The development of slow and fast theta oscillations in the human brain

Abstract

Theta oscillations are pivotal for attention and memory, with developmental shifts in theta activity and connectivity tracking memory ability across the lifespan. Building on initial evidence that the theta band separates into slow and fast sub-bands across development within the medial temporal lobe (MTL) and the prefrontal cortex (PFC), this preregistered study (https://osf.io/gsru7) characterized the frequencies of slow (~1.5-4.5 Hz) and fast (~4.5-9.0 Hz) theta oscillations across the brain in a large developmental cohort. We analyzed intracranial EEG (iEEG) recordings from widespread brain regions in 101 children and adults (5.93-54.00 years, 63 males; n electrodes = 5691) using task-based (attention to to-be-remembered visual stimuli) and task-free (resting-state) data. We reveal distinct slow and fast theta oscillations in all regions and identify a spatial gradient in both frequency ranges, with slow theta oscillations speeding up and fast theta oscillations slowing down from posterior to anterior regions. The dissociation between slow and fast theta frequencies peaks during young adulthood, mirroring the developmental trajectory of attention and memory. In the hippocampus and PFC, attentional state (task-based, task-free) modulated age effects, and individual differences in task-based slow theta frequencies predicted individual differences in memory performance, linking the development of slow theta oscillations to the development of memory. Gray matter volume was not associated with age- or task-related differences in theta frequencies, suggesting that the development of theta oscillations is independent of regional brain structure. This study establishes developmental trajectories of slow and fast theta oscillations in localized brain regions and links the maturation of hippocampal and PFC slow theta oscillations to the development of attention and memory.