Bursting with Potential: How Sensorimotor Beta Bursts Develop from Infancy to Adulthood
- Holly Rayson1,2,5,
- Maciej J. Szul1,2,
- Perla El-Khoueiry1,2,
- Ranjan Debnath3,
- Marine Gautier-Martins1,2,
- Pier F. Ferrari1,2,
- Nathan Fox4, and
- James J. Bonaiuto1,2
- 1Institut des Sciences, Cognitives Marc Jeannerod, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5229, Bron, 69500, France
- 2Université de Lyon, Université Claude Bernard Lyon 1, Lyon, 69100, France
- 3Center for Psychiatry and Psychotherapy, Justus-Liebig University, Giessen, 35394, Germany
- 4Department of Human Development and Quantitative Methodology, University of Maryland, College Park, Maryland, 20742
- 5Inovarion, Paris, 75005, France
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Author contributions: H.R., M.J.S., P.F.F., N.F., and J.J.B. designed research; H.R., M.J.S., P.E., M.G.-M., and J.J.B. analyzed data; H.R. wrote the first draft of the paper; H.R., M.J.S., P.E., R.D., M.G.-M., P.F.F., N.F., and J.J.B. edited the paper; H.R. and J.J.B. wrote the paper; R.D. performed research.
Abstract
Beta activity is thought to play a critical role in sensorimotor processes. However, little is known about how activity in this frequency band develops. Here, we investigated the developmental trajectory of sensorimotor beta activity from infancy to adulthood. We recorded EEG from 9-month-old, 12-month-old, and adult humans (male and female) while they observed and executed grasping movements. We analyzed “beta burst” activity using a novel method that combines time-frequency decomposition and principal component analysis. We then examined the changes in burst rate and waveform motifs along the selected principal components. Our results reveal systematic changes in beta activity during action execution across development. We found a decrease in beta burst rate during movement execution in all age groups, with the greatest decrease observed in adults. Additionally, we identified three principal components that defined waveform motifs that systematically changed throughout the trial. We found that bursts with waveform shapes closer to the median waveform were not rate-modulated, whereas those with waveform shapes further from the median were differentially rate-modulated. Interestingly, the decrease in the rate of certain burst motifs occurred earlier during movement and was more lateralized in adults than in infants, suggesting that the rate modulation of specific types of beta bursts becomes increasingly refined with age.
SIGNIFICANCE STATEMENT We demonstrate that, like in adults, sensorimotor beta activity in infants during reaching and grasping movements occurs in bursts, not oscillations like thought traditionally. Furthermore, different beta waveform shapes were differentially modulated with age, including more lateralization in adults. Aberrant beta activity characterizes various developmental disorders and motor difficulties linked to early brain injury, so looking at burst waveform shape could provide more sensitivity for early identification and treatment of affected individuals before any behavioral symptoms emerge. More generally, comparison of beta burst activity in typical versus atypical motor development will also be instrumental in teasing apart the mechanistic functional roles of different types of beta bursts.
- Received May 15, 2023.
- Revision received July 15, 2023.
- Accepted July 20, 2023.
- Copyright © 2023 Rayson et al.
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