Abstract
We reconstructed, from a whole CNS EM volume, the synaptic map of input and output neurons that underlie food intake behavior of Drosophila larvae. Input neurons originate from enteric, pharyngeal and external sensory organs and converge onto seven distinct sensory synaptic compartments within the CNS. Output neurons consist of feeding motor, serotonergic modulatory and neuroendocrine neurons. Monosynaptic connections from a set of sensory synaptic compartments cover the motor, modulatory and neuroendocrine targets in overlapping domains. Polysynaptic routes are superimposed on top of monosynaptic connections, resulting in divergent sensory paths that converge on common outputs. A completely different set of sensory compartments is connected to the mushroom body calyx. The mushroom body output neurons are connected to interneurons that directly target the feeding output neurons. Our results illustrate a circuit architecture in which monosynaptic and multisynaptic connections from sensory inputs traverse onto output neurons via a series of converging paths.
Highlights
Motor outputs of a nervous system can be broadly defined into those carried out by the muscles to produce movements and by the neuroendocrine glands for secretion (Shepherd 1987)
We provide a comprehensive synaptic map of the sensory and motor output neurons that underlie food intake and metabolic homeostasis in Drosophila larva
They include a cluster of serotonergic neurons that innervate the entire enteric nervous system, and which may have neuromodulatory effects on the feeding system in a global manner
Summary
Motor outputs of a nervous system can be broadly defined into those carried out by the muscles to produce movements and by the neuroendocrine glands for secretion (Shepherd 1987). Advances in the EM reconstruction of an entire CNS of a first instar larva (Ohyama et al 2015; Schlegel et al 2016; Schneider-Mizell et al 2016; Berck et al 2016; Eichler et al 2017; Gerhard et al 2017) (summarized in Kornfeld & Denk, 2018) offers an opportunity to elucidate an animals' feeding system on a brain-wide scale and at synaptic resolution As part of this community effort, we recently performed an integrated analysis of fast synaptic and neuropeptide receptor connections for an identified cluster of 20 interneurons that express the neuropeptide hugin, a homolog of the mammalian neuropeptide neuromedin U, and which regulates food intake behavior (Melcher et al 2006; Schoofs et al 2014a; Schlegel et al 2016). The study provided a starting point for a combined approach to studying synaptic and neuropeptidergic circuits (Diao et al 2017; Williams et al 2017), but a basis for a comprehensive mapping of the sensory and motor neurons that innervate the major feeding and endocrine organs
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