Decoding and disrupting left midfusiform gyrus activity during word reading

Abstract

The nature of the visual representation for words has been fiercely debated for over 150 y. We used direct brain stimulation, pre- and postsurgical behavioral measures, and intracranial electroencephalography to provide support for, and elaborate upon, the visual word form hypothesis. This hypothesis states that activity in the left midfusiform gyrus (lmFG) reflects visually organized information about words and word parts. In patients with electrodes placed directly in their lmFG, we found that disrupting lmFG activity through stimulation, and later surgical resection in one of the patients, led to impaired perception of whole words and letters. Furthermore, using machine-learning methods to analyze the electrophysiological data from these electrodes, we found that information contained in early lmFG activity was consistent with an orthographic similarity space. Finally, the lmFG contributed to at least two distinguishable stages of word processing, an early stage that reflects gist-level visual representation sensitive to orthographic statistics, and a later stage that reflects more precise representation sufficient for the individuation of orthographic word forms. These results provide strong support for the visual word form hypothesis and demonstrate that across time the lmFG is involved in multiple stages of orthographic representation.

Keywords: electrical stimulation; fusiform gyrus; intracranial EEG; temporal dynamics; word reading.

Fig. 1.

Location of implanted electrode. Individual electrode contacts are visible on axial (A, C, and E) and coronal (B, D, and F) views and cortical reconstruction (G) of the postimplantation MRI (P1: A and B; P2: C and D; P3: E and F; P4: G). The VT depth electrodes were placed at the anterior end of the midfusiform sulcus in P1–P3 (yellow arrow), and P4 was implanted with a left temporal subdural grid crossing the lmFG. Red arrowheads (A–F) and red filled circles (G) indicate the word-selective contacts identified in the category localizer, which were used in subsequent electrophysiological and/or stimulation experiments. Talairach coordinates (x, y, z) corresponding to the word-selective contacts were located in postoperative MRI structural images, and were all identified in the left fusiform gyrus, BA 37 (P1 electrodes: −31, −36, −13; −35, −37, −13; −39, −38, −12; P2 electrodes: −30, −46, −11; −34, 6, −12; P3 electrodes: −31, −35, −14; P4 electrodes: −38, −51, −21; −41, −50, −22; −41, −54, −20).

Fig. 2.

Verification of orthographic selectivity at lmFG electrode site. (A) Example of averaged ERP across lmFG electrodes in one of the participants (P1) for three different stimulus categories (bodies, words, and nonobjects). The colored areas indicate SEs. (B) Averaged ERP across all lmFG electrodes and across all of the participants for three different stimulus categories (bodies, words, and nonobjects). The colored areas indicate SEs. (C) Time course of word categorical sensitivity in lmFG electrodes measured by sensitivity index d′ (mean d′ plotted against the beginning of the 100-ms sliding window), averaged across three participants. The MTPA classifier uses time-windowed single-trial potential signal from the electrodes from each subject (window length = 100 ms) with each time point in the window from each electrode as multivariate input features (see Methods for details). Across-participant SEs are shaded gray. See Figs. S1–S4 for single-electrode word categorical sensitivity.

Fig. S1.

Time course of word categorical sensitivity in each single electrode of P1 measured by sensitivity index d′ (mean d′ plotted against the beginning of the 100-ms sliding window). The classifier uses time-windowed ERP signal from a single electrode (window length = 100 ms) as input features (see Methods for details). SEs of cross-validations are shaded gray. Horizontal red line indicates significance threshold. Horizontal gray line indicates chance level (d′ = 0). Electrodes 1–3 were the contact of interest for further analysis in P1.

Fig. S2.

Time course of word categorical sensitivity in each single electrode of P2 measured by sensitivity index d′ (mean d′ plotted against the beginning of the 100-ms sliding window). The classifier uses time-windowed ERP signal from a single electrode (window length = 100 ms) as input features (see Methods for details). SEs of cross-validations are shaded gray. Horizontal red line indicates significance threshold. Horizontal gray line indicates chance level (d′ = 0). Electrodes 3 and 4 were the contact of interest for further analysis in P2 because electrode 1 was noncontiguous with the other word-sensitive electrodes and medial to the fusiform.

Fig. S3.

Time course of word categorical sensitivity in each single electrode in P3 measured by sensitivity index d′ (mean d′ plotted against the beginning of the 100-ms sliding window). The classifier uses time-windowed ERP signal from a single electrode (window length = 100 ms) as input features (see Methods for details). SEs of cross-validations are shaded gray. Horizontal red line indicates significance threshold. Horizontal gray line indicates chance level (d′ = 0). Electrode 3 was the contact of interest for further analysis in P3.

Fig. S4.

Time course of word categorical sensitivity in each single electrode in P4 measured by sensitivity index d′ (mean d′ plotted against the beginning of the 100-ms sliding window). The classifier uses time-windowed ERP signal from a single electrode (window length = 100 ms) as input features (see Methods for details). Horizontal red line indicates significance threshold. Horizontal gray line indicates chance level (d′ = 0). A high-density electrode strip was used in P4. This strip contained two rows of 14 electrode contacts and thus the electrodes of interest, 8, 9, and 22 were next to each other. Other electrodes were either substantially medial to the fusiform (1–5, 15–19) or the classification accuracy was a result of stronger activity for the nonword control stimuli (7, 10–12, 20, 21, 23–25).

Fig. 3.

The effect of stimulation on naming times in lmFG and pre- and postsurgery neuropsychological naming task performance. (A) The average naming reaction time for words, letters, and faces under low stimulation (1–5 mA) and high stimulation (6–10 mA) to lmFG electrodes in P1. Error bars correspond to SE, *P < 0.05. (B) The average naming reaction time for words and pictures under low stimulation (1–5 mA) and high stimulation (6–10 mA) to lmFG electrodes in P2. Error bars correspond to SE, ***P < 0.001. (C) Word length effect pre- and postsurgery in P1. (D) Average percent change in reaction time in the mixed naming task pre- vs. postsurgery in P1, ***P < 0.001.

Fig. S5.

P1 resection location. The former location of the same depth electrode (red line) is indicated on coregistered views of the postoperative MRI (A and B) in relation to the cortical regions that were resected (blue region).

Fig. S6.

P1 performance on neuropsychological tests. Visual word recognition (mean number of correctly named words in TOWRE sight word and phonemic decoding efficiency; presurgery: form A; postsurgery: form B) and phonological awareness (mean correct trials in CTOPP elision and blending words) were measured pre- and postsurgery (6 wk and 3 mo). P1’s postsurgery performance on a standardized test of visual word recognition (40) decreased to a greater extent compared with a test of phonological awareness, which remained stable after surgery (41) (Fig. S5); this suggests that P1’s resection disrupted orthographic, but not phonological processes.

Fig. 4.

Dynamics of sensitivity to sublexical orthographic statistics (bigram frequency) in the lmFG. Classification accuracy time course for comparison between low-bigram frequency real words (low BG) vs. high-bigram frequency real words (high BG) in lmFG electrodes for P1 and P4, respectively, plotted against the beginning of the 100-ms sliding window. The classifier uses time-windowed single-trial potential signal from the electrodes from each subject (window length = 100 ms) with each time point in the window from each electrode as multivariate input features (see Methods for details). The asterisk (*) corresponds to the peak of the windows in which P < 0.05 corrected for multiple comparisons. The P = 0.05 significance threshold corresponds to accuracy = 58.2% (P1) and 59.3% (P4). The horizontal gray line at 50% indicates chance level.

Fig. 5.

Dynamics of word individuation selectivity in the lmFG. Dynamics of averaged pairwise word individuation accuracy for different conditions in lmFG electrodes for P1, P3, and P4, respectively, plotted against the beginning of the 100-ms sliding window. The classifier uses time-windowed single-trial potential signal from the electrodes from each subject (window length = 100 ms) with each time point in the window from each electrode as multivariate input features (see Methods for details). The time course of the accuracy is averaged across all word pairs of the corresponding conditions. The colored areas indicate SEs. Similar pair: a pair of words that have the same length and are only different in one letter, e.g., lint and hint. Different pair: a pair of words that have the same length and are different in all letters, e.g., lint and dome. Horizontal gray line indicates chance level (accuracy = 50%). Colored asterisk (*) corresponds to the peak of the windows in which P < 0.05 corrected for multiple comparisons. The P = 0.05 significance threshold corresponds to accuracy = 56.5% (P1), 56.0% (P3), and 57.1% (P4).