Spontaneous Neural Dynamics and Multi-scale Network Organization

Abstract

Spontaneous neural activity has historically been viewed as task-irrelevant noise that should be controlled for via experimental design, and removed through data analysis. However, electrophysiology and functional MRI studies of spontaneous activity patterns, which have greatly increased in number over the past decade, have revealed a close correspondence between these intrinsic patterns and the structural network architecture of functional brain circuits. In particular, by analyzing the large-scale covariation of spontaneous hemodynamics, researchers are able to reliably identify functional networks in the human brain. Subsequent work has sought to identify the corresponding neural signatures via electrophysiological measurements, as this would elucidate the neural origin of spontaneous hemodynamics and would reveal the temporal dynamics of these processes across slower and faster timescales. Here we survey common approaches to quantifying spontaneous neural activity, reviewing their empirical success, and their correspondence with the findings of neuroimaging. We emphasize invasive electrophysiological measurements, which are amenable to amplitude- and phase-based analyses, and which can report variations in connectivity with high spatiotemporal precision. After summarizing key findings from the human brain, we survey work in animal models that display similar multi-scale properties. We highlight that, across many spatiotemporal scales, the covariance structure of spontaneous neural activity reflects structural properties of neural networks and dynamically tracks their functional repertoire.

Distributed representation of context by intrinsic subnetworks in prefrontal cortex

“…Spontaneous correlations are increasingly found to reflect functional organization (14), yet their role in and consequences for neural computations remain poorly understood. One proposal is that spontaneous correlations are tuned by Hebbian mechanisms to reflect the natural statistics of the environment (28) such that correlated spontaneous activity has the effect of regularizing task-evoked activity (11).…”

“…Neural responses to repeated presentations of sensory stimuli, or in the absence of stimulation and explicit task demands, exhibit variability that is attributed to ongoing spontaneous activity (10)(11)(12)(13). Traditional analyses consider spontaneous activity to be noise, but there is increasing evidence that shared spontaneous variability is a signature of functional organization (14). Analyses of spontaneous correlations have been used to identify multiple large-scale functional networks (4,5,15) and boundaries between functional areas (2,(16)(17)(18) in human and nonhuman primate association cortex.…”

Local Field Potentials: Myths and Misunderstandings

“…Nevertheless, a more thorough understanding of how spatial microscopic factors affect intracerebral LFPs will also help clarify certain aspects of the EEG as a mass phenomenon, and this should be considered a necessary step toward accurately interpreting these recordings. Such information is also likely to be beneficial to the ongoing debate into other specific issues, such as the different information gathered from FPs observed over different spatial scales (Nunez et al, 1997; Foster et al, 2016). Indeed, not all types of neurons, pathways or structures are appropriate to generate LFPs and hence, they will not contribute to EEGs either.…”

EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: A review

“…This new view of how the brain processes information led to a vast amount of studies that investigated large-scale brain networks at rest: their spatial organization, temporal dynamics, associations with cognitive states, and alterations due to different cognitive disorders and neurological diseases (Cabral et al, 2014;Foster et al, 2016;Fox and Greicius, 2010;Mitra and Raichle, 2016). Various methods are used to reveal these networks, leading to different interpretations regarding their spatial and temporal organization.…”