Individual word representations dissociate from linguistic context along a cortical unimodal to heteromodal gradient.

Language comprehension involves multiple hierarchical processing stages across time, space, and levels of representation. When processing a word, the sensory input is transformed into increasingly abstract representations that need to be integrated with the linguistic context. Thus, language comprehension involves both input-driven as well as context-dependent processes. While neuroimaging research has traditionally focused on mapping individual brain regions to the distinct underlying processes, recent studies indicate that whole-brain distributed patterns of cortical activation might be highly relevant for cognitive functions, including language. One such pattern, based on resting-state connectivity, is the 'principal cortical gradient', which dissociates sensory from heteromodal brain regions. The present study investigated the extent to which this gradient provides an organizational principle underlying language function, using a multimodal neuroimaging dataset of functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) recordings from 102 participants during sentence reading. We found that the brain response to individual representations of a word (word length, orthographic distance, and word frequency), which reflect visual; orthographic; and lexical properties, gradually increases towards the sensory end of the gradient. Although these properties showed opposite effect directions in fMRI and MEG, their association with the sensory end of the gradient was consistent across both neuroimaging modalities. In contrast, MEG revealed that properties reflecting a word's relation to its linguistic context (semantic similarity and position within the sentence) involve the heteromodal end of the gradient to a stronger extent. This dissociation between individual word and contextual properties was stable across earlier and later time windows during word presentation, indicating interactive processing of word representations and linguistic context at opposing ends of the principal gradient. To conclude, our findings indicate that the principal gradient underlies the organization of a range of linguistic representations while supporting a gradual distinction between context-independent and context-dependent representations. Furthermore, the gradient reveals convergent patterns across neuroimaging modalities (similar location along the gradient) in the presence of divergent responses (opposite effect directions).

The lexical categorization model: A computational model of left ventral occipito-temporal cortex activation in visual word recognition.

To characterize the functional role of the left-ventral occipito-temporal cortex (lvOT) during reading in a quantitatively explicit and testable manner, we propose the lexical categorization model (LCM). The LCM assumes that lvOT optimizes linguistic processing by allowing fast meaning access when words are familiar and filtering out orthographic strings without meaning. The LCM successfully simulates benchmark results from functional brain imaging described in the literature. In a second evaluation, we empirically demonstrate that quantitative LCM simulations predict lvOT activation better than alternative models across three functional magnetic resonance imaging studies. We found that word-likeness, assumed as input into a lexical categorization process, is represented posteriorly to lvOT, whereas a dichotomous word/non-word output of the LCM could be localized to the downstream frontal brain regions. Finally, training the process of lexical categorization resulted in more efficient reading. In sum, we propose that word recognition in the ventral visual stream involves word-likeness extraction followed by lexical categorization before one can access word meaning.

Predictive pre-activation of orthographic and lexical-semantic representations facilitates visual word recognition.

To a crucial extent, the efficiency of reading results from the fact that visual word recognition is faster in predictive contexts. Predictive coding models suggest that this facilitation results from pre-activation of predictable stimulus features across multiple representational levels before stimulus onset. Still, it is not sufficiently understood which aspects of the rich set of linguistic representations that are activated during reading-visual, orthographic, phonological, and/or lexical-semantic-contribute to context-dependent facilitation. To investigate in detail which linguistic representations are pre-activated in a predictive context and how they affect subsequent stimulus processing, we combined a well-controlled repetition priming paradigm, including words and pseudowords (i.e., pronounceable nonwords), with behavioral and magnetoencephalography measurements. For statistical analysis, we used linear mixed modeling, which we found had a higher statistical power compared to conventional multivariate pattern decoding analysis. Behavioral data from 49 participants indicate that word predictability (i.e., context present vs. absent) facilitated orthographic and lexical-semantic, but not visual or phonological processes. Magnetoencephalography data from 38 participants show sustained activation of orthographic and lexical-semantic representations in the interval before processing the predicted stimulus, suggesting selective pre-activation at multiple levels of linguistic representation as proposed by predictive coding. However, we found more robust lexical-semantic representations when processing predictable in contrast to unpredictable letter strings, and pre-activation effects mainly resembled brain responses elicited when processing the expected letter string. This finding suggests that pre-activation did not result in "explaining away" predictable stimulus features, but rather in a "sharpening" of brain responses involved in word processing.

Context-Based Facilitation in Visual Word Recognition: Evidence for Visual and Lexical But Not Pre-Lexical Contributions.

Word familiarity and predictive context facilitate visual word processing, leading to faster recognition times and reduced neuronal responses. Previously, models with and without top-down connections, including lexical-semantic, pre-lexical (e.g., orthographic/phonological), and visual processing levels were successful in accounting for these facilitation effects. Here we systematically assessed context-based facilitation with a repetition priming task and explicitly dissociated pre-lexical and lexical processing levels using a pseudoword (PW) familiarization procedure. Experiment 1 investigated the temporal dynamics of neuronal facilitation effects with magnetoencephalography (MEG; N = 38 human participants), while experiment 2 assessed behavioral facilitation effects (N = 24 human participants). Across all stimulus conditions, MEG demonstrated context-based facilitation across multiple time windows starting at 100 ms, in occipital brain areas. This finding indicates context-based facilitation at an early visual processing level. In both experiments, we furthermore found an interaction of context and lexical familiarity, such that stimuli with associated meaning showed the strongest context-dependent facilitation in brain activation and behavior. Using MEG, this facilitation effect could be localized to the left anterior temporal lobe at around 400 ms, indicating within-level (i.e., exclusively lexical-semantic) facilitation but no top-down effects on earlier processing stages. Increased pre-lexical familiarity (in PWs familiarized utilizing training) did not enhance or reduce context effects significantly. We conclude that context-based facilitation is achieved within visual and lexical processing levels. Finally, by testing alternative hypotheses derived from mechanistic accounts of repetition suppression, we suggest that the facilitatory context effects found here are implemented using a predictive coding mechanism.