Development and distribution of serotonin in the central nervous system of Manduca sexta during embryogenesis I. The brain and frontal ganglion

Abstract

Development of the serotonergic system in the brain and frontal ganglion of the Manduca embryo between 35 and 100% of development was studied immunocytochemically with an antiserum to serotonin (5-HT). Serotonin immunoreactivity was initially detectable at 40-45% development in short fibers in the head region, prior to differentiation of the brain. Immunoreactive cell bodies were first seen in the brain at 60% development, located in the protocerebrum and tritocerebrum. Thick fiber tracts crossing the midline (commissures) could also be observed at this early stage. As development of the embryo progressed, eight immunoreactive cell groups, containing a total of about 38-40 cells, and four commissures with terminal arborizations appeared successively in the brain. From 75 to 100% development, no obvious changes occurred in the number or distribution of cells, and the brain exhibited the same pattern of 5-HT immunoreactive cells, fiber tracts and arborizations as in last instar larvae of Manduca. However, an increase in the size of the cells in both the brain and frontal ganglion was noted between 75 and 80% development, followed by a decrease by 100% development. The frontal ganglion was found to contain three 5-HT immunoreactive cells, which appeared to send bilateral projections into the frontal connectives and the recurrent nerve. During embryonic development, the dendritic arborizations of these frontal ganglion cells increased, while the amount of 5-HT immunoreactivity in the cell bodies decreased. Thus, the serotonergic system first appears in the Manduca embryo at an early stage of development, similar to the situation in other insects as well as vertebrates. By the end of the embryonic period, the same number of serotonergic neurons are present in the brain as in larval and adult Manduca, suggesting that once formed, these cells persist through postembryonic development and metamorphosis.

Neurons involved in nitric oxide-mediated cGMP signaling in the tobacco hornworm,Manduca sexta

“…In addition, based on their location, size, and axon branching, the three stained cells in the FG (Fig. 1B and 7) are possibly a subset of serotonin‐containing neurons thought to innervate the midgut and the CC–CA complex (Granger et al, 1989; Radwan et al, 1989). Similar results have been obtained in Drosophila larvae, where the CA of the ring gland and VUM neurons are also NADPHd positive (Wildemann and Bicker, 1999).…”

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

“…DOI 10.1002/cne bodies, together with expansion of the neuropil, that transforms the initially oval ganglion into its characteristic pear-shape in the adult. Unlike the serotonergic neurons in the frontal ganglion of Manduca, the size of which decreases after an initial phase of increase (Radwan et al, 1989), serotonergic ENS neurons of Locusta never reduce their diameter.…”

“…In the insect ENS the embryonic development of the serotonergic system has been described in the frontal ganglion of Manduca (Radwan et al, 1989). In Drosophila, Budnik et al (1989) described the postembryonic development of serotonergic midgut arborizations and its dependence on the presence of serotonin.…”

“…A broad variety of neurotransmitters has been found in the insect ENS, e.g., various peptides (Copenhaver and Taghert, 1989a;Duve and Thorpe, 2003;Hill and Orchard, 2003;Clark et al, 2006), GABA (Luffy and Dorn, 1992;Trumm and Dorn, 2000), acetylcholine (Bicker et al, 2004), and serotonin (Davis, 1985;Klemm et al, 1986;Radwan et al, 1989;Luffy and Dorn, 1992;Molaei and Lange, 2003). Serotonergic neurons form a large group among ENS neurons.…”

GABA and serotonin immunoreactivity during postembryonic brain development in the beetleTenebrio molitor

“…This study will review the distribution of serotonin and GABA immunoreactive neurons in the central brain of Tenebrio molitor, and additional data will be provided on developmental processes involved in pattern formation of antennal lobes and central body. The limited number of serotonin immunoreactive neurons in the insect brain allows a detailed analysis of the morphology of these neurons throughout postembryonic development and indicates that they are developmentally conserved (Breidbach, 1990;Granger et al, 1989;Radwan et al, 1989;Seidel and Bicker, 1996;White, 1986, 1988;Wegerhoff and Breidbach, 1992). For serotonin containing wide-field neurons that centrifugally invade sensory neuropils, a role in modulation of the integration of sensory inputs has been shown for different insect species (Erber and Kloppenburg, 1995;Erber et al, 1991Erber et al, , 1993Muszynska-Pytel and Cymborowski, 1978;Salecker and Distler, 1990), whereas serotonin or other amines in small field neurons may serve as a conventional transmitter in local neuronal circuits (for review see Homberg, 1994).…”