Abstract
Recent studies on Drosophila melanogaster and other insects have revealed important insights into the functions and evolution of neuropeptide signaling. In contrast, in- and output connections of insect peptidergic circuits are largely unexplored. Existing morphological descriptions typically do not determine the exact spatial location of peptidergic axonal pathways and arborizations within the neuropil, and do not identify peptidergic in- and output compartments. Such information is however fundamental to screen for possible peptidergic network connections, a prerequisite to understand how the CNS controls the activity of peptidergic neurons at the synaptic level. We provide a precise 3D morphological description of peptidergic neurons in the thoracic and abdominal neuromeres of the Drosophila larva based on fasciclin-2 (Fas2) immunopositive tracts as landmarks. Comparing the Fas2 “coordinates” of projections of sensory or other neurons with those of peptidergic neurons, it is possible to identify candidate in- and output connections of specific peptidergic systems. These connections can subsequently be more rigorously tested. By immunolabeling and GAL4-directed expression of marker proteins, we analyzed the projections and compartmentalization of neurons expressing 12 different peptide genes, encoding approximately 75% of the neuropeptides chemically identified within the Drosophila CNS. Results are assembled into standardized plates which provide a guide to identify candidate afferent or target neurons with overlapping projections. In general, we found that putative dendritic compartments of peptidergic neurons are concentrated around the median Fas2 tracts and the terminal plexus. Putative peptide release sites in the ventral nerve cord were also more laterally situated. Our results suggest that i) peptidergic neurons in the Drosophila ventral nerve cord have separated in- and output compartments in specific areas, and ii) volume transmission is a prevailing way of peptidergic communication within the CNS. The data can further be useful to identify colocalized transmitters and receptors, and develop peptidergic neurons as new landmarks.
Highlights
Neuropeptides are neuronal signaling molecules that are involved in the regulation of diverse processes such as development and growth, metabolism, reproduction, ion homeostasis, circadian rhythms and behavior
The peptide selection focused on neuropeptide hormones stored in thoracic or abdominal neurohemal organs (FMRFa-like peptides, CAPA peptides) or peripheral release sites on body wall muscles or the gut (CCAP, myoinhibitory peptides (MIPs), leucokinin, pigment-dispersing factor (PDF)), and the availability of specific GAL4-lines
Of the peptidergic neurons with cell bodies in the VNC, only those expressing corazonin were found to have varicosities indicative of release sites around the dorsal median (DM) and VM tracts (Fig. 5). These findings suggest that the arborizations around the DM and VM tracts are mainly input compartments for peptidergic VNC neurons, and point to this midline region as a main site for synaptic inputs onto peptidergic neurons including the CCAP neurons
Summary
Neuropeptides are neuronal signaling molecules that are involved in the regulation of diverse processes such as development and growth, metabolism, reproduction, ion homeostasis, circadian rhythms and behavior. Neuropeptides can be produced by neurosecretory cells (secretory neurons) as well as interneurons, and are released as hormones into the circulation, or locally within the CNS. The role of direct synaptic input in the control of activity of peptidergic insect neurons is largely unexplored. This applies to the fruit fly Drosophila melanogaster, it has been shown that peptidergic Drosophila neurons express functional receptors for various neurotransmitters and biogenic amines [5,6,7,8]. Our knowledge on the behavioral or physiological effects of insect neuropeptides is steadily increasing (see [1,2,3]), the identity of targets of peptidergic neurons and the cellular mechanisms behind peptide signaling are commonly unknown, and we do not know whether centrally released peptides act as intrinsic or extrinsic neuromodulators (see [9])
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