skip to main content

Title: Hierarchical dynamics as a macroscopic organizing principle of the human brain

Multimodal evidence suggests that brain regions accumulate information over timescales that vary according to anatomical hierarchy. Thus, these experimentally defined “temporal receptive windows” are longest in cortical regions that are distant from sensory input. Interestingly, spontaneous activity in these regions also plays out over relatively slow timescales (i.e., exhibits slower temporal autocorrelation decay). These findings raise the possibility that hierarchical timescales represent an intrinsic organizing principle of brain function. Here, using resting-state functional MRI, we show that the timescale of ongoing dynamics follows hierarchical spatial gradients throughout human cerebral cortex. These intrinsic timescale gradients give rise to systematic frequency differences among large-scale cortical networks and predict individual-specific features of functional connectivity. Whole-brain coverage permitted us to further investigate the large-scale organization of subcortical dynamics. We show that cortical timescale gradients are topographically mirrored in striatum, thalamus, and cerebellum. Finally, timescales in the hippocampus followed a posterior-to-anterior gradient, corresponding to the longitudinal axis of increasing representational scale. Thus, hierarchical dynamics emerge as a global organizing principle of mammalian brains.

; ;
Publication Date:
Journal Name:
Proceedings of the National Academy of Sciences
Page Range or eLocation-ID:
p. 20890-20897
Proceedings of the National Academy of Sciences
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Endogenous attention is the cognitive function that selects the relevant pieces of sensory information to achieve goals and it is known to be controlled by dorsal fronto-parietal brain areas. Here we expand this notion by identifying a control attention area located in the temporal lobe. By combining a demanding behavioral paradigm with functional neuroimaging and diffusion tractography, we show that like fronto-parietal attentional areas, the human posterior inferotemporal cortex exhibits significant attentional modulatory activity. This area is functionally distinct from surrounding cortical areas, and is directly connected to parietal and frontal attentional regions. These results show that attentional control spans three cortical lobes and overarches large distances through fiber pathways that run orthogonally to the dominant anterior-posterior axes of sensory processing, thus suggesting a different organizing principle for cognitive control.

  2. Abstract

    Spontaneous infra-slow (<0.1 Hz) fluctuations in functional magnetic resonance imaging (fMRI) signals are temporally correlated within large-scale functional brain networks, motivating their use for mapping systems-level brain organization. However, recent electrophysiological and hemodynamic evidence suggest state-dependent propagation of infra-slow fluctuations, implying a functional role for ongoing infra-slow activity. Crucially, the study of infra-slow temporal lag structure has thus far been limited to large groups, as analyzing propagation delays requires extensive data averaging to overcome sampling variability. Here, we use resting-state fMRI data from 11 extensively-sampled individuals to characterize lag structure at the individual level. In addition to stable individual-specific features, we find spatiotemporal topographies in each subject similar to the group average. Notably, we find a set of early regions that are common to all individuals, are preferentially positioned proximal to multiple functional networks, and overlap with brain regions known to respond to diverse behavioral tasks—altogether consistent with a hypothesized ability to broadly influence cortical excitability. Our findings suggest that, like correlation structure, temporal lag structure is a fundamental organizational property of resting-state infra-slow activity.

  3. Brain large-scale dynamics is constrained by the heterogeneity of intrinsic anatomical substrate. Little is known how the spatiotemporal dynamics adapt for the heterogeneous structural connectivity (SC). Modern neuroimaging modalities make it possible to study the intrinsic brain activity at the scale of seconds to minutes. Diffusion magnetic resonance imaging (dMRI) and functional MRI reveals the large-scale SC across different brain regions. Electrophysiological methods (i.e. MEG/EEG) provide direct measures of neural activity and exhibits complex neurobiological temporal dynamics which could not be solved by fMRI. However, most of existing multimodal analytical methods collapse the brain measurements either in space or time domain and fail to capture the spatio-temporal circuit dynamics. In this paper, we propose a novel spatio-temporal graph Transformer model to integrate the structural and functional connectivity in both spatial and temporal domain. The proposed method learns the heterogeneous node and graph representation via contrastive learning and multi-head attention based graph Transformer using multimodal brain data (i.e. fMRI, MRI, MEG and behavior performance). The proposed contrastive graph Transformer representation model incorporates the heterogeneity map constrained by T1-to-T2-weighted (T1w/T2w) to improve the model fit to structurefunction interactions. The experimental results with multimodal resting state brain measurements demonstrate the proposed method couldmore »highlight the local properties of large-scale brain spatio-temporal dynamics and capture the dependence strength between functional connectivity and behaviors. In summary, the proposed method enables the complex brain dynamics explanation for different modal variants.« less
  4. Abstract Functional connectivity (FC) describes the statistical dependence between neuronal populations or brain regions in resting-state fMRI studies and is commonly estimated as the Pearson correlation of time courses. Clustering or community detection reveals densely coupled sets of regions constituting resting-state networks or functional systems. These systems manifest most clearly when FC is sampled over longer epochs but appear to fluctuate on shorter timescales. Here, we propose a new approach to reveal temporal fluctuations in neuronal time series. Unwrapping FC signal correlations yields pairwise co-fluctuation time series, one for each node pair or edge, and allows tracking of fine-scale dynamics across the network. Co-fluctuations partition the network, at each time step, into exactly two communities. Sampled over time, the overlay of these bipartitions, a binary decomposition of the original time series, very closely approximates functional connectivity. Bipartitions exhibit characteristic spatiotemporal patterns that are reproducible across participants and imaging runs, capture individual differences, and disclose fine-scale temporal expression of functional systems. Our findings document that functional systems appear transiently and intermittently, and that FC results from the overlay of many variable instances of system expression. Potential applications of this decomposition of functional connectivity into a set of binary patterns are discussed.
  5. Objective

    We examine the spatiotemporal dynamics of neural activity and its correlates in heart rate and its variability (HR/HRV) during a fatiguing visuospatial working memory task.


    The neural and physiological drivers of fatigue are complex, coupled, and poorly understood. Investigations that combine the fidelity of neural indices and the field-readiness of physiological measures can facilitate measurements of fatigue states in operational settings.


    Sixteen healthy adults, balanced by sex, completed a 60-minute fatiguing visuospatial working memory task. Changes in task performance, subjective measures of effort and fatigue, cerebral hemodynamics, and HR/HRV were analyzed. Peak brain activation, functional and effective connections within relevant brain networks were contrasted against spectral and temporal features of HR/HRV.


    Task performance elicited increased neural activation in regions responsible for maintaining working memory capacity. With the onset of time-on-task effects, resource utilization was seen to increase beyond task-relevant networks. Over time, functional connections in the prefrontal cortex were seen to weaken, with changes in the causal relationships between key regions known to drive working memory. HR/HRV indices were seen to closely follow activity in the prefrontal cortex.


    This investigation provided a window into the neurophysiological underpinnings of working memory under the time-on-task effect. HR/HRV was largely shown to mirrormore »changes in cortical networks responsible for working memory, therefore supporting the possibility of unobtrusive state recognition under ecologically valid conditions.


    Findings here can inform the development of a fieldable index for cognitive fatigue.

    « less