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Molecular and functional profiling of cell diversity and identity in the lateral superior olive, an auditory brainstem center with ascending and descending projections

Authors :
Ayse Maraslioglu-Sperber
Erika Pizzi
Jonas O. Fisch
Kathrin Kattler
Tamara Ritter
Eckhard Friauf
Source :
Frontiers in Cellular Neuroscience, Vol 18 (2024)
Publication Year :
2024
Publisher :
Frontiers Media S.A., 2024.

Abstract

The lateral superior olive (LSO), a prominent integration center in the auditory brainstem, contains a remarkably heterogeneous population of neurons. Ascending neurons, predominantly principal neurons (pLSOs), process interaural level differences for sound localization. Descending neurons (lateral olivocochlear neurons, LOCs) provide feedback into the cochlea and are thought to protect against acoustic overload. The molecular determinants of the neuronal diversity in the LSO are largely unknown. Here, we used patch-seq analysis in mice at postnatal days P10-12 to classify developing LSO neurons according to their functional and molecular profiles. Across the entire sample (n = 86 neurons), genes involved in ATP synthesis were particularly highly expressed, confirming the energy expenditure of auditory neurons. Two clusters were identified, pLSOs and LOCs. They were distinguished by 353 differentially expressed genes (DEGs), most of which were novel for the LSO. Electrophysiological analysis confirmed the transcriptomic clustering. We focused on genes affecting neuronal input–output properties and validated some of them by immunohistochemistry, electrophysiology, and pharmacology. These genes encode proteins such as osteopontin, Kv11.3, and Kvβ3 (pLSO-specific), calcitonin-gene-related peptide (LOC-specific), or Kv7.2 and Kv7.3 (no DEGs). We identified 12 “Super DEGs” and 12 genes showing “Cluster similarity.” Collectively, we provide fundamental and comprehensive insights into the molecular composition of individual ascending and descending neurons in the juvenile auditory brainstem and how this may relate to their specific functions, including developmental aspects.

Details

Language :
English
ISSN :
16625102
Volume :
18
Database :
Directory of Open Access Journals
Journal :
Frontiers in Cellular Neuroscience
Publication Type :
Academic Journal
Accession number :
edsdoj.b74c7e5a0320480fbdf4c9d8bd49d5c1
Document Type :
article
Full Text :
https://doi.org/10.3389/fncel.2024.1354520