Global waves synchronize the brain’s functional systems with fluctuating arousal

Abstract

We propose and empirically support a parsimonious account of intrinsic, brain-wide spatiotemporal organization arising from traveling waves linked to arousal. We hypothesize that these waves are the predominant physiological process reflected in spontaneous functional magnetic resonance imaging (fMRI) signal fluctuations. The correlation structure (“functional connectivity”) of these fluctuations recapitulates the large-scale functional organization of the brain. However, a unifying physiological account of this structure has so far been lacking. Here, using fMRI in humans, we show that ongoing arousal fluctuations are associated with global waves of activity that slowly propagate in parallel throughout the neocortex, thalamus, striatum, and cerebellum. We show that these waves can parsimoniously account for many features of spontaneous fMRI signal fluctuations, including topographically organized functional connectivity. Last, we demonstrate similar, cortex-wide propagation of neural activity measured with electrocorticography in macaques. These findings suggest that traveling waves spatiotemporally pattern brain-wide excitability in relation to arousal.

Revisiting Nonlinear Functional Brain Co-activations: Directed, Dynamic, and Delayed

“…In further work, we expect that will uncover a relation between this window-based functional connectivity and the information provided from the delays of our method. Another point that deserves to be clarified is the meaning of the peaks in the delay distribution, something already intriguing from previous results obtained using Pearson's correlation delays (see Figure 5 in Mitra et al, 2015a ), which was recently related to very slow arousal fluctuations (Raut et al, 2021 ).…”

“…It is important to remind that, in terms of neurophysiology, the observed changes in the BOLD signal can not be simply and exclusively attributed to change in neural responses (Aguirre et al, 1998 ; Noseworthy et al, 2003 ; Handwerker et al, 2004 ; Raut et al, 2021 ). The HRF variability has been pointed several times as a common confounder in the determination of functional connectivity using Pearson's correlation of the BOLD signals (Rangaprakash et al, 2018 ; Yan et al, 2018 ).…”

“…Several studies (Mitra et al, 2014 , 2015a , b ; Mitra and Raichle, 2016 , 2018 ) have provided consistent evidence for the presence of very slow (>1 s) fluctuations in the fMRI BOLD signal propagating throughout the neocortex, thalamus, striatum, and cerebellum. More recently, these slow waves of activity were shown to be associated with spontaneous arousal fluctuations that, in turn, can account for the topographic organization of the brain functional connectivity (Raut et al, 2021 ). This information was gathered by the use of conventional lagged cross-covariance between pairs of BOLD time series x i ( t ) and x j ( t ) extracted from regions i and j : where τ is the lag (in units of TRs).…”

Non-linear Functional Brain Co-activations in Short-Term Memory Distortion Tasks

“…It is worth mentioning that the type of correlation analysis used here is appealing, given the recent results indicating that BOLD infraslow signal fluctuations throughout the brain are coherent with arousal fluctuations (Raut et al, 2021). These results on humans fMRI show that ongoing arousal fluctuations are correlated with global waves of activity slowly propagating in parallel through the neocortex, thalamus, striatum, and FIGURE 6 | Distributions of delays between the stimuli and the nearest BOLD peaks for three ROIs significant for retrieval in local information processing (see Table 3).…”

Non-linear functional brain co-activations in short-term memory distortion tasks

“…It is worth mentioning that the type of correlation analysis used here is appealing, given the recent results indicating that BOLD infraslow signal fluctuations throughout the brain are coherent with arousal fluctuations (Raut et al, 2021). These results on humans fMRI show that ongoing arousal fluctuations are correlated with global waves of activity slowly propagating in parallel through the neocortex, thalamus, striatum, and cerebellum.…”