Directional patterns of cross frequency phase and amplitude coupling within the resting state mimic patterns of fMRI functional connectivity

Abstract

Functional imaging investigations into the brain's resting state interactions have yielded a wealth of insight into the intrinsic and dynamic neural architecture supporting cognition and behavior. Electrophysiological studies however have highlighted the fact that synchrony across large-scale cortical systems is composed of spontaneous interactions occurring at timescales beyond the traditional resolution of fMRI, a feature that limits the capacity of fMRI to draw inference on the true directional relationship between network nodes. To approach the question of directionality in resting state signals, we recorded resting state functional MRI (rsfMRI) and electrocorticography (ECoG) from four human subjects undergoing invasive epilepsy monitoring. Using a seed-point based approach, we employed phase-amplitude coupling (PAC) and biPhase Locking Values (bPLV), two measures of cross-frequency coupling (CFC) to explore both outgoing and incoming connections between the seed and all non-seed, site electrodes. We observed robust PAC between a wide range of low-frequency phase and high frequency amplitude estimates. However, significant bPLV, a CFC measure of phase-phase synchrony, was only observed at specific narrow low and high frequency bandwidths. Furthermore, the spatial patterns of outgoing PAC connectivity were most closely associated with the rsfMRI connectivity maps. Our results support the hypothesis that PAC is relatively ubiquitous phenomenon serving as a mechanism for coordinating high-frequency amplitudes across distant neuronal assemblies even in absence of overt task structure. Additionally, we demonstrate that the spatial distribution of a seed-point rsfMRI sensorimotor network is strikingly similar to specific patterns of directional PAC. Specifically, the high frequency activities of distal patches of cortex owning membership in a rsfMRI sensorimotor network were most likely to be entrained to the phase of a low frequency rhythm engendered from the neural populations at the seed-point, suggestive of greater directional coupling from the seed out to the site electrodes.

Evaluation of Phase-Amplitude Coupling in Resting State Magnetoencephalographic Signals: Effect of Surrogates and Evaluation Approach

“…Similarly, dynamic functional connectivity analysis using MEG source imaging also reveals the appearance and disappearance of various sensory or sensory-motor networks over time in the resting brain (de Pasquale et al, 2010; Brookes et al, 2014). Moreover, recent studies have also suggested a possible role of ubiquitous PAC in assisting the resting state network (Wang et al, 2012; Weaver et al, 2016). However, in the present study, PAC phenomenon appeared to be very limited (for the 15 s window length) or almost absent (for the 2 s window length) over multiple time segments across the nodes (Figure 5).…”

“…Recently, an MEG study on PAC during the resting state showed that 41–61% of cortical voxels exhibited significant PAC (Florin and Baillet, 2015). Recent invasive (electrocorticogram [EcoG] and local field potential [LFP]) studies have also suggested ubiquitous PAC phenomenon during the resting state that assists high-frequency communication across remote neuronal assemblies even in the absence of an overt task structure (Wang et al, 2012; Weaver et al, 2016). …”

Neural correlates of the lexicality effect in children

“…Neuroimaging meta-analysis studies that examine the lexicality effect (the difference between words and pseudowords) on adults' brain activation suggest that the familiarity and the lexical status of written stimuli affect the degree to which different reading-related brain regions are involved (Cattinelli et al, 2013; Jobard, Crivello, & Tzourio-Mazoyer, 2003; McNorgan, Chabal, O'Young, Lukic, & Booth, 2015; Mechelli et al, 2005; Protopapas et al, 2016; Pugh et al, 2001, 2010; Taylor et al, 2013). Pseudowords as compared to words show greater activation in regions that are associated with spelling to sound mapping, such as the supramarginal gyrus (SMG) and inferior parietal lobule (IPL) (Graves, Binder, Desai, Conant, & Seidenberg, 2010; Jobard et al, 2003), and phonological processing, such as the superior temporal gyrus (STG) and dorsal inferior frontal gyrus (IFG) (Fiez & Petersen, 1998; Richlan, Kronbichler, & Wimmer, 2011; Turkeltaub, Gareau, Flowers, Zeffiro, & Eden, 2003).…”

BCI Use and Its Relation to Adaptation in Cortical Networks

“…It is important to note that this decrease is consistent with predictions based on other motor learning tasks, suggesting that not only activity patterns but also connectivity patterns of BCI learning and use follow those of motor tasks [54]. However, while pure amplitude-based STWC experienced decreases, nonlinear cross-frequency phase-phase connectivity as assessed by biphase locking (bPLV) [55], [56] remained strikingly consistent throughout the period of task execution, and generally was observed between sites farther apart from each other than those with significant STWC [4]. The heterogeneity of connectivity changes across the brain, across frequency ranges, and between amplitude and phase measures require further investigation.…”