Aligned Organization of Synapses and Mitochondria in Auditory Hair Cells

Jing Liu; Shengxiong Wang; Yan Lu; Haoyu Wang; Fangfang Wang; Miaoxin Qiu; Qiwei Xie; Hua Han; Yunfeng Hua

doi:10.1007/s12264-021-00801-w

Aligned Organization of Synapses and Mitochondria in Auditory Hair Cells

Neurosci Bull. 2022 Mar;38(3):235-248. doi: 10.1007/s12264-021-00801-w. Epub 2021 Nov 27.

Authors

Jing Liu^#^{1

2

3}, Shengxiong Wang^#^{4

5}, Yan Lu^#^{5

6

7

8}, Haoyu Wang^#^{5

6

7

8}, Fangfang Wang⁵, Miaoxin Qiu⁴, Qiwei Xie⁹, Hua Han^{10

11

12}, Yunfeng Hua^{13

14

15

16}

Affiliations

¹ National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing, 100190, China.
² School of Artificial Intelligence, School of Future Technology, University of Chinese Academy of Sciences, Beijing, 101408, China.
³ CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai, 200031, China.
⁴ Putuo People's Hospital, Tongji University, Shanghai, 200060, China.
⁵ Shanghai Institute of Precision Medicine, Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200125, China.
⁶ Department of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People's Hospital, Shanghai, 200125, China.
⁷ Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai, 200125, China.
⁸ Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases, Shanghai, 200125, China.
⁹ Research Base of Beijing Modern Manufacturing Development, Beijing University of Technology, Beijing, 100124, China.
¹⁰ National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing, 100190, China. [email protected].
¹¹ School of Artificial Intelligence, School of Future Technology, University of Chinese Academy of Sciences, Beijing, 101408, China. [email protected].
¹² CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai, 200031, China. [email protected].
¹³ Shanghai Institute of Precision Medicine, Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200125, China. [email protected].
¹⁴ Department of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People's Hospital, Shanghai, 200125, China. [email protected].
¹⁵ Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai, 200125, China. [email protected].
¹⁶ Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases, Shanghai, 200125, China. [email protected].

^# Contributed equally.

Abstract

Recent studies have revealed great functional and structural heterogeneity in the ribbon-type synapses at the basolateral pole of the isopotential inner hair cell (IHC). This feature is believed to be critical for audition over a wide dynamic range, but whether the spatial gradient of ribbon morphology is fine-tuned in each IHC and how the mitochondrial network is organized to meet local energy demands of synaptic transmission remain unclear. By means of three-dimensional electron microscopy and artificial intelligence-based algorithms, we demonstrated the cell-wide structural quantification of ribbons and mitochondria in mature mid-cochlear IHCs of mice. We found that adjacent IHCs in staggered pairs differ substantially in cell body shape and ribbon morphology gradient as well as mitochondrial organization. Moreover, our analysis argues for a location-specific arrangement of correlated ribbon and mitochondrial function at the basolateral IHC pole.

Keywords: AI-based image processing; Inner hair cell; Mitochondrial network; Ribbon synapse; Volume electron microscopy.

MeSH terms

Animals
Artificial Intelligence*
Cochlea / metabolism
Hair Cells, Auditory, Inner*
Mice
Mitochondria
Synapses / metabolism