Transitioning between preparatory and precisely sequenced neuronal activity in production of a skilled behavior
- UT Southwestern Medical Center, United States
- University of Tokyo, Japan
- Texas Christian Unversity, United States
- University of Zurich/ETH Zurich, Switzerland
- Korea Brain Research Institute, Korea (South), Republic of
- Emory University, United States
Abstract
Precise neural sequences are associated with the production of well-learned skilled behaviors. Yet, how neural sequences arise in the brain remains unclear. In songbirds, premotor projection neurons in the cortical song nucleus HVC are necessary for producing learned song and exhibit precise sequential activity during singing. Using cell-type specific calcium imaging we identify populations of HVC premotor neurons associated with the beginning and ending of singing-related neural sequences. We characterize neurons that bookend singing-related sequences and neuronal populations that transition from sparse preparatory activity prior to song to precise neural sequences during singing. Recordings from downstream premotor neurons or the respiratory system suggest that pre-song activity may be involved in motor preparation to sing. These findings reveal population mechanisms associated with moving from non-vocal to vocal behavioral states and suggest that precise neural sequences begin and end as part of orchestrated activity across functionally diverse populations of cortical premotor neurons.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been included for the following main figures: 1F; 2B; 2D; 3G; 3H; 3I; 3J; 4G; 5D; 6B-E. All the data has been compiled into a single excel file, with the corresponding data represented in different sheet tabs. Matlab files used for calcium imaging analysis, specifically for selecting ROIs and filtering calcium traces, have also been included.
Article and author information
Author details
Richard HR Hahnloser
Funding
National Institute of Neurological Disorders and Stroke (R01NS108424)
- Todd F Roberts
National Institute on Deafness and Other Communication Disorders (R01DC014364)
- Todd F Roberts
National Science Foundation (IOS-1457206)
- Todd F Roberts
Swiss National Science Foundation (31003A_127024)
- Richard HR Hahnloser
Swiss National Science Foundation (31003A_156976)
- Richard HR Hahnloser
National Institute of Neurological Disorders and Stroke (R01NS108424)
- Brenton G Cooper
- Richard HR Hahnloser
- Todd F Roberts
National Institute of Neurological Disorders and Stroke (R01NS084844)
- Samuel J Sober
National Institute of Neurological Disorders and Stroke (R01NS099375)
- Samuel J Sober
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Experiments described in this study were conducted using adult male zebra finches and Bengalese finches ( >90 days post hatch). During experiments, birds were housed individually in sound-attenuating chambers on a 12/12 h day/night schedule and were given ad libitum access to food and water. All procedures were performed in accordance with established protocols approved by Animal Care and Use Committee's at UT Southwestern Medical Centers (2016-101562), Texas Christian University, Emory University, and the Korea Brain Research Institute. Research conducted by our colleagues in Korea was under IACUC-15-00028 and research at Emory was under 2003538.
Copyright
© 2019, Daliparthi 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.
Metrics
-
- 3,274
- views
-
- 454
- downloads
-
- 26
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Transitioning between preparatory and precisely sequenced neuronal activity in production of a skilled behavior
eLife 8:e43732.
https://doi.org/10.7554/eLife.43732
Further reading
-
- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
-
- Neuroscience
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.
