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Trajectory of frequency stability in typical development

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Abstract

This work explores a feature of brain dynamics, metastability, by which transients are observed in functional brain data. Metastability is a balance between static (stable) and dynamic (unstable) tendencies in electrophysiological brain activity. Furthermore, metastability is a theoretical mechanism underlying the rapid synchronization of cell assemblies that serve as neural substrates for cognitive states, and it has been associated with cognitive flexibility. While much previous research has sought to characterize metastability in the adult human brain, few studies have examined metastability in early development, in part because of the challenges of acquiring adequate, noise free continuous data in young children. To accomplish this endeavor, we studied a new method for characterizing the stability of EEG frequency in early childhood, as inspired by prior approaches for describing cortical phase resets in the scalp EEG of healthy adults. Specifically, we quantified the variance of the rate of change of the signal phase (i.e., frequency) as a proxy for phase resets (signal instability), given that phase resets occur almost simultaneously across large portions of the scalp. We tested our method in a cohort of 39 preschool age children (age =53 ± 13.6 months). We found that our outcome variable of interest, frequency variance, was a promising marker of signal stability, as it increased with the number of phase resets in surrogate (artificial) signals. In our cohort of children, frequency variance decreased cross-sectionally with age (r = −0.47, p = 0.0028). EEG signal stability, as quantified by frequency variance, increases with age in preschool age children. Future studies will relate this biomarker with the development of executive function and cognitive flexibility in children, with the overarching goal of understanding metastability in atypical development.

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Acknowledgments

The authors are deeply grateful to all children and parents who volunteered their time to advance our knowledge of typical development. We thank Dr. Mikhail Rabinovich for his comments on theoretical aspects of this work, as well as Dr. Ted Hutman and Dr. Carrie Bearden for their much appreciated feedback on the manuscript. A warm thank you is also extended to Nima Chenari for his kind help producing illustrations and to Christina Shimizu, Andrew Sanders, and Amanda Noroña for their patience and professionalism in assisting with data collection. This work was supported by NIMH K23MH094517-01.

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All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study

Conflict of interest

Joel Frohlich, Andrei Irimia, and Shafali S. Jeste declare that they have no conflicts of interest.

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Frohlich, J., Irimia, A. & Jeste, S.S. Trajectory of frequency stability in typical development. Brain Imaging and Behavior 9, 5–18 (2015). https://doi.org/10.1007/s11682-014-9339-3

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