Scale-free behavioral dynamics directly linked with scale-free cortical dynamics
- University of Arkansas at Fayetteville, United States
Abstract
Naturally occurring body movements and collective neural activity both exhibit complex dynamics, often with scale-free, fractal spatiotemporal structure. Scale-free dynamics of both brain and behavior are important because each is associated with functional benefits to the organism. Despite their similarities, scale-free brain activity and scale-free behavior have been studied separately, without a unified explanation. Here we show that scale-free dynamics of mouse behavior and neurons in visual cortex are strongly related. Surprisingly, the scale-free neural activity is limited to specific subsets of neurons, and these scale-free subsets exhibit stochastic winner-take-all competition with other neural subsets. This observation is inconsistent with prevailing theories of scale-free dynamics in neural systems, which stem from the criticality hypothesis. We develop a computational model which incorporates known cell-type-specific circuit structure, explaining our findings with a new type of critical dynamics. Our results establish neural underpinnings of scale-free behavior and clear behavioral relevance of scale-free neural activity.
Data availability
The data analyzed here were first published in Stringer et al. (2019) and are publicly available on Figshare at Stringer, Carsen; Pachitariu, Marius; Reddy, Charu; Carandini, Matteo; Harris, Kenneth D. (2018): Recordings of ten thousand neurons in visual cortex during spontaneous behaviors. Janelia Research Campus. Dataset. https://doi.org/10.25378/janelia.6163622.v6. Analysis and simulation codes are publicly available on Figshare https://doi.org/10.6084/m9.figshare.21954389.v1
-
Code for computational model, power law fitting, power law range [Shew Lab]https://doi.org/10.6084/m9.figshare.21954389.v1.
Article and author information
Author details
Funding
National Institutes of Health (NIHR15NS116742)
- Woodrow L Shew
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Gordon J Berman, Emory University, United States
Ethics
Animal experimentation: All experimental procedures were conducted according to the UK Animals Scientific Procedures Act (1986). Experiments were performed at University College London under personal and project licenses released by the Home Office following appropriate ethics review.
Version history
- Preprint posted: May 13, 2021 (view preprint)
- Received: May 3, 2022
- Accepted: January 6, 2023
- Accepted Manuscript published: January 27, 2023 (version 1)
- Version of Record published: February 15, 2023 (version 2)
Copyright
© 2023, Jones 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
-
- 1,944
- Page views
-
- 329
- Downloads
-
- 7
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
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)
Scale-free behavioral dynamics directly linked with scale-free cortical dynamics
eLife 12:e79950.
https://doi.org/10.7554/eLife.79950
Further reading
-
- Neuroscience
Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.
-
- Neuroscience
Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.
