rhythms. This fictive motor production depends critically on the ongoing release of modulatory neurotransmitters from projection neurons that have somata located in anterior ganglia. When these descending inputs are blocked, gastric mill and pyloric activity in the ganglion is significantly reduced or abolished (Russel, 1979
). Therefore, neuromodulation plays an essential role in the production and modification of both motor rhythms. There are at least 19 different transmitters, amines, and peptides present in inputs to the ganglion (Harris-Warrick et al., 1992b) and it is beyond the scope of this review to survey the array of physiological effects these agents exert on stomatogastric networks (see reviews by Harris-Warrick et al., 1992b; Nusbaum, 1994; Harris-Warrick et al., 1997). However, it is important to emphasize that previous work in crabs (Cancer sp.) has shown that many stomatogastric neurons are multifunctional. That is, they are conditional elements of both the gastric mill and pyloric motor networks, and can switch back and forth between the two. This is the case for spontaneous activity in in vitro preparations (Weimann et al., 1991) as well as in the intact animal (Heinzel et al., 1993). Moreover, neuromodulatory inputs can trigger pattern-switching in stomatogastric neurons (e.g., Weimann et al., 1993).
The role of NO/cGMP signaling in the STG has been investigated in in vitro preparations from the crab, C. productus. As shown in Figure 4, the isolated STG spontaneously generates a robust gastric mill and pyloric motor pattern. Gastric neurons (e.g., DG and GM) fire protracted bursts of action potentials that last for several seconds and cycle with a period that lasts from 5–20 sec. By comparison, the 1 Hz cycle frequency of the pyloric network (e.g., the PD neurons) is more rapid.
The presence of citrulline immunoreactivity in descending inputs (Fig. 1) suggests that these projection neurons may be a source of NO which, when released into the synaptic neuropil of the STG, could lead to sGC activation and cGMP accumulation in the 13 NO-responsive neurons in the ganglion (Fig. 3A). Surprisingly, enhancing intrinsic NO/cGMP signaling with NO donors [sodium nitroprusside (SNP), 3-morpholinosydnonimine (SIN-1), or S-nitroso-N-acetylpenicillamine (SNAP)] or 8-bromo-cGMP has little effect on the basic structure of the gastric mill or pyloric motor pattern (Scholz et al., 2001). By contrast, inhibitors of the NO/cGMP pathway evoke rapid changes in the functional organization of both networks. More specifically, inhibitors of NO diffusion (250 µM PTIO) or sGC activation (50 µM ODQ) trigger a collapse of the two separate rhythms into a conjoint motor pattern. In the absence of NO/cGMP signaling, the gastric mill network (as monitored by the medial tooth subsystem) is dismantled and all active neurons fire in pyloric time. The time course for ODQ-evoked changes in the two motor rhythms is shown in Figure 5A. Within seconds of application, ODQ begins to excite the pyloric rhythm (as revealed by the activity of the PD neurons). As the DG burst shortens and eventually falls silent, the GM neurons, which were previously active in gastric time, pattern-switch and begin firing in phase with the pyloric rhythm. Intracellular recordings from a GM neuron and a pyloric cell (PY) demonstrate ODQ-induced pattern-switching more clearly and are shown in Figure 5B. Strikingly, alternating PTIO or ODQ treatments with normal saline serves to shift the spontaneously active preparation back and forth between unitary and binary network configurations.
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It is not clear why supplementing the NO/cGMP pathway with NO donors or 8-bromo-cGMP has little effect on motor output from the STG. NO donors only stimulate cGMP accumulation in the ganglion if endogenous phosphodiesterase (PDE) activity is blocked (Scholz et al., 1996
). Consequently, in the intact system, cGMP hydrolysis by PDEs may prevent a substantial increase in intracellular cGMP in response to an excess of NO. With respect to 8-bromo-cGMP, the membrane-permeant analog has a low affinity for cGMP-dependent PDEs (Lincoln and Cornwell, 1993). It is possible that 8-bromo-cGMP has no effect on stomatogastic networks because endogenous cGMP normally acts via these effector proteins.
Collectively, these data show that NO/cGMP signaling is involved in the functional specification of stomatogastric networks. As in certain molluscan networks (Jacklet, 1995; Park et al., 1998), NO appears to act as an orthograde transmitter. In addition, sGC activity appears to be particularly important for the spontaneous production of the gastric mill motor rhythm. It is important to emphasize, however, that NO research in the STG is at an early stage. The modulatory effects of NO/cGMP signaling on the full range of gastric mill and pyloric motor patterns has not been determined, and effects of the pathway on interactions between the pyloric and gastric mill networks (Bartos et al., 1999) has yet to be investigated. It is also not clear if NO is released alone or as a cotransmitter, perhaps by one of the many modulatory projection neurons that have been previously identified in this system (e.g., Nusbaum and Marder, 1989; Coleman and Nusbaum, 1994; Norris et al., 1996). Despite these qualifications, the STG is a promising model system for deciphering the cellular and synaptic mechanisms involved in NO-mediated neuromodulation and network plasticity.
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CGMP AND THE DEVELOPMENTAL MATURATION OF PATTERN-GENERATING NETWORKS |
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Neural development and the ontogeny of neuromodulatory pathways have been studied extensively in clawed lobsters belonging to the genus Homarus (Beltz et al., 1992
). For example, the spatial and temporal expression of NOS-like proteins and sGC have been mapped in larval and early postlarval stages of H. americanus (Scholz et al., 1998). The development of adult-specific motor networks in the lobster stomatogastric nervous system has recently become the focus of considerable attention (Casasnovas and Meyrand, 1995; Scholz et al., 1998; Fenelon et al., 1998a, 1999; Le Feuvre et al., 1999; Kilman et al., 1999). This section will briefly review these studies, which highlight potential roles for NO and other neuromodulators in the developmental tuning and long-term maintenance of adult motor circuits (Fenelon et al., 1998b).
In clawed lobsters (Homarus sp.), embryos develop while the eggs are attached to the ventral surface of the mother's abdomen (Herrick, 1895). Hatching larvae are released into the water column, and they spend three developmental stages (instars) as zooplankton (stages I–III). At the end of larval development they undergo metamorphosis and begin a transitional settlement to the seafloor (stages IV and V). As lobsters metamorphose from a planktonic larvae to a benthic juvenile they undergo significant changes in their feeding structures, digestive system, and feeding ecology (Factor, 1981). For example, newly hatched larvae lack a gastric mill. The foregut first appears in embryos as a stomodeum, and this simple structure persists throughout larval development (Casasnovas and Meyrand, 1995). The foregut begins to mature at metamorphosis (stages III–IV). The most prominent structural change is the appearance of the medial tooth of the gastric mill at stage III and the lateral teeth at stage IV (Factor, 1981; Casasnovas and Meyrand, 1995). Therefore, the gastric mill first becomes operational at some point during early juvenile development.
Direct recordings from the lobster stomatogastric nervous system indicate that adult-specific motor patterns also appear relatively late in development (Casasnovas and Meyrand, 1995). Beginning at metamorphosis (stage IV), the gastric mill and pyloric motor patterns begin to differentiate from a unique embryonic/larval network in the STG. This process takes place gradually over several postlarval instars. Consequently, there is a close temporal association between the extrusion of the teeth of the gastric mill at metamorphosis and the appearance of spontaneous gastric mill motor patterns in the ganglion.
Interestingly, stomatogastric neurons begin to express an NO-sensitive sGC in parallel with the ontogeny of adult motor networks (Scholz et al., 1998). There are no NO-sensitive neurons in the lobster STG at hatching (Fig. 6). However, a single cell becomes NO-sensitive when the medial tooth of the gastric mill appears at stage III. As the lateral teeth appear and the gastric mill rhythm begins to form (Casasnovas and Meyrand, 1995), additional neurons become NO-responsive. The close relationship between gastric mill formation, network reorganization in the STG, and the stage-specific expression of sGC among stomatogastric neurons is illustrated in Figure 7.
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The developmental appearance of an active sGC in the STG suggests that the NO/cGMP pathway may somehow be involved in the gradual maturation of adult-specific motor behaviors in this system. However, the underlying mechanism has yet to be established. It is interesting to note that several other modulatory pathways are also expressed in the stages that lead up to metamorphosis (Fenelon et al., 1999
; Kilman et al., 1999). As the ganglion develops, NO and other inputs may tune the active properties of the networks, thereby extending the range and complexity of the motor behaviors produced by this system. |
CONCLUSIONS |
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Invertebrate models continue to make important contributions to our general understanding of NO-mediated signaling in the nervous system. In crustaceans, components of the NO/cGMP pathway have been identified in neural networks that underlie olfaction (Johansson et al., 1996
; Scholz et al., 1998; Johansson and Mellon, 1998), vision (Lee et al., 2000), rhythmic motor behaviors (Scholz et al., 1996, 2001), escape behavior (Aonuma et al., 2000), and neurosecretion (Lee et al., 2000). Crustacean motor circuits, including the stomatogastric nervous system, the cardiac ganglion, and the abdominal neurons involved in escape reflexes, have been studied extensively for several decades. These systems in particular should provide considerable insight into NO's mechanism(s) of action. For example, future studies in the STG might consider 1) the effects of NO and cGMP on the physiological and synaptic properties of identified, sGC-expressing neurons; 2) the modulatory effects of NO on the full range of motor patterns produced by the ganglion; 3) potential interactions between the NO/cGMP pathway and other transmitter and neurohormonal inputs (Harris-Warrick et al., 1992b); 4) the extent to which NO/cGMP signaling underlies circuit interactions in intact, freely-behaving animals (e.g., Clemens et al., 1998); and 5) sGC's role in the development and maturation of adult-specific motor behaviors. The other crustacean networks identified in this review should be amenable to similar, integrative analyses of NO-mediated neuromodulation.
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ACKNOWLEDGMENTS |
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I am grateful for the support of Kathy Graubard and James W. Truman, who together advised my graduate research in the Department of Zoology at the University of Washington. I am also indebted to Michael Goy and Ernest Chang for guiding my work on cGMP biochemistry and lobster developmental biology, respectively. This research would not have been possible without Jan de Vente's generous gift of the cGMP antibody. James Baker, Dave Baldwin, Steve Gammie, Sarah Gibbs, Wes Grueber, and Laura Hurley provided critical input on various aspects of my research. Finally, Jana Labenia reviewed the manuscript and provided invaluable technical assistance throughout most of this work. Supported by a NIH predoctoral traineeship and NIH grants NS15697 to KG and NS13079 to JWT.
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FOOTNOTES |
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1 From the Symposium Nitric Oxide in the Invertebrates: Comparative Physiology and Diverse Functions presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia.
2 E-mail: Nathaniel.Scholz{at}noaa.gov
3 Present address: Northwest Fisheries Science Center, 2725 Montlake Blvd. E., Seattle, WA 98112
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