Original Research ARTICLE
Diverse intrinsic properties shape functional phenotype of low-frequency neurons in the auditory brainstem
- 1Communication Sciences and Disorders, Northwestern University, United States
- 2Florida State University, United States
In the auditory system, tonotopy is the spatial arrangement of where sounds of different frequencies are processed. Defined by the organization of neurons and their inputs, tonotopy emphasizes distinctions in neuronal structure and function across topographic gradients and is a common feature shared among vertebrates. In this study we characterized action potential firing patterns and ion channel properties from neurons located in the extremely low-frequency region of the chicken nucleus magnocellularis (NM), an auditory brainstem structure. We found that NM neurons responsible for encoding the lowest sound frequencies (termed NMc neurons) have enhanced excitability and fired bursts of action potentials to sinusoidal inputs ≤10 Hz; a distinct firing pattern compared to higher-frequency neurons. This response property was due to lower amounts of voltage dependent potassium (KV) conductances, unique combination of KV subunits and specialized sodium (NaV) channel properties. Particularly, NMc neurons had significantly lower KV1 and KV3 currents, but higher KV2 current. NMc neurons also showed larger and faster transient NaV current (INaT) with different voltage dependence of inactivation from higher-frequency neurons. In contrast, significantly smaller resurgent sodium current (INaR) was present in NMc with kinetics and voltage dependence that differed from higher-frequency neurons. Immunohistochemistry showed expression of NaV1.6 channel subtypes across the tonotopic axis. However, various immunoreactive patterns were observed between regions, likely underlying some tonotopic differences in INaT and INaR. Finally, using pharmacology and computational modeling, we concluded that KV3, KV2 channels and INaR work synergistically to regulate burst firing in NMc.
Keywords: nucleus magnocellularis, Potassium Channels, Sodium Channels, Action Potentials, auditory brainstem, resurgent sodium current, tonotopic map
Received: 31 Jan 2018;
Accepted: 04 Jun 2018.
Edited by:Arianna Maffei, Stony Brook University, United States
Reviewed by:Maxim Volgushev, University of Connecticut, United States
Ivan Milenkovic, Leipzig University, Germany
Copyright: © 2018 Hong, Wang, Lu, Zorio, Wang and Sanchez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Dr. Yuan Wang, Florida State University, Tallahassee, United States, email@example.com
Dr. Jason T. Sanchez, Northwestern University, Communication Sciences and Disorders, 2240 Campus Drive, Frances Searle Building, Evanston, 60206, IL, United States, firstname.lastname@example.org