Embryonic differentiation of serotonin‐containing neurons in the enteric nervous system of the locust (Locusta migratoria)

Abstract

The enteric nervous system (ENS) of the locust consists of four ganglia (frontal and hypocerebral ganglion, and the paired ingluvial ganglia) located on the foregut, and nerve plexus innervating fore- and midgut. One of the major neurotransmitters of the ENS, serotonin, is known to play a vital role in gut motility and feeding. We followed the anatomy of the serotonergic system throughout embryonic development. Serotonergic neurons are generated in the anterior neurogenic zones of the foregut and migrate rostrally along the developing recurrent nerve to contribute to the frontal ganglion. They grow descending neurites, which arborize in all enteric ganglia and both nerve plexus. On the midgut, the neurites closely follow the leading migrating midgut neurons. The onset of serotonin synthesis occurs around halfway through development-the time of the beginning of midgut closure. Cells developing to serotonergic phenotype express the serotonin uptake transporter (SERT) significantly earlier, beginning at 40% of development. The neurons begin SERT expression during migration along the recurrent nerve, indicating that they are committed to a serotonergic phenotype before reaching their final destination. After completion of the layout of the enteric ganglia (at 60%) a maturational phase follows, during which serotonin-immunoreactive cell bodies increase in size and the fine arborizations in the nerve plexus develop varicosities, putative sites of serotonin release (at 80%). This study provides the initial step for future investigation of potential morphoregulatory functions of serotonin during ENS development.

Nitric oxide regulates axonal regeneration in an insect embryonic CNS

“…At this stage, serotonergic neurons do not yet synthesize serotonin, but can be made visible by preincubation of ganglia with 5 lM serotonin before fixation a few hours after birth (Condron, 1999). This is caused by the expression of the serotonin reuptake transporter (SERT) before onset of serotonin synthesis, a feature that is observed for serotonergic neurons in the CNS of the locust (Condron, 1999) and Drosophila (Couch et al, 2004) and the enteric nervous system of the locust (Stern et al, 2007). At 45% development, three neurons stain for serotonin uptake in each hemiganglion in abdominal and thoracic segments after their primary neurite has crossed the midline through the posterior commissure [ Fig.…”

Patterns of dye coupling involving serotonergic neurons provide insights into the cellular organization of a central complex lineage of the embryonic grasshopper Schistocerca gregaria

“…This may have a functional significance in that sensory information (e.g., polarized vision, visual pattern recognition) enters the central complex first via the tangential system and is then passed on to the columnar system for premotor processing (Träger et al 2008). Developing neuronal networks are often active prior to the appearance of the adult behaviors (e.g., flight in the grasshopper; Stevenson and Kutsch 1986), and since serotonin is thought to influence processes such as neurogenesis, apoptosis, and axogenesis (Condron 1999;Richards et al 2003;Sykes and Condron 2005;Stern et al 2007;Filla et al 2008), it may contribute to the development and maturation of the neural circuitry involved.…”

“…In the periphery, it plays a role in the control of both skeletal and visceral muscle contraction (see Roeder 2002). Developmentally, serotonin has been considered to function as a general coordinator of biochemical differentiation and neuronal function (Gaspar et al 2003;Vitalis et al 2007), and is thought to influence developmental processes such as neurogenesis, axogenesis, and cellular differentiation (Condron 1999;Richards et al 2003;Sykes and Condron 2005;Stern et al 2007).…”

NO als Regulator neuronaler Motilität und Regeneration in einfachen Nervensystemen

“…Neben den wandernden Neuronen wird der Mitteldarmplexus auch von zusätzlichen Neuriten innerviert, die am Vorderdarm positionierten kleinen Ganglienknoten des enterischen Nervensystems entspringen und größtenteils durch Serotonin-Immunzytochemie darstellbar sind (Stern et al 2007). Das Neuritenwachtum dieser Neuronenpopulation folgt unmit-…”

“…Dadurch konnten wir die Frage entscheiden, ob sich eine Blockade der NO-Synthese auch auf die Entwicklung von Neuronen auswirkt, die keine unmittelbaren Zielzellen der NO/cGMP-Kaskade sind. Wird die Wanderung der Mitteldarmzellen pharmakologisch mit 7NI gehemmt, so wird auch das Auswachsen der serotonergen Fasern verzögert (Stern et al 2007). Damit ist gezeigt, dass Entwicklungsdefekte, die durch eine Störung der NO-Synthese bedingt sind, auch auf andere Zellen außerhalb der NO/ cGMP-Signalkaskade übersprechen.…”