Greater Repertoire and Temporal Variability of Cross-Frequency Coupling (CFC) Modes in Resting-State Neuromagnetic Recordings among Children with Reading Difficulties.

Stavros I. Dimitriadis,Panagiotis G. Simos,Andrew C. Papanicolaou,Nikolaos A. Laskaris,Jack M. Fletcher

doi:10.3389/fnhum.2016.00163

Abstract

Cross-frequency, phase-to-amplitude coupling (PAC) between neuronal oscillations at rest may serve as the substrate that supports information exchange between functionally specialized neuronal populations both within and between cortical regions. The study utilizes novel algorithms to identify prominent instantaneous modes of cross-frequency coupling and their temporal stability in resting state magnetoencephalography (MEG) data from 25 students experiencing severe reading difficulties (RD) and 27 age-matched non-impaired readers (NI). Phase coherence estimates were computed in order to identify the prominent mode of PAC interaction for each sensor, sensor pair, and pair of frequency bands (from δ to γ) at successive time windows of the continuous MEG record. The degree of variability in the characteristic frequency-pair PACf1−f2 modes over time was also estimated. Results revealed a wider repertoire of prominent PAC interactions in RD as compared to NI students, suggesting an altered functional substrate for information exchange between neuronal assemblies in the former group. Moreover, RD students showed significant variability in PAC modes over time. This temporal instability of PAC values was particularly prominent: (a) within and between right hemisphere temporo-parietal and occipito-temporal sensors and, (b) between left hemisphere frontal, temporal, and occipito-temporal sensors and corresponding right hemisphere sites. Altered modes of neuronal population coupling may help account for extant data revealing reduced, task-related neurophysiological and hemodynamic activation in left hemisphere regions involved in the reading network in RD. Moreover, the spatial distribution of pronounced instability of cross-frequency coupling modes in this group may provide an explanation for previous reports suggesting the presence of inefficient compensatory mechanisms to support reading.

Highlights

The neurophysiological basis and functional significance of spontaneous brain activity remains disputable among neuroscientists, ever since the initial demonstration of focally reduced activity associated with increased cognitive demands (Pinneo, 1966)
To ensure that phase-to-amplitude coupling (PAC) values were not driven by the power of the low-frequency signal, we estimated the difference between: (a) the low frequency involved in computing each PAC value and (b) the frequency associated with the highest power in the signal, separately for each time window, sensor, and sensor pair
Group averaging can only be used for demonstration purposes, the distributions of individual TV PAC values were clearly different between groups (Wilxocon test, p < 10−12)

Summary

Introduction

The neurophysiological basis and functional significance of spontaneous brain activity remains disputable among neuroscientists, ever since the initial demonstration of focally reduced activity associated with increased cognitive demands (Pinneo, 1966). Restingstate functional connectivity has been studied in relation to disorders of consciousness (Heine et al, 2012), Alzheimer’s disease (Buckner et al, 2008; Stam et al, 2009; Khazaee et al, 2015), schizophrenia (Bassett et al, 2012; Damaraju et al, 2014), depression (Jin et al, 2011; for reviews see Rosazza and Minati, 2011; Dutta et al, 2014), in mTBI (Dimitriadis et al, 2015d; Antonakakis et al, 2016), in dyslexia (Koyama et al, 2010, 2011; Dimitriadis et al, 2013b), and in normal populations (Raichle et al, 2001; Greicius et al, 2003; Fair et al, 2008; De Pasquale et al, 2010; Brookes et al, 2011) In this line of research, the brain is viewed as a complex network comprised of sets of smaller subsystems, interacting in a dynamic manner, both locally and at longer ranges (Tognoli and Kelso, 2014a,b). There is rapidly accumulating experimental evidence supporting this role of CFC in cognition (Jensen and Colgin, 2007; Canolty and Knight, 2010; Palva and Palva, 2011; Buzsáki and Watson, 2012; Jirsa and Müller, 2013; Dimitriadis et al, 2015a,c; Dimitriadis et al, 2016)

Methods

Results

Conclusion