Exploring mechanisms of spontaneous functional connectivity in MEG: How delayed network interactions lead to structured amplitude envelopes of band-pass filtered oscillations

Rhythmic activity plays a central role in neural computations and brain functions ranging from homeostasis to attention, as well as in neurological and neuropsychiatric disorders. Despite this pervasiveness, little is known about the mechanisms whereby the frequency and power of oscillatory activity are modulated, and how they reflect the inputs received by neurons. Numerous studies have reported input-dependent fluctuations in peak frequency and power (as well as couplings across these features). However, it remains unresolved what mediates these spectral shifts among neural populations. Extending previous findings regarding stochastic nonlinear systems and experimental observations, we provide analytical insights regarding oscillatory responses of neural populations to stimulation from either endogenous or exogenous origins. Using a deceptively simple yet sparse and randomly connected network of neurons, we show how spiking inputs can reliably modulate the peak frequency and power expressed by synchronous neural populations without any changes in circuitry. Our results reveal that a generic, non-nonlinear and input-induced mechanism can robustly mediate these spectral fluctuations, and thus provide a framework in which inputs to the neurons bidirectionally regulate both the frequency and power expressed by synchronous populations. Theoretical and computational analysis of the ensuing spectral fluctuations was found to reflect the underlying dynamics of the input stimuli driving the neurons. Our results provide insights regarding a generic mechanism supporting spectral transitions observed across cortical networks and spanning multiple frequency bands.

The brain regulates information flow by balancing the segregation and integration of incoming stimuli to facilitate flexible cognition and behaviour. Topological features of brain networks, in particular network communities and hubs, support this segregation and integration but do not provide information regarding how external inputs are processed dynamically (i.e. over time). Experiments in which the consequences of selective inputs on brain activity are controlled and traced with great precision could provide such information. However, such strategies have thus far had limited success. By contrast, recent whole-brain computational modelling approaches have enabled us to start assessing the effect of input perturbations on brain dynamics in silico. IntroductionEvolution has developed many different strategies for the survival of species. The relative evolutionary success of mammals has been made possible by sophisticated brains that can combine current stimuli with past memories to predict the future and to adapt behaviour accordingly. The healthy human brain is very good at segregating and integrating information from different sensory modalities, which is combined with memory traces and with information about the current state of the brain and body to guide predictions and decision-making processes needed for adaptive behaviour. Take the example of a tennis player who effortless can integrate the colour, movement and shape of a tennis ball whilst segregating this object from the changing background of the tennis court and crowd, while she is predicting its trajectory and planning how best to position her tennis racket to return the ball beyond her opponent's reach. The integrated information can be formally defined as the information possessed by a system which is above and beyond the information that is available from the sum of its parts 1, 2 . Such information integration has been linked to

Structural and functional connectivity (SC and FC) have received much attention over the last decade, as they offer unique insight into the coordination of brain functioning. They are often assessed independently with three imaging modalities: SC using diffusion‐weighted imaging (DWI), FC using functional magnetic resonance imaging (fMRI), and magnetoencephalography/electroencephalography (MEG/EEG). DWI provides information about white matter organization, allowing the reconstruction of fiber bundles. fMRI uses blood‐oxygenation level‐dependent (BOLD) contrast to indirectly map neuronal activation. MEG and EEG are direct measures of neuronal activity, as they are sensitive to the synchronous inputs in pyramidal neurons. Seminal studies have targeted either the electrophysiological substrate of BOLD or the anatomical basis of FC. However, multimodal comparisons have been scarcely performed, and the relation between SC, fMRI‐FC, and MEG‐FC is still unclear. Here we present a systematic comparison of SC, resting state fMRI‐FC, and MEG‐FC between cortical regions, by evaluating their similarities at three different scales: global network, node, and hub distribution. We obtained strong similarities between the three modalities, especially for the following pairwise combinations: SC and fMRI‐FC; SC and MEG‐FC at theta, alpha, beta and gamma bands; and fMRI‐FC and MEG‐FC in alpha and beta. Furthermore, highest node similarity was found for regions of the default mode network and primary motor cortex, which also presented the highest hubness score. Distance was partially responsible for these similarities since it biased all three connectivity estimates, but not the unique contributor, since similarities remained after controlling for distance. Hum Brain Mapp 37:20–34, 2016. © 2015 The Authors Human Brain Mapping Published by Wiley Periodicals, Inc.