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Spatiotemporal dynamics of orthographic and lexical processing in the ventral visual pathway

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Abstract

Reading is a rapid, distributed process that engages multiple components of the ventral visual stream. To understand the neural constituents and their interactions that allow us to identify written words, we performed direct intra-cranial recordings in a large cohort of humans. This allowed us to isolate the spatiotemporal dynamics of visual word recognition across the entire left ventral occipitotemporal cortex. We found that mid-fusiform cortex is the first brain region sensitive to lexicality, preceding the traditional visual word form area. The magnitude and duration of its activation are driven by the statistics of natural language. Information regarding lexicality and word frequency propagates posteriorly from this region to visual word form regions and to earlier visual cortex, which, while active earlier, show sensitivity to words later. Further, direct electrical stimulation of this region results in reading arrest, further illustrating its crucial role in reading. This unique sensitivity of mid-fusiform cortex to sub-lexical and lexical characteristics points to its central role as the orthographic lexicon—the long-term memory representations of visual word forms.

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Fig. 1: Experimental design of the passive viewing and sentence reading tasks.
Fig. 2: Population activation map and single-participant activations.
Fig. 3: Spatial mapping of selectivity to hierarchical orthographic stimuli.
Fig. 4: Spatiotemporal map of word frequency and lexicality effects during sentence reading.
Fig. 5: Anteroposterior differences in the timing of frequency and lexicality effects.
Fig. 6: Cortical stimulation mapping (CSM) of reading.

Data availability

The datasets generated from this research are not publicly available due to their containing information non-compliant with HIPAA, and the human participants from whom the data were collected have not consented to their public release. However, they are available on request from the corresponding author.

Code availability

The custom code that supports the findings of this study is available from the corresponding author on request.

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Acknowledgements

The authors thank Y. Wang for assistance coordinating participant data transfers and E. Klier for comments on previous versions of this manuscript. We thank all the individuals who participated in this study, the neurologists at the Texas Comprehensive Epilepsy Program who participated in the care of these people and all the nurses and technicians in the Epilepsy Monitoring Unit at Memorial Hermann Hospital who helped make this research possible. This work was supported by the National Institute of Neurological Disorders and Stroke and the National Institute on Deafness and Communicable Disorders via the BRAIN initiative ‘Research on Humans’ grant NS098981. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Authors and Affiliations

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Contributions

Conceptualization: O.W., N.T. and S.D.; Methodology: O.W., C.D., N.T. and S.D.; Data curation: O.W., C.D., P.S.R. and N.E.C.; Software: O.W., K.J.F. and C.D.; Formal analysis: O.W.; Writing – original draft: O.W.; Writing – review and editing: O.W.,. N.T., S.F.B., Y.L. and S.D.; Visualization: O.W.; Supervision: N.T.; Project administration: N.T.; Funding acquisition: N.T.

Corresponding author

Correspondence to Nitin Tandon.

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Extended data

Extended Data Fig. 1 Lateralization of word-responsive electrodes in ventral cortex.

Map of word responsive (yellow; activation >20% above baseline) and unresponsive (red) electrodes in the passive viewing (a; 27 patients) and sentence (b; 28 patients) tasks. In the non-dominant right hemisphere (14 patients), word responses were confined to occipital cortex.

Extended Data Fig. 2 Spatiotemporal mapping of selectivity to hierarchical orthographic stimuli.

Word-amplitude normalized selectivity profiles grouped in 20 mm intervals along the y (antero-posterior) axis in Talairach space for three consecutive time windows (20 patients). Within each time window, electrodes with >20% activation above baseline in response to words were utilized. Averaged within patient. Standard errors represent between patient variability. Individual data points are overlaid. Horizontal dashed lines represent word response.

Extended Data Fig. 3 Lexical and Sub-Lexical Frequency Effects in Mid-Fusiform Cortex.

a, Mid-fusiform responses to real words from the word list condition separated by word frequency and length (49 electrodes, 15 patients). b, Pseudoword responses in mid-fusiform cortex from the Jabberwocky condition separated by bigram frequency (BGF) and word length (49 electrodes, 15 patients).

Extended Data Fig. 4 Timing of the selectivity to hierarchical orthographic stimuli in the passive viewing task.

a, Temporal representations of the two archetypal components generated from NNMF of the z-scores of words against each non-word condition. b, Spatial map of the NNMF decompositions of the z-score word selectivity (207 electrodes, 20 patients). c, Spatiotemporal representation of word vs non-word selectivity (non-word normalized to word activity) for each of the letter-form conditions. Electrode selectivity profiles were grouped every 20 mm along the antero-posterior axis in Talairach space. Each condition shows an anterior-to-posterior spread of word selectivity (red). FF: False Font, IL: Infrequent Letters, FL: Frequent Letters, BG: Frequent Bigrams, QG: Frequent Quadrigrams.

Supplementary information

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Supplementary Video 1

Spatiotemporal map of lexical sensitivity in ventral visual cortex. MEMA activation video showing the regions of significant activation to the real word (W; left) stimuli and infrequent letter (IL; middle) stimuli (27 patients). The word normalized amplitude map (right) shows regions with preferential activation to words (red) or infrequent letters (blue)

Supplementary Video 2

Spatiotemporal map of sensitivity to sub-lexical structure in ventral visual cortex. MEMA video showing word-normalized activation amplitudes for each of the non-word conditions from the sub-lexical task, demonstrating regions with preferential activation to words (red) or non-words (blue) (27 patients). FF, false font; IL, infrequent letters; FL, frequent letters; BG, frequent bigrams; QG, frequent quadrigrams

Supplementary Video 3

Cortical stimulation mapping (CSM) of mid-fusiform cortex and lateral occipitotemporal gyrus. CSM session for TA774B showing stimulation of either site results in selective deficits in word reading with no associated naming or speech production deficits. Transcriptions are of the presented reading stimuli. Recording provided with patient’s consent

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Woolnough, O., Donos, C., Rollo, P.S. et al. Spatiotemporal dynamics of orthographic and lexical processing in the ventral visual pathway. Nat Hum Behav 5, 389–398 (2021). https://doi.org/10.1038/s41562-020-00982-w

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