Voluntary effort to read reshapes stimulus selectivity in the visual word form area and increases its communication with the language network

Abstract

Reading depends on a brain region known as the "visual word form area" (VWFA) in left ventral occipito-temporal cortex. This regions function is debated because its stimulus selectivity is not absolute, it is modulated by a variety of task demands, and it is inconsistently localized. We used fMRI to characterize the combination of sensory and cognitive factors that activate word-responsive regions that we precisely localized in 16 adult humans (4 male). We then presented three types of character strings: English words, pseudowords, and unfamiliar characters with matched visual features. Participants performed three different tasks while viewing those stimuli: detecting real words, detecting color in the characters, and detecting color in the fixation mark. There were three primary findings about the VWFAs response: (1) It preferred letter strings over unfamiliar characters even when the stimuli were ignored during the fixation task; (2) Compared to those baseline responses, engaging in the word reading task enhanced the response to words but suppressed the response to unfamiliar characters. (3) Attending to the stimuli to judge their font color had little effect on the response magnitudes. Thus, the VWFA is uniquely modulated by a cognitive signal that is specific to voluntary linguistic processing and is not additive. Functional connectivity analyses revealed that communication between the VWFA and a left frontal language area increased when the participant engaged in the linguistic task. We conclude that the VWFA is inherently selective for familiar orthography, but it falls under control of the language network when the task demands it. Significance StatementThe function of the "visual word form area" (VWFA) is controversial. Some researchers emphasize its bottom-up visual selectivity for words, hence the regions common name. Others argue that its activity is explained by feedback from regions that control attention or language. To seek clarity, we investigated what drives the VWFA: seeing words, attending visually to words, or trying to read words. None of those factors was sufficient on its own. Our results support a hybrid model: the VWFA has inherent selectivity for words, but its function is reshaped by voluntary language processing. Thus, with an integrated analysis of sensory inputs, task demands, and network connectivity, we provide some resolution to debates about this important region.