How to innervate a simple gut: Familiar themes and unique aspects in the formation of the insect enteric nervous system

Abstract

Like the vertebrate enteric nervous system (ENS), the insect ENS consists of interconnected ganglia and nerve plexuses that control gut motility. However, the insect ENS lies superficially on the gut musculature, and its component cells can be individually imaged and manipulated within cultured embryos. Enteric neurons and glial precursors arise via epithelial-to-mesenchymal transitions that resemble the generation of neural crest cells and sensory placodes in vertebrates; most cells then migrate extensive distances before differentiating. A balance of proneural and neurogenic genes regulates the morphogenetic programs that produce distinct structures within the insect ENS. In vivo studies have also begun to decipher the mechanisms by which enteric neurons integrate multiple guidance cues to select their pathways. Despite important differences between the ENS of vertebrates and invertebrates, common features in their programs of neurogenesis, migration, and differentiation suggest that these relatively simple preparations may provide insights into similar developmental processes in more complex systems. Developmental Dynamics 236:1841-1864, 2007.

The Digestive Tract of Drosophila melanogaster

“…The adult digestive tract receives innervation from three sources (Figure 3c,d): (a) the stomatogastric nervous system (SNS) (39,78,168); (b) the corpus cardiacum, a neurosecretory structure that, in adult flies, is fused with one of the stomatogastric ganglia (the hypocerebral ganglion) (99); and (c) neurons located in the central nervous system (CNS), which extend their axons toward three sections of the digestive tract (37,115,116,179).…”

Peptidergic control of food intake and digestion in insects1This review is part of a virtual symposium on recent advances in understanding a variety of complex regulatory processes in insect physiology and endocrinology, including development, metabolism, cold hardiness, food intake and digestion, and diuresis, through the use of omics technologies in the postgenomic era.

“…In the migratory locust (Locusta migratoria (L., 1758)), neurons from within the CNS project via the frontal connectives towards the SNS, indicating complex innervation of the gut and interactions between CNS and SNS (Bräunig 2008). The hindgut is innervated by proctodeal and rectal nerves originating from the terminal abdominal ganglia of the CNS (Copenhaver 2007). The suboesophageal ganglion (SOG) is situated below the brain and oesophagus.…”

Regulation of enteric neuron migration by the gaseous messenger molecules CO and NO

“…However, despite the common developmental origin from neuroepithelial parts of the foregut, enteric nervous systems of insects exhibit extensive variations in the detailed pattern of cell migration and underlying molecular guidance cues (Hartenstein, 1997;Ganfornina et al, 1996;Copenhaver, 2007). For example, whereas in Manduca specific sets of visceral muscle bands support migration of the enteric neurons on the midgut (Copenhaver and Taghert, 1989;Copenhaver et al, 1996;Wright et al, 1999) no morphologically distinct muscle bands can be recognized along the migratory pathways in the grasshopper embryo (Ganfornina et al, 1996).…”

“…Neuronal precursors emerge from proliferative zones in the foregut epithelium and perform extensive cell migrations before they assemble into discrete peripheral ganglia and gastric nerve plexus. The genetic and cellular bases of neuronal specification, guidance cues for directed cell migration, and differentiation towards neuronal phenotypes have been particularly well investigated in the two holometabolous insects Drosophila and Manduca (Hartenstein, 1997;Copenhaver, 2007). In the hemimetabolous grasshopper Schistocerca, the enteric midgut neurons of the grasshopper embryo migrate posteriorly from caudal pockets of the ingluvial ganglia towards the foregut-midgut boundary of the embryo (Ganfornina et al, 1996).…”