The role of the arthropod stomatogastric nervous system in moulting behaviour and ecdysis

Ayali, Amir

doi:10.1242/jeb.023879

Cited by 27 publications

(13 citation statements)

References 46 publications

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“…Among arthropods, much is known about SNS development in insects [80], and the crustacean SNS is a leading model in the study of peripheral neuronal circuits and their control over rhythmic behaviors [81]. In the lobster foregut, for example, separate stomatogastric circuits control gastric chewing, pyloric peristalsis, and water swallowing (to increase internal body pressure for ecdysis) [82]. The foreguts of errant polychaetes also exhibit multiple behaviors.…”

Section: Resultsmentioning

confidence: 99%

Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae)

2010

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BackgroundMembers of Family Nereididae have complex neural morphology exemplary of errant polychaetes and are leading research models in the investigation of annelid nervous systems. However, few studies focus on the development of their nervous system morphology. Such data are particularly relevant today, as nereidids are the subjects of a growing body of "evo-devo" work concerning bilaterian nervous systems, and detailed knowledge of their developing neuroanatomy facilitates the interpretation of gene expression analyses. In addition, new data are needed to resolve discrepancies between classic studies of nereidid neuroanatomy. We present a neuroanatomical overview based on acetylated α-tubulin labeling and confocal microscopy for post-embryonic stages of Neanthes arenaceodentata, a direct-developing nereidid.ResultsAt hatching (2-3 chaetigers), the nervous system has developed much of the complexity of the adult (large brain, circumesophageal connectives, nerve cords, segmental nerves), and the stomatogastric nervous system is partially formed. By the 5-chaetiger stage, the cephalic appendages and anal cirri are well innervated and have clear connections to the central nervous system. Within one week of hatching (9-chaetigers), cephalic sensory structures (e.g., nuchal organs, Langdon's organs) and brain substructures (e.g., corpora pedunculata, stomatogastric ganglia) are clearly differentiated. Additionally, the segmental-nerve architecture (including interconnections) matches descriptions of other, adult nereidids, and the pharynx has developed longitudinal nerves, nerve rings, and ganglia. All central roots of the stomatogastric nervous system are distinguishable in 12-chaetiger juveniles. Evidence was also found for two previously undescribed peripheral nerve interconnections and aspects of parapodial muscle innervation.ConclusionsN. arenaceodentata has apparently lost all essential trochophore characteristics typical of nereidids. Relative to the polychaete Capitella, brain separation from a distinct epidermis occurs later in N. arenaceodentata, indicating different mechanisms of prostomial development. Our observations of parapodial innervation and the absence of lateral nerves in N. arenaceodentata are similar to a 19th century study of Alitta virens (formerly Nereis/Neanthes virens) but contrast with a more recent study that describes a single parapodial nerve pattern and lateral nerve presence in A. virens and two other genera. The latter study apparently does not account for among-nereidid variation in these major neural features.

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Section: Resultsmentioning

confidence: 99%

Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae)

2010

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“…Synthesis of new cuticle ensues, and when complete, the molt is terminated on ecdysis of the old cuticle. A recent review compares the neuroendocrine control of ecdysis in insects and crustaceans (Ayali 2009). …”

Section: Neuropeptide Regulation Of Insect Ecdysismentioning

confidence: 99%

Neuropeptide Action in Insects and Crustaceans

Mykles

Adams²,

GÄde³

et al. 2010

Physiological and Biochemical Zoology

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Physiological processes are regulated by a diverse array of neuropeptides that coordinate organ systems. The neuropeptides, many of which act through G protein–coupled receptors, affect the levels of cyclic nucleotides (cAMP and cGMP) and Ca2+ in target tissues. In this perspective, their roles in molting, osmoregulation, metabolite utilization, and cardiovascular function are highlighted. In decapod crustaceans, inhibitory neuropeptides (molt-inihibiting hormone and crustacean hyperglycemic hormone) suppress the molting gland through cAMP- and cGMP-mediated signaling. In insects, the complex movements during ecdysis are controlled by ecdysis-triggering hormone and a cascade of downstream neuropeptides. Adipokinetic/hypertrehalosemic/hyperprolinemic hormones mobilize energy stores in response to increased locomotory activity. Crustacean cardioacceleratory (cardioactive) peptide, proctolin, and FMRFamide-related peptides act on the heart, accessory pulsatile organs, and excurrent ostia to control hemolymph distribution to tissues. The osmoregulatory challenge of blood gorging in Rhodnius prolixus requires the coordinated release of serotonin and diuretic and antidiuretic hormones acting on the midgut and Malpighian tubules. These studies illustrate how multiple neuropeptides allow for flexibility in response to physiological challenges.

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“…Locust foregut movements are responsible for passing food particles from the pharynx to the crop, and also for pumping air to inflate the alimentary canal at early stages of the molt (Hughes, 1980; Ayali, 2004, 2009; Zilberstein et al, 2006). Although the gut has some intrinsic contractile capabilities (Oldfield and Huddart, 1982; Banner et al, 1987), foregut movements are under the control of the stomatogastric nervous system (STNS), which is comprised of a small set of peripheral ganglia (Figure 1): the frontal ganglion (FG), the hypocerebral ganglion (HG), and the paired ingluvial ganglia (IG; Chapman, 1998).…”

Section: Introductionmentioning

confidence: 99%

The Effect of Octopamine on the Locust Stomatogastric Nervous System

Rand¹,

Knebel²,

Ayali³

2012

Front. Physio.

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Octopamine (OA) is a prominent neuromodulator of invertebrate nervous systems, influencing multiple physiological processes. Among its many roles in insects are the initiation and maintenance of various rhythmic behaviors. Here, the neuromodulatory effects of OA on the components of the locust stomatogastric nervous system were studied, and one putative source of OA modulation of the system was identified. Bath application of OA was found to abolish the endogenous rhythmic output of the fully isolated frontal ganglion (FG), while stimulating motor activity of the fully isolated hypocerebral ganglion (HG). OA also induced rhythmic movements in a foregut preparation with intact HG innervation. Complex dose-dependent effects of OA on interconnected FG-HG preparations were seen: 10−5 M OA accelerated the rhythmic activity of both the HG and FG in a synchronized manner, while 10−4 M OA decreased both rhythms. Intracellular stimulation of an identified octopaminergic dorsal unpaired median neuron in the subesophageal ganglion was found to exert a similar effect on the FG motor output as that of OA application. Our findings suggest a mechanism of regulation of insect gut patterns and feeding-related behavior during stress and times of high energy demand.

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The role of the arthropod stomatogastric nervous system in moulting behaviour and ecdysis

Cited by 27 publications

References 46 publications

Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae)

Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae)

Neuropeptide Action in Insects and Crustaceans

The Effect of Octopamine on the Locust Stomatogastric Nervous System

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