Frequency-specific directed interactions in the human brain network for language

Abstract

The brain's remarkable capacity for language requires bidirectional interactions between functionally specialized brain regions. We used magnetoencephalography to investigate interregional interactions in the brain network for language while 102 participants were reading sentences. Using Granger causality analysis, we identified inferior frontal cortex and anterior temporal regions to receive widespread input and middle temporal regions to send widespread output. This fits well with the notion that these regions play a central role in language processing. Characterization of the functional topology of this network, using data-driven matrix factorization, which allowed for partitioning into a set of subnetworks, revealed directed connections at distinct frequencies of interaction. Connections originating from temporal regions peaked at alpha frequency, whereas connections originating from frontal and parietal regions peaked at beta frequency. These findings indicate that the information flow between language-relevant brain areas, which is required for linguistic processing, may depend on the contributions of distinct brain rhythms.language | Granger causality | brain networks | magnetoencephalography T he human brain is capable of effortlessly extracting meaning from sequences of written or spoken words by means of a sophisticated interplay between dedicated neocortical regions. Neuroanatomical research has revealed a number of white-matter pathways that facilitate these interregional interactions (1). Electrophysiological research with electro-and magnetoencephalography (EEG/MEG) has revealed with high temporal precision the sequential activation of individual nodes embedded within the human brain network for language (2, 3). However, the nature of the functional interactions that enable the efficient flow of information between the nodes of this network has yet to be elucidated.One important feature of cortical interregional connections is that they are frequently reciprocal in nature (4), which implies that information can be exchanged in a bidirectional fashion. Moreover, the information flow between cortical regions may be facilitated by interregional rhythmic synchronization (5), where neuronal rhythms of specific different frequencies reflect the direction in which the information is flowing (6, 7). This bidirectional flow of information should also be a crucial feature of the neurobiological system that supports language processing. Linguistic processing is not a simple bottom-up process where incoming linguistic information (for instance, when reading a sentence) drives a sequence of activations of cortical areas that gradually transforms a string of letters into a representation of sentence and discourse meaning. Rather, contextual information, which is either already available, or built up while a sentence unfolds, can also provide top-down information, affecting the response in lower-order areas.Here, we show that interregional interactions in the human brain network for language are subserved by rhyt...

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