Motor cortex analogue neurons in songbirds utilize Kv3 subunits to generate ultranarrow spikes
- Oregon Health and Science University, United States
- Pennsylvania State University, United States
Abstract
Complex motor skills in vertebrates require specialized upper motor neurons with precise action potential (AP) firing. To examine how diverse populations of upper motor neurons subserve distinct functions and the specific repertoire of ion channels involved, we conducted a thorough study of the excitability of upper motor neurons controlling somatic motor function in the zebra finch. We found that robustus arcopallialis projection neurons (RAPNs), key command neurons for song production, exhibit ultranarrow spikes and higher firing rates compared to neurons controlling non-vocal somatic motor functions (AId neurons). Pharmacological and molecular data indicate that this striking difference is associated with the higher expression in RAPNs of a high threshold, fast-activating voltage-gated K+ channel, Kv3.1 (KCNC1). The spike waveform and Kv3.1 expression in RAPNs mirror properties of Betz cells, specialized upper motor neurons involved in fine digit control in humans and other primates but absent in rodents. Our study thus provides evidence that songbirds and primates have convergently evolved the use of Kv3.1 to ensure precise, rapid AP firing in upper motor neurons controlling fast and complex motor skills.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for all Figures.
Article and author information
Author details
Leonardo ES Tavares
Henrique von Gersdorff
Funding
National Science Foundation (NSF1456302)
- Claudio V Mello
National Science Foundation (NSF1645199)
- Claudio V Mello
National Institutes of Health (GM120464)
- Claudio V Mello
National Institutes of Health (DC004274)
- Henrique von Gersdorff
National Institutes of Health (DC012938)
- Henrique von Gersdorff
National Institutes of Health (AG055378)
- Benjamin M Zemel
National Science Foundation (NSF2154646)
- Claudio V Mello
- Henrique von Gersdorff
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols of the OHSU (IACUC # IP0000146).
Copyright
© 2023, Zemel et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Motor cortex analogue neurons in songbirds utilize Kv3 subunits to generate ultranarrow spikes
eLife 12:e81992.
https://doi.org/10.7554/eLife.81992
Further reading
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When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
