Early Top-Down Modulation in Visual Word Form Processing: Evidence From an Intracranial SEEG Study

Visual word recognition, at a minimum, involves the processing of word form and lexical information. Opinions diverge on the spatiotemporal distribution of and interaction between the two types of information. Feedforward theory argues that they are processed sequentially, whereas interactive theory advocates that lexical information is processed fast and modulates early word form processing. To distinguish between the two theories, we applied stereoelectroencephalography (SEEG) to 33 human adults with epilepsy (25 males and eight females) during visual lexical decisions. The stimuli included real words (RWs), pseudowords (PWs) with legal radical positions, nonwords (NWs) with illegal radical positions, and stroked-changed words (SWs) in Chinese. Word form and lexical processing were measured by the word form effect (PW versus NW) and lexical effect (RW versus PW), respectively. Gamma-band (60 ∼ 140 Hz) SEEG activity was treated as an electrophysiological measure. A word form effect was found in eight left brain regions (i.e., the inferior parietal lobe, insula, fusiform, inferior temporal, middle temporal, middle occipital, precentral and postcentral gyri) from 50 ms poststimulus onset, whereas a lexical effect was observed in five left brain regions (i.e., the calcarine, middle temporal, superior temporal, precentral, and postcentral gyri) from 100 ms poststimulus onset. The two effects overlapped in the precentral (300 ∼ 500 ms) and postcentral (100 ∼ 200 ms and 250 ∼ 600 ms) gyri. Moreover, high-level regions provide early feedback to word form regions. These results demonstrate that lexical processing occurs early and modulates word form recognition, providing vital supportive evidence for interactive theory.SIGNIFICANCE STATEMENT A pivotal unresolved dispute in the field of word processing is whether word form recognition is obligatorily modulated by high-level lexical top-down information. To address this issue, we applied intracranial SEEG to 33 adults with epilepsy to precisely delineate the spatiotemporal dynamics between processing word form and lexical information during visual word recognition. We observed that lexical processing occurred from 100 ms poststimulus presentation and even spatiotemporally overlapped with word form processing. Moreover, the high-order regions provided feedback to the word form regions in the early stage of word recognition. These results revealed the crucial role of high-level lexical information in word form recognition, deepening our understanding of the functional coupling among brain regions in word processing networks.