Modality independence of word comprehension

Functional magnetic resonance imaging (fMRI) was used to examine the functional anatomy of word comprehension in the auditory and visual modalities of presentation. We asked our subjects to determine if word pairs were semantically associated (e.g., table, chair) and compared this to a reference task where they were asked to judge whether word pairs rhymed (e.g., bank, tank). This comparison showed task-specific and modality-independent activation for semantic processing in the heteromodal cortices of the left inferior frontal gyrus (BA 46, 47) and left middle temporal gyrus (BA 21). There were also modality-specific activations in the fusiform gyrus (BA 37) for written words and in the superior temporal gyrus (BA 22) for spoken words. Our findings are consistent with the hypothesis that word form recognition (lexical encoding) occurs in unimodal cortices and that heteromodal brain regions in the anterior as well as posterior components of the language network subserve word comprehension (semantic decoding).     

The neural substrates of visual perceptual learning of words: implications for the visual word form area hypothesis

Abstract It remains under debate whether the fusiform visual word form area (VWFA) is specific to visual word form and whether visual expertise increases its sensitivity (Xue et al., 2006; Cohen et al., 2002). The present study examined three related issues: (1) whether the VWFA is also involved in processing foreign writing that significantly differs from the native one, (2) the effect of visual word form training on VWFA activation after controlling the task difficulty, and (3) the transfer of visual word form learning. Eleven native English speakers were trained, during five sessions, to judge whether two subsequently flashed (100-msec duration with 200-msec interval) foreign characters (i.e., Korean Hangul) were identical or not. Visual noise was added to the stimuli to manipulate task difficulty. In functional magnetic resonance imaging scans before and after training, subjects performed the task once with the same noise level (i.e., parameter-matched scan) and once with noise level changed to match performance from pretraining to posttraining (i.e., performance-matched scan). Results indicated that training increased the accuracy in parameter-matched condition but remained constant in performance-matched condition (because of increasing task difficulty). Pretraining scans revealed stronger activation for English words than for Korean characters in the left inferior temporal gyrus and the left inferior frontal cortex, but not in the VWFA. Visual word form training significantly decreased the activation in the bilateral middle and left posterior fusiform when either parameters or performance were matched and for both trained and new items. These results confirm our conjecture that the VWFA is not dedicated to words, and visual expertise acquired with training reduces rather than increases its activity.     

The orthography-specific functions of the left fusiform gyrus: Evidence of modality and category specificity

We report on an investigation of the cognitive functions of an individual with a resection of the left fusiform gyrus. This individual and a group of control participants underwent testing to examine the question of whether or not there are neural substrates within the left fusiform gyrus that are dedicated to orthographic processing. We evaluated the modality specificity (written vs spoken language) and the category specificity (written language vs other visual categories) of this individual's impairments. The results clearly reveal deficits affecting lexical processes in both reading and spelling. Specifically, we find disruption of normal, rapid access to meaning from print in reading and of accurate retrieval of the spellings of words from their meaning in writing. These deficits stand in striking contrast with intact processing of spoken language and categories of visual stimuli such as line drawings of objects and faces. The modality and category specificity of the deficits provide clear evidence of neural substrates within the left-mid-fusiform gyrus that are specialized and necessary for normal orthographic processing.     

The inversion effect in visual word form processing

Reading is one of the best well-practiced visual tasks for modern people. We investigated how the visual cortex analyzes spatial configuration in written words by studying the inversion effect in Chinese character processing. We measured the psychometric functions and brain activations for upright real-characters and non-characters and their inverted (upside down) versions. In the psychophysical experiment, the real-characters showed an inversion effect at both 1° and 4° eccentricities, while the non-characters showed no inversion effect for all eccentricities tested. In the functional magnetic resonance image (fMRI) experiment, the left fusiform gyrus and a small area in the bilateral lateral occipital regions showed a significant differential activation between upright and inverted real-characters. The bilateral fusiform gyri also show differential activation between upright real- and non-characters. The dorsal lateral occipital regions showed character-selective activation when compared with scrambled lines. The result suggested that the occipitoparietal regions may analyze the local features of an object regardless of its familiarity. Therefore, the lateral occipital regions may play an intermediate role in integrating the local information in an object. Finally, the fusiform gyrus plays a critical role in analyzing global configurations of a visual word form. This is consistent with the notion that the human visual cortex analyzes an object in a hierarchical way.     

Relation between brain activation and lexical performance

Functional magnetic resonance imaging (fMRI) was used to determine whether performance on lexical tasks was correlated with cerebral activation patterns. We found that such relationships did exist and that their anatomical distribution reflected the neurocognitive processing routes required by the task. Better performance on intramodal tasks (determining if visual words were spelled the same or if auditory words rhymed) was correlated with more activation in unimodal regions corresponding to the modality of sensory input, namely the fusiform gyrus (BA 37) for written words and the superior temporal gyrus (BA 22) for spoken words. Better performance in tasks requiring cross-modal conversions (determining if auditory words were spelled the same or if visual words rhymed), on the other hand, was correlated with more activation in posterior heteromodal regions, including the supramarginal gyrus (BA 40) and the angular gyrus (BA 39). Better performance in these cross-modal tasks was also correlated with greater activation in unimodal regions corresponding to the target modality of the conversion process (i.e., fusiform gyrus for auditory spelling and superior temporal gyrus for visual rhyming). In contrast, performance on the auditory spelling task was inversely correlated with activation in the superior temporal gyrus possibly reflecting a greater emphasis on the properties of the perceptual input rather than on the relevant transmodal conversions.     

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

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.     

Cortical dynamics of word recognition

While functional neuroimaging studies have helped elucidate major regions implicated in word recognition, much less is known about the dynamics of the associated activations or the actual neural processes of their functional network. We used intracerebral electroencephalography recordings in 10 patients with epilepsy to directly measure neural activity in the temporal and frontal lobes during written words' recognition, predominantly in the left hemisphere. The patients were presented visually with consonant strings, pseudo-words, and words and performed a hierarchical paradigm contrasting semantic processes (living vs. nonliving word categorization task), phonological processes (rhyme decision task on pseudo-words), and visual processes (visual analysis of consonant strings). Stimuli triggered a cascade of modulations in the gamma-band (>40 Hz) with reproducible timing and task-sensitivity throughout the functional reading network: the earliest gamma-band activations were observed for all stimuli in the mesial basal temporal lobe at 150 ms, reaching the word form area in the mid fusiform gyrus at 200 ms, evidencing a superiority effect for word-like stimuli. Peaks of gamma-band activations were then observed for word-like stimuli after 400 ms in the anterior and middle portion of the superior temporal gyrus (BA 38 and BA 22 respectively), in the pars triangularis of Broca's area for the semantic task (BAs 45 and 47), and in the pars opercularis for the phonological task (BA 44). Concurrently, we observed a two-pronged effect in the prefrontal cortex (BAs 9 and 46), with nonspecific sustained dorsal activation related to sustained attention and, more ventrally, a strong reflex deactivation around 500 ms, possibly due to semantic working memory reset.     

Parametric analysis of event-related potentials in semantic comprehension: evidence for parallel brain mechanisms

In event-related potential (ERP) studies of cognitive processes, the electrophysiological responses are typically contrasted between experimental conditions that are taken to represent discrete categories (e.g. attended vs. unattended stimuli, or real vs. nonsense words). Because categorical variation is less powerful than continuous or parametric variation, a more effective method may be to relate continuous variation in the cognitive process with matching variation in the electrophysiological responses. We assessed continuous variation in the expectancy and meaningfulness of words in different sentence contexts by having subjects rate the words along these two dimensions. ERP averages were then created for each word by averaging the ERP across all subjects' responses to that word. A parametric principal components analysis was then conducted by multiplying the factor topographies from the temporal PCA by the parameter correlation maps for each rating parameter. This analysis showed that both expectancy and meaningfulness begin to influence lexical processing around 200 ms. Source localization of the expectancy N2 (recognition potential) pointed to a source in the left fusiform gyrus region (visual word form area). Source localization of the meaningfulness N2 (meaning recognition potential) suggested a right inferior posterior source, such as in the right cerebellum or right fusiform area. Further research with parametric analysis of dense array ERPs may clarify the multiple neural mechanisms of word recognition.     

fMRI evidence for dual routes to the mental lexicon in visual word recognition.

Event-related fMRI was used to investigate lexical decisions to words of high and low frequency of occurrence and to pseudowords. The results obtained strongly support dual-route models of visual word processing. By contrasting words with pseudowords, bilateral occipito-temporal brain areas and posterior left middle temporal gyrus (MTG) were identified as contributing to the successful mapping of orthographic percepts onto visual word form representations. Low-frequency words and pseudowords elicited greater activations than high-frequency words in the superior pars opercularis [Brodmann's area (BA) 44] of the left inferior frontal gyrus (IFG), in the anterior insula, and in the thalamus and caudate nucleus. As processing of these stimuli during lexical search is known to rely on phonological information, it is concluded that these brain regions are involved in grapheme-to-phoneme conversion. Activation in the pars triangularis (BA 45) of the left IFG was observed only for low-frequency words. It is proposed that this region is involved in processes of lexical selection.     

Neural pathways involved in the processing of concrete and abstract words.

The purpose of this study was to delineate the neural pathways involved in processing concrete and abstract words using functional magnetic resonance imaging (fMRI). Word and pseudoword stimuli were presented visually, one at a time, and the participant was required to make a lexical decision. Lexical decision epochs alternated with a resting baseline. In each lexical decision epoch, the stimuli were either concrete words and pseudowords, or abstract words and pseudowords. Behavioral data indicated that, as with previous research, concrete word stimuli were processed more efficiently than abstract word stimuli. Analysis of the fMRI data indicated that processing of word stimuli, compared to the baseline condition, was associated with neural activation in the bilateral fusiform gyrus, anterior cingulate, left middle temporal gyrus, right posterior superior temporal gyrus, and left and right inferior frontal gyrus. A direct comparison between the abstract and concrete stimuli epochs yielded a significant area of activation in the right anterior temporal cortex. The results are consistent with recent positron emission tomography work showing right hemisphere activation during processing of abstract representations of language. The results are interpreted as support for a right hemisphere neural pathway in the processing of abstract word representations.     

Auditory and visual word processing studied with fMRI

Brain activations associated with semantic processing of visual and auditory words were investigated using functional magnetic resonance imaging (fMRI). For each form of word presentation, subjects performed two tasks: one semantic, and one nonsemantic. The semantic task was identical for both auditory and visual presentation: single words were presented and subjects determined whether the word was concrete or abstract. In the nonsemantic task for auditory words, subjects determined whether the word had one syllable or multiple syllables. In the nonsemantic task for visual words, subjects determined whether the word was presented in lower case or upper case. There was considerable overlap in where auditory and visual word semantic processing occurred. Visual and auditory semantic tasks both activated the left inferior frontal (BA 45), bilateral anterior prefrontal (BA 10, 46), and left premotor regions (BA 6) and anterior SMA (BA 6, 8). Left posterior temporal (middle temporal and fusiform gyrus) and predominantly right‐sided cerebellar activations were observed during the auditory semantic task but were not above threshold during visual word presentation. The data, when averaged across subjects, did not show obligatory activation of left inferior frontal and temporal language areas during nonsemantic word tasks. Individual subjects showed differences in the activation of the inferior frontal region while performing the same task, even though they showed similar response latency and accuracy. Hum. Brain Mapping 7:15–28, 1999. © 1999 Wiley‐Liss, Inc.     

A Heteromodal Word-Meaning Binding Site in the Visual Word Form Area under Top-Down Frontoparietal Control

The integral capacity of human language together with semantic memory drives the linkage of words and their meaning, which theoretically is subject to cognitive control. However, it remains unknown whether, across different language modalities and input/output formats, there is a shared system in the human brain for word-meaning binding and how this system interacts with cognitive control. Here, we conducted a functional magnetic resonance imaging experiment based on a large cohort of subjects (50 females, 50 males) to comprehensively measure the brain responses evoked by semantic processing in spoken and written word comprehension and production tasks (listening, speaking, reading, and writing). We found that heteromodal word input and output tasks involved distributed brain regions within a frontal-parietal-temporal network and focally coactivated the anterior lateral visual word form area (VWFA), which is located in the basal occipitotemporal area. Directed connectivity analysis revealed that the VWFA was invariably under significant top-down modulation of the frontoparietal control network and interacts with regions related to attention and semantic representation. This study reveals that the VWFA is a key site subserving general semantic processes linking words and meaning, challenging the predominant emphasis on this area''s specific role in reading or more general visual processes. Our findings also suggest that the dynamics between semantic memory and cognitive control mechanisms during word processing are largely independent of the modalities of input or output.SIGNIFICANCE STATEMENT Binding words and their meaning into a coherent whole during retrieval requires accessing semantic memory and cognitive control, allowing our thoughts to be expressed and comprehended through mind-external tokens in multiple modalities, such as written or spoken forms. However, it is still unknown whether multimodal language comprehension and production share a common word-meaning binding system in human brains and how this system is connected to a cognitive control mechanism. By systematically measuring brain activity evoked by spoken and written verbal input and output tasks tagging word-meaning binding processes, we demonstrate a general word-meaning binding site within the visual word form area (VWFA) and how this site is modulated by the frontal-parietal control network.     

Differential activation of object-selective visual areas by passive viewing of pictures and words

Functional imaging has shown that pictures of faces (N. Kanwisher, J. McDermott, M.M. Chun, The fusiform face area: a module in human extrastriate cortex specialized for face perception, J. Neurosci. 17 (1997) 4302-4311) and buildings (R. Epstein, N. Kanwisher, A cortical representation of the local visual environment, Nature 391 (1998) 598-601) activate different regions within the lateral occipital complex (LOC). To investigate effects of stimulus format on activation in these areas, we used event-related fMRI to measure brain activity during the passive viewing of pictures showing buildings and faces, and of words identifying these pictures. Consistent with earlier findings, pictures of faces activated bilateral regions in the lateral fusiform gyri, whereas pictures of buildings activated bilateral regions in the parahippocampal gyri. Analyzing the activation elicited by visually presenting the written names of the pictures, however, we did not find an effect of word meaning on the fMRI signal change in these areas: fMRI signal changes for the names of faces and the names of buildings did not differ in any of the areas selectively activated by the corresponding pictures. In general, both word conditions and non-preferred picture conditions elicited similar signal amplitudes. While presentation of words did not lead to strong activation in object-specific areas, activation for words of both categories was found in the left occipito-temporal cortex, close to the location which has tentatively been called 'visual word form area' (L. Cohen, S. Dehaene, L. Naccache, S. Lehéricy, G. Dehaene-Lambertz, et al., The visual word form are: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients, Brain 123 (2000) 291-307), revealing that words were processed effectively during the experiment. Taken together, these results show that names of pictures do not automatically activate the corresponding object-selective areas.     

Lexical/semantic processing in dorsal left inferior frontal gyrus

Previous studies have not determined whether the dorsal left inferior frontal gyrus has a lexical or semantic function. This study conducted an event-related functional MRI experiment to explore its function using Japanese words and nonsense words in a syllable counting task. The word task activated a dorsal area (BA6/44) and a ventral area (BA45/47) more extensively than did the nonsense word task. The results indicate that the dorsal area also has lexical or semantic functions, despite that it has been related to phonological processing from studies using written stimuli. The more extensive activation by the word task might result from the same level of effort during phonological processing of Japanese words and nonsense words.     

The left fusiform area is affected by written frequency of words

The recent neuroimaging literature gives conflicting evidence about whether the left fusiform gyrus (FG) might recognize words as unitary visual objects. The sensitivity of the left FG to word frequency might provide a neural basis for the orthographic input lexicon theorized by reading models [Patterson, K., Marshall, J. C., & Coltheart, M. (1985). Surface dyslexia: Cognitive and neuropsychological studies of phonological reading. London: Lawrence Erlbaum]. The goal of this study was to investigate the time course and neural correlates of word processing in right-handed readers engaged in an orthographic decision task. Three hundred and twenty Italian words of high and low written frequency and 320 non-derived legal pseudo-words were presented for 250ms in the central visual field. ERPs were recorded from 128 scalp sites in 10 Italian University students. Behavioural data showed a word superiority effect, with faster RTs to words than pseudo-words. Left occipito/temporal N2 (240ms) was greater to high-frequency than low-frequency words and pseudo-words. According to the swLORETA inverse solution, the underlying neural source of this effect was located in the left fusiform gyrus of the occipital lobe (X=-29, Y=-66, Z=-10, BA19) and the right superior temporal gyrus (X=51, Y=6, Z=-5, BA22), which are probably involved in word recognition and semantic representation, respectively. Later frontal ERP components, LPN (300-350) and P3 (400-500), also showed strong lexical sensitivity, thus suggesting implicit semantic processes. The results shed some light on the possible neural substrate of visual reading disabilities such as developmental surface dyslexia or pure alexia.     

Repetition suppression and semantic enhancement: an investigation of the neural correlates of priming

The priming of a stimulus by another has become an important tool for exploring the neural underpinnings of conceptual representations. However, priming effects can derive from many different types of relationships and it is important to distinguish between them in order to be able to develop theoretical accounts of the representation of conceptual knowledge. While it is well known that repetition priming (the repeated presentation of the same stimulus) is associated with a reduced neural response, called repetition suppression (RS), the neural correlates of semantic priming (when two stimuli are related in meaning but not identical) are not so well established. We compared the neural correlates of repetition and semantic priming using written words, independently manipulating form and meaning. In an fMRI study, subjects saw single words and made a concrete-abstract decision. Two consecutive words were identical (town-town) or varied along a continuum of semantic relatedness, from highly related (cord-string) to unrelated (face-sail). We found distinct patterns of activation for repetition and semantic priming. Repetition priming was associated with RS in LIFG, bilateral parahippocampal gyrus and R fusiform gyrus. We also observed increased activation for word repetition in the RMFG and RMTG/STG, which may reflect recognition of item's earlier presentation. There was no evidence of suppression for semantic relatedness. Semantic priming was associated with enhanced activation in multiple bilateral fronto-temporal areas, i.e. semantic enhancement. The results suggest that repetition and semantic priming in visual word recognition depend on distinct cognitive processes and neural substrates.     

Temporal lobe abnormalities in semantic processing by criminal psychopaths as revealed by functional magnetic resonance imaging

We tested the hypothesis that psychopathy is associated with abnormalities in semantic processing of linguistic information. Functional magnetic resonance imaging (fMRI) was used to elucidate and characterize the neural architecture underlying lexico-semantic processes in criminal psychopathic individuals and in a group of matched control participants. Participants performed a lexical decision task in which blocks of linguistic stimuli alternated with a resting baseline condition. In each lexical decision block, the stimuli were either concrete words and pseudowords or abstract words and pseudowords. Consistent with our hypothesis, psychopathic individuals, relative to controls, showed poorer behavioral performance for processing abstract words. Analysis of the fMRI data for both groups indicated that processing of word stimuli, compared with the resting baseline condition, was associated with neural activation in bilateral fusiform gyrus, anterior cingulate, left middle temporal gyrus, right posterior superior temporal gyrus, and left and right inferior frontal gyrus. Analyses confirmed our prediction that psychopathic individuals would fail to show the appropriate neural differentiation between abstract and concrete stimuli in the right anterior temporal gyrus and surrounding cortex. The results are consistent with other studies of semantic processing in psychopathy and support the theory that psychopathy is associated with right hemisphere abnormalities for processing conceptually abstract material.     

Alexia due to ischemic stroke of the visual word form area

The visual word form area (VWFA) is a region in the posterior left occipitotemporal cortex adjacent to the fusiform gyrus hypothesized to mediate word recognition. Evidence supporting the role of this area in reading comes from neuroimaging studies of normal subjects, case-controlled lesion studies, and studies of patients with surgical resection of the VWFA for tumors or epilepsy. Based on these prior reports, a small discrete lesion to the VWFA would be expected to cause alexia in a literate person without prior brain process, but such a case has not previously been reported to our knowledge. Here, we report the case of a previously-healthy 63-year-old man with the acute onset of alexia without other significant impairments. Magnetic resonance imaging (MRI) of the brain revealed a small ischemic stroke localized to the inferior left occipitotemporal cortex, corresponding to the approximate location of the putative VWFA. Characteristic of pure alexia, testing in the weeks following the stroke revealed a letter-by-letter reading strategy and a word length effect on single word reading. Formal visual field testing was normal. There was no color anomia, or object or face recognition deficits, although a mild agraphia may have been present. This case of acute-onset alexia in a previously normal individual due to a small stroke restricted to the VWFA and sparing occipital cortex and white matter pathways supports the conclusion that the VWFA is crucial for reading.