Cross-species evidence for the refinement of intrinsic neural timescales supporting executive system maturation through adolescence
Shane D. McKeoniD, Daniel Justin PetrieiD, Valerie J. SydnoriD, Zhengyang WangiD, Junda ZhuiD, Alyssa Famalette, Will ForaniD, Ashley C. ParriD, Finnegan J. CalabroiD, Taylor J. AbeliD, Christos ConstantinidisiD, Beatríz LunaiD
Abstract
Brain functional, structural, and neurochemical maturation has been found to support the specialization of executive systems through adolescence that will lead to adult level processing. Importantly, animal models and initial EEG studies in humans indicate developmental improvements in neural processing of complex information that would be evident in changes in temporal dynamics, which are not well-understood. Intrinsic neural timescales (INTs), or the temporal windows over which neural populations integrate inputs, have been proposed to reflect circuit-level properties such as excitatory-inhibitory (E/I) balance, myelination, and functional properties supporting complex information processing such as in executive functioning. Here, we used a multimodal, cross-species approach to investigate how INTs develop across adolescence to support cognitive specialization. In parallel analyses using a large longitudinal human EEG cohort, adolescent intracranial sEEG recordings, and macaque local field potentials, we observed robust reductions in INTs through adolescence, particularly in frontal and parietal association cortices. These developmental reductions were shaped by local circuit physiology, as evidenced by associations between shorter INTs and both lower aperiodic exponents, indicative of increased E/I balance, and reduced spectral offsets, suggesting lower aggregate spiking. We also found structural contributions via developmental interactions between age and deep layer intracortical myelination which predicted shorter INTs, suggesting that long-range circuitry may play a key role in shaping spontaneous temporal dynamics. Functionally, shorter INTs in adolescence were linked to improved working memory accuracy and reduced response time variability, indicating a behavioral advantage of refined temporal integration windows through development. Together, these findings establish INTs as a conserved, biologically grounded signature of adolescent brain maturation, providing a mechanistic framework for how structural and physiological refinements reorganize temporal processing to support increasingly efficient cognitive function.
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