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
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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)