Local synaptic inputs support opposing, network-specific odor representations in a widely projecting modulatory neuron.

Xiaonan Zhang,Andrew Dacks,Quentin Gaudry,Cengiz Günay,J Scott Lauritzen,Davi Bock,Kaylynn Coates,Feng Li,Steven A Calle-Schuler

doi:10.7554/elife.46839

Abstract

Serotonin plays different roles across networks within the same sensory modality. Previously, we used whole-cell electrophysiology in Drosophila to show that serotonergic neurons innervating the first olfactory relay are inhibited by odorants (Zhang and Gaudry, 2016). Here we show that network-spanning serotonergic neurons segregate information about stimulus features, odor intensity and identity, by using opposing coding schemes in different olfactory neuropil. A pair of serotonergic neurons (the CSDns) innervate the antennal lobe and lateral horn, which are first and second order neuropils. CSDn processes in the antennal lobe are inhibited by odors in an identity independent manner. In the lateral horn, CSDn processes are excited in an odor identity dependent manner. Using functional imaging, modeling, and EM reconstruction, we demonstrate that antennal lobe derived inhibition arises from local GABAergic inputs and acts as a means of gain control on branch-specific inputs that the CSDns receive within the lateral horn.

Highlights

All neuronal circuits are subject to neuromodulation from both neurons intrinsic to a network and extrinsic centrifugal sources (Katz, 1995; Lizbinski and Dacks, 2017)
The olfactory bulb (OB) in mammals receives a tremendous amount of centrifugal innervation (Padmanabhan et al, 2018) that can be critical for proper olfactory behavior (Nunez-Parra et al, 2013)
We initially imaged contralaterally-projecting serotonin-immunoreactive deuterocerebral neuron (CSDn) neurites in the antennal lobe (AL) (Figure 1B, Figure 1— video 1) and found that most compounds in a diverse panel of odorants resulted in inhibition (Figure 1C and D and Figure 1—figure supplement 1)

Summary

Introduction

All neuronal circuits are subject to neuromodulation from both neurons intrinsic to a network and extrinsic centrifugal sources (Katz, 1995; Lizbinski and Dacks, 2017). By spanning and innervating most cortical and subcortical regions, modulatory systems target multiple points along the sensory-motor axis of functional circuits. Modulatory systems are traditionally regarded as integrate-and-fire models where the neurons integrate synaptic inputs in their dendrites within their local nuclei and use action potentials to broadcast this signal to release sites across sensory networks. Such models imply that modulator release will be inherently correlated across distal targets. As virtually all axons are subject to pre-synaptic regulation

Methods

Results

Conclusion