Top-down processing of symbolic meanings modulates the visual word form area

Abstract

Functional magnetic resonance imaging (fMRI) studies on humans have identified a region in the left middle fusiform gyrus consistently activated by written words. This region is called the visual word form area (VWFA). Recently, a hypothesis, called the interactive account, is proposed that to effectively analyze the bottom-up visual properties of words, the VWFA receives predictive feedback from higher-order regions engaged in processing sounds, meanings, or actions associated with words. Further, this top-down influence on the VWFA is independent of stimulus formats. To test this hypothesis, we used fMRI to examine whether a symbolic nonword object (e.g., the Eiffel Tower) intended to represent something other than itself (i.e., Paris) could activate the VWFA. We found that scenes associated with symbolic meanings elicited a higher VWFA response than those not associated with symbolic meanings, and such top-down modulation on the VWFA can be established through short-term associative learning, even across modalities. In addition, the magnitude of the symbolic effect observed in the VWFA was positively correlated with the subjective experience on the strength of symbol-referent association across individuals. Therefore, the VWFA is likely a neural substrate for the interaction of the top-down processing of symbolic meanings with the analysis of bottom-up visual properties of sensory inputs, making the VWFA the location where the symbolic meaning of both words and nonword objects is represented.

Figure 1.

Example stimuli for each stimulus condition in Experiment 1.

Figure 2.

The symbolic effect in the VWFA. A, The response magnitudes for symbolic scenes and nonsymbolic scenes in the VWFA and PPA. y-axis indicates the percentage BOLD signal change, and error bars indicate ±1 SEM. B, The correlation between the VWFA response to the symbolic scenes versus nonsymbolic scenes (VWFA symbolic effect) and the subjective experiences on the strength of symbolic meanings of the symbolic scenes versus nonsymbolic scenes (behavioral symbolic effect) across the participants. x-axis is the t value by comparing VWFA response to the symbolic scenes with the nonsymbolic scenes, whereas y-axis is the normalized difference in subjective evaluation of the strength of symbol–referent association in two types of scenes in a seven-point Likert scale. C, The response magnitude for symbolic scenes, nonsymbolic scenes, images of chairs, and Chinese characters in the VWFA. y-axis indicates the percentage BOLD signal change, and error bars indicate ±1 SEM.

Figure 3.

Associative experience in establishing the top-down influence on the VWFA. A, Four dumbbell-shaped exemplars for the Trained, Variant, and Novel stimuli respectively in fMRI scans in Experiment 2. Note that the Variant condition contains the same part components as those in the Trained condition, whereas their configurations are different. B, Behavioral results in associative learning. The accuracies and reaction times are shown as functions of training sessions. The left y-axis indicates the reaction time in making a correct action after seeing a dumbbell-shaped object, whereas the right y-axis indicates the percentage of correct responses in associative learning at the chance level of 50%. C, The response magnitudes for the Trained (i.e., symbolic) and Novel (i.e., nonsymbolic) stimuli in the VWFA and LO. D, The response magnitude for the variants of the trained stimuli (Variant) compared with the magnitude for the Trained and Novel condition respectively in the VWFA. y-axis indicates the percentage BOLD signal change, and error bars indicate ±1 SEM.