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.
Highlights
Nervous system signaling occurs either at synapses or via secreted diffusible chemicals that signal to target cells expressing specific receptors
We found that the Platynereis larval apical nervous system (ANS) has a low degree of synaptic connectivity, a strong neurosecretory character, and a high diversity of neuropeptide expression
We identified very specific peptidergic links based on proneuropeptide and G protein-coupled receptors (GPCRs) transcript expression that connect only a small subset of ANS neurons
Summary
Nervous system signaling occurs either at synapses or via secreted diffusible chemicals that signal to target cells expressing specific receptors. In Caenorhabditis elegans, the spatial mapping of monoamines and neuropeptides and their G protein-coupled receptors (GPCRs) revealed interconnected networks of synaptic and non-synaptic signaling (Bentley et al 2016) Neurosecretory centers, such as the vertebrate hypothalamus and pituitary, are found in the anterior brain of many animals and show exceptionally high levels of neuropeptide expression (Herget and Ryu 2015; Siegmund and Korge 2001; Campbell et al 2017) suggesting extensive non-synaptic signaling. The apical organ area or apical nervous system (ANS) in Platynereis larvae shows a distinct molecular fingerprint with similarities to other neuroendocrine centers, including the anterior medial neurosecretory center of arthropods and the vertebrate hypothalamus, suggesting a common ancestry (Tessmar-Raible et al 2007; Steinmetz et al 2010; Conzelmann et al 2013; Hunnekuhl and Akam 2014). Through connectomics and functional studies we reveal how this endocrine region can interact with the synaptic nervous system by peptidergic modulation of the ciliomotor circuitry
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