A temporal sequence of thalamic activity unfolds at transitions in behavioral arousal state

Abstract

The moment of awakening from sleep reflects a profound transformation in neural activity and behavior. The thalamus is a key controller of arousal state, but whether its diverse nuclei exhibit coordinated or distinct activity at transitions in behavioral arousal state is not known. Using fast fMRI at ultra-high field (7 Tesla), we measured sub-second activity across thalamocortical networks and within nine thalamic nuclei to delineate these dynamics during spontaneous transitions in behavioral arousal state. We discovered a stereotyped sequence of activity across thalamic nuclei that preceded behavioral arousal after a period of inactivity, followed by widespread cortical deactivation. These thalamic dynamics were linked to whether participants remained awake or fell back asleep, with unified thalamic activation reflecting subsequent maintenance of awake behavior. These results provide an outline of the complex interactions across thalamocortical circuits that orchestrate arousal state transitions, and additionally, demonstrate that fast fMRI can resolve sub-second subcortical dynamics in the human brain.

Resting-state fMRI signals contain spectral signatures of local hemodynamic response timing

“…Improvements in the temporal resolution of BOLD fMRI have also sparked interest in detecting neural sequences at sub-second timescales, which are highly relevant for many studies of cognition. Recent studies have leveraged fast fMRI to detect rapid sequences of neural events related to visual sequence detection ( Wittkuhn and Schuck, 2021 ), auditory dynamics ( Frühholz et al, 2020 ), and changes in arousal state ( Setzer et al, 2021 ). As we continue to identify these rapid neural sequences, it will become even more crucial to consider how the hemodynamic response varies across regions to determine whether a given sequence represents regional differences in neuronal or in hemodynamic timing.…”

“…Advances in acquisition technology now allow high-resolution whole brain fMRI data to be acquired at fast (<500ms) rates ( Polimeni and Lewis, 2021 ; Chen et al, 2019 ; Barth et al, 2016 ; Chiew et al, 2018 ; Hennig et al, 2007 ; Setsompop et al, 2016 ), suggesting that fMRI could provide a unique tool to noninvasively track temporal sequences of neural activity ( Menon et al, 1998 ) across the entire brain. Indeed, recent studies have revealed highly structured temporal dynamics using fMRI and suggest that fMRI can enable whole-brain mapping of temporal sequences ( Lee et al, 2013 ; Setzer et al, 2021 ; Raut et al, 2021 ; Mitra et al, 2016 ; Vizioli et al, 2018 ). Furthermore, hemodynamic signals have been shown to contain more information about fast and high-frequency activity than previously thought ( Lee et al, 2013 ; Smith et al, 2012 ; Chen and Glover, 2015 ; Lewis et al, 2016 ; Sasai et al, 2021 ).…”

Resting-state fMRI signals contain spectral signatures of local hemodynamic response timing

“…Improvements in the temporal resolution of BOLD fMRI have also sparked interest in detecting neural sequences at sub-second timescales, which are highly relevant for many studies of cognition. Recent studies have leveraged fast fMRI to detect rapid sequences of neural events related to visual sequence detection (76), auditory dynamics (77), and changes in arousal state (22). As we continue to identify these rapid neural sequences, it will become even more crucial to consider how the hemodynamic response varies across regions to determine whether a given sequence represents regional differences in neuronal or in hemodynamic timing.…”

Abstract Book 6: OHBM 2024 Annual Meeting

“…pattern of BOLD activity propagates across the thalamus with fluctuating arousal(Gu et al, 2021;Raut et al, 2021;Setzer et al, 2021), which is a core deep-brain structure comprised of sub-nuclei with diverse functional roles in cognition. Therefore, slow, rhythmic brain dynamics have some functional and spatial structure.…”