Triangulating the neural cornerstones of reading: Within-participant double dissociations induced by direct cortical stimulation
Daifu-Kobayashi, M.; Shimotake, A.; Ota, M.; Sakamoto, M.; Kobayashi, K.; Kikuchi, T.; Yoshida, K.; Kunieda, T.; Miyamoto, S.; Takahashi, R.; Ikeda, A.; Ralph, M. A. L.; Matsumoto, R.
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How does the human brain recognize a written word and read it aloud? The "triangle" neurocognitive model proposes that reading is founded on three cognitive systems: visual-orthography, phonology and semantics. We tested this theory via a unique opportunity to generate transient double dissociations within the same patient via direct cortical stimulation to contrastive regions. Five patients with intractable temporal lobe epilepsy who underwent presurgical evaluation with subdural electrode were included. Reading of kanji words, with three levels of spelling-to-sound consistency level, and kana non-words with 2 to 5 mora, was examined. Low-intensity electrical stimulation was applied to the anterior basal temporal language area (BTLA) (<6 cm from the temporal pole, all patients), posterior BTLA (>6 cm, in four patients) and supramarginal gyrus (SMG, one patient). Electrical or sham stimulation was delivered time-locked to the presentation of each word, and the reaction time (RT) was evaluated. One double dissociation was generated by contrastive SMG (phonological alexia; poor non-word reading) vs. anterior BTLA stimulation (surface dyslexia; poor kanji reading). A different double dissociation was elicited following anterior vs. posterior BTLA stimulation with the former showing effects of kanji consistency level as expected in surface dyslexia, and the latter with length effects as expected in a pure alexia. In conclusion, going beyond classic lesion studies, we were uniquely able to demonstrate the double dissociations within the same patient on a transient reversible basis. Consistent with the triangle model of reading, three different reading disorders were elicited following low-intensity stimulation to each primary cognitive system.
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