Reading words aloud is a foundational aspect of the acquisition of literacy. The rapid rate at which multiple distributed neural substrates are engaged in this process can only be probed via techniques with high spatiotemporal resolution. We used direct intracranial recordings in a large cohort to create a holistic yet fine-grained map of word processing, enabling us to derive the spatiotemporal neural codes of multiple word attributes critical to reading: lexicality, word frequency and orthographic neighborhood. We found that lexicality is encoded by early activity in mid-fusiform (mFus) cortex and precentral sulcus. Word frequency is also first represented in mFus followed by later engagement of the inferior frontal gyrus (IFG) and inferior parietal sulcus (IPS), and orthographic neighborhood is encoded solely in the IPS. A lexicality decoder revealed high weightings for electrodes in the mFus, IPS, anterior IFG and the pre-central sulcus. These results elaborate the neural codes underpinning extant dual-route models of reading, with parallel processing via the lexical route, progressing from mFus to IFG, and the sub-lexical route, progressing from IPS to anterior IFG.

The ability to comprehend meaningful phrases is an essential component of language. Here we evaluate a minimal compositional scheme – the ‘red-boat’ paradigm – using intracranial recordings to map the process of semantic composition in phrase structure comprehension. 18 human participants, implanted with penetrating depth or surface subdural intracranial electrode for the evaluation of medically refractory epilepsy, were presented with auditory recordings of adjective-noun, pseudoword-noun and adjective-pseudoword phrases before being presented with a colored drawing, and were asked to judge whether the phrase matched the object presented. Significantly greater broadband gamma activity (70-150Hz) occurred in temporo-occipital junction (TOJ) and posterior middle temporal gyrus (pMTG) for pseudowords over words (300-700ms post-onset) in both first- and second-word positions. Greater inter-trial phase coherence (8-12Hz) was found for words than for pseudowords in posterior superior temporal gyrus (pSTG). Isolating phrase structure sensitivity, we identified a portion of TOJ and posterior superior temporal sulcus (pSTS) that showed increased gamma activity for phrase composition than for non-composition, while left anterior temporal lobe (ATL) showed greater low frequency (2-15Hz) activity for phrase composition, likely coordinating distributed semantic representations. Greater functional connectivity between pSTS-TOJ and pars triangularis, and between pSTS-TOJ and ATL, was also found for phrase composition. STG, ATL and pars triangularis were found to encode anticipation of composition in the beta band (15-30Hz), and alpha (8-12Hz) power increases in ATL were also linked to anticipation. These results indicate that pSTS-TOJ appears to be crucial hub in the network responsible for the retrieval and computation of minimal phrases, and that anticipation of such composition is encoded in fronto-temporal regions.