Synaptic and peptidergic connectome of a neurosecretory center in the annelid brain

Abstract

Neurosecretory centers in animal brains use peptidergic signaling to influence physiology and behavior. Understanding neurosecretory center function requires mapping cell types, synapses, and peptidergic networks. Here we use transmission electron microscopy and gene expression mapping to analyze the synaptic and peptidergic connectome of an entire neurosecretory center. We reconstructed 78 neurosecretory neurons and mapped their synaptic connectivity in the brain of larval Platynereis dumerilii, a marine annelid. These neurons form an anterior neurosecretory center expressing many neuropeptides, including hypothalamic peptide orthologs and their receptors. Analysis of peptide-receptor pairs in spatially mapped single-cell transcriptome data revealed sparsely connected networks linking specific neuronal subsets. We experimentally analyzed one peptide-receptor pair and found that a neuropeptide can couple neurosecretory and synaptic brain signaling. Our study uncovered extensive networks of peptidergic signaling within a neurosecretory center and its connection to the synaptic brain.

Dual signaling of Wamide myoinhibitory peptides through a peptide‐gated channel and a GPCR in Platynereis

“…The expression patterns of MGIC were projected to the spatially mapped single-cell transcriptome data as previously described (17).…”

“…We next wanted to test if MAG and MGIC participate in different signaling networks in Platynereis. The expression pattern of MGIC was thus mapped to a virtual larval brain of spatially mapped single-cell transcriptome data (17,38) (Fig. 8A).…”

“…8A). We have previously mapped the expression of MAG and MIP and established peptidergic signaling networks between the expressing cells by treating MIP-expressing cells as source nodes and MAG-expressing cells as target nodes (17) (Fig. 8B).…”

“…A comprehensive complement of neuropeptides has been described for this species, consisting of 100 proneuropeptide genes (12). Several of these neuropeptides have been mapped to the nervous system and have been studied functionally (13)(14)(15)(16)(17). Furthermore, .20 different neuropeptide and monoamine GPCRs have been experimentally identified in Platynereis, including the founding members of several major bilaterian neuropeptide-receptor families (achatin, FMRFamide, RGWamide, FLamide, and elevenin receptors) and the first invertebrate adrenergic receptors (17)(18)(19).…”

Mapping Molecular Datasets Back to the Brain Regions They are Extracted from: Remembering the Native Countries of Hypothalamic Expatriates and Refugees

“…In this section, we have focused on molecular extraction of molecules from the hypothalamus, including, to name a few, neuropeptides of the hypothalamo-neurohypophysial system (OT and VP), the circadian system (VIP), and wakefulness and energy balance (H/O, MCH, AgRP). However, it is important to bear in mind that these “hypothalamic-derived” molecules are not strictly linked to the vertebrate hypothalamus per se , since large-scale molecular phylogenetic studies have identified precursors and analogs of these molecules in animal taxa that have evolved nervous systems lacking a hypothalamus [197, 282, 455]. For example, Semmens et al (2016) [391] performed transcriptomic studies of the radial nerve cords of the European starfish, Asterias rubens , and identified >40 neuropeptide precursors in this echinoderm, many of which have homologs in the vertebrate hypothalamus.…”