Theta-Modulated Gamma-Band Synchronization Among Activated Regions During a Verb Generation Task

Abstract

Expressive language is complex and involves processing within a distributed network of cortical regions. Functional MRI and magnetoencephalography (MEG) have identified brain areas critical for expressive language, but how these regions communicate across the network remains poorly understood. It is thought that synchronization of oscillations between neural populations, particularly at a gamma rate (>30 Hz), underlies functional integration within cortical networks. Modulation of gamma rhythms by theta-band oscillations (4–8 Hz) has been proposed as a mechanism for the integration of local cell coalitions into large-scale networks underlying cognition and perception. The present study tested the hypothesis that these oscillatory mechanisms of functional integration were present within the expressive language network. We recorded MEG while subjects performed a covert verb generation task. We localized activated cortical regions using beamformer analysis, calculated inter-regional phase locking between activated areas, and measured modulation of inter-regional gamma synchronization by theta phase. The results show task-dependent gamma-band synchronization among regions activated during the performance of the verb generation task, and we provide evidence that these transient and periodic instances of high-frequency connectivity were modulated by the phase of cortical theta oscillations. These findings suggest that oscillatory synchronization and cross-frequency interactions are mechanisms for functional integration among distributed brain areas supporting expressive language processing.

Mapping Critical Language Sites in Children Performing Verb Generation: Whole-Brain Connectivity and Graph Theoretical Analysis in MEG

“…Group source analysis showed low-beta [13, 23] Hz ERD at left inferior frontal and posterior temporal regions, consistent with previous MEG expressive language studies (Singh et al, 2002; Hirata et al, 2004; Kadis et al, 2008, 2011; Ressel et al, 2008; Pang et al, 2011; Doesburg et al, 2012). Whole brain connectivity based on PLV metric derived from broad-band (3–30 Hz) sources suggested prominent connectivity at left perisylvian sites (Figure 1B) and hubs in left prefrontal regions (Figure 1C).…”

“…More recently, researchers have begun to use sophisticated analytic strategies such as functional and effective connectivity analysis to explore regional interactions for language (Bitan et al, 2005, 2006; Sonty et al, 2007; Allen et al, 2008; Leff et al, 2008; Schofield et al, 2009; David et al, 2011; Doesburg et al, 2012, 2015; Verly et al, 2014; Kadis et al, 2015; Xiao et al, 2016). In our recent MEG study of verb generation in children, we observed frequency dependent patterns of connectivity together with an increased number of suprathreshold effective (directed) connections with age, even though the extent of the network decreased and became increasingly left lateralized with age (Kadis et al, 2015).…”

Development of Network Synchronization Predicts Language Abilities

“…Task-dependent increases in inter-regional synchronization have been associated with numerous cognitive processes (see Uhlhaas et al, 2009a;Palva et al, 2012 for reviews) including both expressive and receptive language (Doesburg et al, 2008(Doesburg et al, , 2012 and letter processing (Herdman, 2011). Presently, we establish the normative developmental trajectory of inter-regional network synchronization throughout childhood and adolescence.…”

“…Modulation of neural oscillations, and their coordination across brain areas, have been linked to expressive language, receptive language, and the interactions between language networks and brain regions mediating other cognitive and perceptual abilities (i.e. Bastiaansen et al, 2005;Bedo et al, 2014;Bögels et al, 2014;Doesburg et al, 2008Doesburg et al, , 2012Ewald et al, 2012;Hermes et al, 2014;Mellem et al, 2013;Piai et al, 2013;Weiss & Mueller 2012), and local neural oscillations have been related to the encoding of speech sounds as well as the development of language abilities during infancy and early childhood (Benasich et al, 2008;Gou et al, 2011). Whether inter-regional coherence changes throughout childhood and adolescence, as well as if such changes are related to the development of language abilities, remains unknown.…”

Electroencephalography theta differences between object nouns and action verbs when identifying semantic relations

“…Specifically, gamma power increases more in response to action verbs than object nouns over motor cortices (Pulvermiiller et al, 1996) and increases over both left and right inferior frontal areas during verb generation tasks (Doesburg, Vinette, Cheung, & Pang, 2012). Conversely, gamma power decreases are observed in response to incongruent or unrelated informa tion in ongoing sentences (Bastiaansen et al, 2010;Hagoort et al, 2004;Hald et al, 2006;Penolazzi, Angrilli, & Job, 2009;Wang et al, 2012).…”