Functional Network Dynamics of the Language System

Cerebral Cortex, Oct 2016

During linguistic processing, a set of brain regions on the lateral surfaces of the left frontal, temporal, and parietal cortices exhibit robust responses. These areas display highly correlated activity while a subject rests or performs a naturalistic language comprehension task, suggesting that they form an integrated functional system. Evidence suggests that this system is spatially and functionally distinct from other systems that support high-level cognition in humans. Yet, how different regions within this system might be recruited dynamically during task performance is not well understood. Here we use network methods, applied to fMRI data collected from 22 human subjects performing a language comprehension task, to reveal the dynamic nature of the language system. We observe the presence of a stable core of brain regions, predominantly located in the left hemisphere, that consistently coactivate with one another. We also observe the presence of a more flexible periphery of brain regions, predominantly located in the right hemisphere, that coactivate with different regions at different times. However, the language functional ROIs in the angular gyrus and the anterior temporal lobe were notable exceptions to this trend. By highlighting the temporal dimension of language processing, these results suggest a trade-off between a region's specialization and its capacity for flexible network reconfiguration.

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Functional Network Dynamics of the Language System

Functional Network Dynamics of the Language System Lucy R. Chai 2 Marcelo G. Mattar 1 2 Idan Asher Blank 0 5 Evelina Fedorenko 0 4 5 Danielle S. Bassett 2 3 0 Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology , Cambridge, MA 02139 , USA 1 Department of Psychology, University of Pennsylvania , Philadelphia, PA 19104 , USA 2 Department of Bioengineering, University of Pennsylvania , Philadelphia, PA 19104 , USA 3 Department of Electrical & Systems Engineering, University of Pennsylvania , Philadelphia, PA 19104 , USA 4 Department of Psychiatry, Massachusetts General Hospital , Charlestown, MA 02129 , USA 5 Department of Psychiatry, Harvard Medical School , Boston, MA, 02115 , USA During linguistic processing, a set of brain regions on the lateral surfaces of the left frontal, temporal, and parietal cortices exhibit robust responses. These areas display highly correlated activity while a subject rests or performs a naturalistic language comprehension task, suggesting that they form an integrated functional system. Evidence suggests that this system is spatially and functionally distinct from other systems that support high-level cognition in humans. Yet, how different regions within this system might be recruited dynamically during task performance is not well understood. Here we use network methods, applied to fMRI data collected from 22 human subjects performing a language comprehension task, to reveal the dynamic nature of the language system. We observe the presence of a stable core of brain regions, predominantly located in the left hemisphere, that consistently coactivate with one another. We also observe the presence of a more flexible periphery of brain regions, predominantly located in the right hemisphere, that coactivate with different regions at different times. However, the language functional ROIs in the angular gyrus and the anterior temporal lobe were notable exceptions to this trend. By highlighting the temporal dimension of language processing, these results suggest a trade-off between a region's specialization and its capacity for flexible network reconfiguration. angular gyrus; dynamic networks; flexibility; language; language comprehension; lateralization; modularity; networks - High-level language processing recruits an extended set of cortical regions in the human brain (Blank et al. 2014; Tie et al. 2014) that are distinct from those recruited for other cognitive functions (Fedorenko et al. 2011; Blank et al. 2014). In the earliest reports of brain damaged patients with language deficits, only a few of those regions were initially identified (Dax 1865; Broca 1861; Wernicke 1874). More recent work in functional neuroimaging has extended these findings by revealing the breadth of the language system’s spatial distribution, which is now thought to span the frontal, temporal, and parietal cortices (Binder et al. 1997; Fedorenko and Thompson-Schill 2014) (see Luria (1965); Mesulam (1990) for early discussions). Furthermore, the distributed nature of brain regions that support language processing has been observed not only in task-based studies (Binney et al. 2010; Fedorenko et al. 2010; Binney and Ralph 2015), but also during naturalistic cognition paradigms (Tomasi and Volkow 2012; Muller and Meyer 2014; Zhu et al. 2014). This distributed system displays some degree of hemispheric lateralization. Indeed, evidence from dichotic listening paradigms (Kimura 1961), the Wada test (Woermann et al. 2003; Janecek et al. 2013), aphasia (Dax 1865), and split-brain patients (Gazzaniga 2005) point to a left-hemisphere (LH) dominance of language processing that is supported by neuroimaging studies (Springer et al. 1999; Woermann et al. 2003; Janecek et al. 2013). Yet, imaging studies have also reported activations in the right-hemisphere (RH) homologs of the left-hemisphere language regions for a variety of language tasks, suggesting that the right hemisphere also plays some role in language processing (Binder et al. 1997; Fedorenko et al. 2010; Price 2012). Despite the evidence for bilateral involvement, our understanding of the relative contributions of left vs. right hemisphere brain regions, and the dynamics of their within vs. between-hemisphere interactions, remains limited. One recent and potentially useful theoretical framework focuses on the fact that functional interactions between brain regions plausibly change over time, and suggests that patterns of inter-regional communication may determine the degree of any given region’s functional specialization. In particular, regions that are only transiently engaged during linguistic processing may support domain-general processes (Bassett et al. 2013b), whereas regions that are stably engaged may support processes that are specific to the language domain (Fedorenko and Thompson-Schill 2014). We build on this general notion to posit that lateralization may reflect differences between left and right hemisphere re (...truncated)


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Lucy R. Chai, Marcelo G. Mattar, Idan Asher Blank, Evelina Fedorenko, Danielle S. Bassett. Functional Network Dynamics of the Language System, Cerebral Cortex, 2016, pp. 4148-4159, 26/11, DOI: 10.1093/cercor/bhw238