The entire brain, more or less, is at work: 'Language regions' are artefacts of averaging

Abstract

Models of the neurobiology of language suggest that a small number of anatomically fixed brain regions are responsible for language functioning. This derives from centuries of aphasia studies and decades of neuroimaging. The latter rely on thresholded measures of central tendency applied to activity patterns from heterogeneous stimuli. We hypothesised that these methods obscure the whole brain distribution of regions supporting language. Specifically, language regions are connectivity hubs, coordinating varying peripheral activity that averages out following thresholding. We tested this with neuroimaging meta-analyses and movie-fMRI. Results show that words localise to language regions when averaged but are distributed throughout the brain when examining specific linguistic representations. These language regions are partially connectivity hubs that are spatiotemporally dynamic, making connections with [~]40% of the brain periphery outside those regions, and only appearing in the aggregate over time. Hub-periphery connections encode linguistic representations, not the language regions alone. Results replicate with audiobook-fMRI. Finally, intracranial neuronal recordings support findings, showing language regions are hub-like, with linguistic representations decodable throughout the brain. Together, these four studies suggest that language regions are artefacts of averaging heterogeneous language representations. Instead, they are connectivity hubs coordinating whole-brain distributed network representations, suggesting why their damage results in aphasia.