Classifying Drosophila olfactory projection neuron boutons by quantitative analysis of electron microscopic reconstruction

Kai Yang; Tong Liu; Ze Wang; Jing Liu; Yuxinyao Shen; Xinyi Pan; Ruyi Wen; Haotian Xie; Zhaoxuan Ruan; Zixiao Tan; Yingying Chen; Aike Guo; He Liu; Hua Han; Zengru Di; Ke Zhang

doi:10.1016/j.isci.2022.104180

Classifying Drosophila olfactory projection neuron boutons by quantitative analysis of electron microscopic reconstruction

iScience. 2022 Apr 1;25(5):104180. doi: 10.1016/j.isci.2022.104180. eCollection 2022 May 20.

Authors

Kai Yang^{1

2}, Tong Liu³, Ze Wang³, Jing Liu⁴, Yuxinyao Shen⁵, Xinyi Pan⁵, Ruyi Wen⁵, Haotian Xie⁵, Zhaoxuan Ruan⁵, Zixiao Tan⁵, Yingying Chen⁵, Aike Guo^{3

5

6}, He Liu³, Hua Han⁴, Zengru Di³, Ke Zhang³

Affiliations

¹ School of Basic Medicine, Guangzhou University of Chinese Medicine, Guangzhou, Guangdong 510006, China.
² BNU-BUCM Hengqin Innovation Institute of Science and Technology, Zhuhai, Guangdong 518057, China.
³ International Academic Center of Complex Systems, Advanced Institute of Natural Sciences, Beijing Normal University at Zhuhai, Zhuhai, Guangdong 519087, China.
⁴ Institute of Automation, Chinese Academy of Sciences, Beijing 100190, China.
⁵ Huitong College, Beijing Normal University at Zhuhai, Zhuhai, Guangdong 519087, China.
⁶ School of Life Sciences, Shanghai University, Shanghai 200444, China.

Abstract

In Drosophila melanogaster, olfactory projection neurons (PNs) convey odor information from the antenna lobe to higher brain regions. Recent transcriptomic studies reveal a large diversity of transcription factors, cell-surface molecules, neurotransmitter-coding, and neuropeptide-coding genes in PNs; however, their structural diversity remains unknown. Herein, we achieved a volumetric reconstruction of 89 PN boutons under Focused Ion Beam Scanning Electron Microscopy (FIB-SEM) and quantitatively analyzed the internal presynaptic active zones (PAZs) and dense-core vesicles (DCVs). The ultrastructure-based cluster analysis reveals three morphological distinct bouton subtypes: complex boutons, unilobed boutons, and simple boutons. The complex boutons contain the most PAZs and DCVs, which suggests that they are of the highest capability of releasing neurotransmitters and neuromodulators. By labeling a subset of boutons under FIB-SEM, we found that DCVs are preferentially distributed in certain GH146-positive subtypes. Our study demonstrates that PN boutons display distinct morphology, which may determine their capacity of releasing neurotransmitters and neuromodulators.

Keywords: Cell biology; Neuroscience; Sensory neuroscience.