Brain mechanisms for reading words and pseudowords: an integrated approach

The present study tested two predictions of dual-process models of reading: (i) that the brain structures involved in sublexical phonological analysis and those involved in whole-word phonological access during reading are different; and (ii) that reading of meaningful items, by means of the addressed phonology process, is mediated by different brain structures than reading of meaningless letter strings. We obtained brain activation profiles using Magnetic Source Imaging and, in addition, pronunciation latencies during reading of: (i) exception words (primarily involving addressed phonology and having meaning), (ii) pseudohomophones (requiring assembled phonology and having meaning), and (iii) pseudowords (requiring assembled phonology but having no meaning). Reading of meaningful items entailed a high degree of activation of the left posterior middle temporal gyrus (MTGp) and mesial temporal lobe areas, whereas reading the meaningless pseudowords was associated with much reduced activation of these two regions. Reading of all three types of print resulted in activation of the posterior superior temporal gyrus (STGp), inferior parietal and basal temporal areas. In addition, pronunciation speed of exception words correlated significantly with the onset of activity in MTGp but not STGp, whereas the opposite was true for pseudohomophones and pseudowords. These findings are consistent with the existence of two different brain mechanisms that support phonological processing in word reading: one mechanism that subserves assembled phonology and depends on the posterior part of STGp, and a second mechanism that is responsible for pronouncing words with rare print-to-sound correspondences and does not necessarily involve this region but instead appears to depend on MTGp.     

Memory traces for spoken words in the brain as revealed by the hemodynamic correlate of the mismatch negativity

The mismatch negativity response, considered a brain correlate of automatic preattentive auditory processing, is enhanced for word stimuli as compared with acoustically matched pseudowords. This lexical enhancement, taken as a signature of activation of language-specific long-term memory traces, was investigated here using functional magnetic resonance imaging to complement the previous electrophysiological studies. In passive oddball paradigm, word stimuli were randomly presented as rare deviants among frequent pseudowords; the reverse conditions employed infrequent pseudowords among word stimuli. Random-effect analysis indicated clearly distinct patterns for the different lexical types. Whereas the hemodynamic mismatch response was significant for the word deviants, it did not reach significance for the pseudoword conditions. This difference, more pronounced in the left than right hemisphere, was also assessed by analyzing average parameter estimates in regions of interests within both temporal lobes. A significant hemisphere-by-lexicality interaction confirmed stronger blood oxygenation level-dependent mismatch responses to words than pseudowords in the left but not in the right superior temporal cortex. The increased left superior temporal activation and the laterality of cortical sources elicited by spoken words compared with pseudowords may indicate the activation of cortical circuits for lexical material even in passive oddball conditions and suggest involvement of the left superior temporal areas in housing such word-processing neuronal circuits.     

Common neural substrates for inhibition of spoken and manual responses

The inhibition of speech acts is a critical aspect of human executive control over thought and action, but its neural underpinnings are poorly understood. Using functional magnetic resonance imaging and the stop-signal paradigm, we examined the neural correlates of speech control in comparison to manual motor control. Initiation of a verbal response activated left inferior frontal cortex (IFC: Broca's area). Successful inhibition of speech (naming of letters or pseudowords) engaged a region of right IFC (including pars opercularis and anterior insular cortex) as well as presupplementary motor area (pre-SMA); these regions were also activated by successful inhibition of a hand response (i.e., a button press). Moreover, the speed with which subjects inhibited their responses, stop-signal reaction time, was significantly correlated between speech and manual inhibition tasks. These findings suggest a functional dissociation of left and right IFC in initiating versus inhibiting vocal responses, and that manual responses and speech acts share a common inhibitory mechanism localized in the right IFC and pre-SMA.     

Silence is golden: transient neural deactivation in the prefrontal cortex during attentive reading

It is becoming increasingly clear that attention-demanding tasks engage not only activation of specific cortical regions but also deactivation of other regions that could interfere with the task at hand. At the same time, electrophysiological studies in animals and humans have found that the participation of cortical regions to cognitive processes translates into local synchronization of rhythmic neural activity at frequencies above 40 Hz (so-called gamma-band synchronization). Such synchronization is seen as a potential facilitator of neural communication and synaptic plasticity. We found evidence that cognitive processes can also involve the disruption of gamma-band activity in high-order brain regions. Intracerebral electroencephalograms were recorded in 3 epileptic patients during 2 reading tasks. Visual presentation of words induced a strong deactivation in a broad (20-150 Hz) frequency range in the left ventral lateral prefrontal cortex, in parallel with gamma-band activations within the reading network, including Broca's area. The observed energy decrease in neural signals was reproducible across patients. It peaked around 500 ms after stimulus onset and appeared subject to attention-modulated amplification. Our results suggest that cognition might be mediated by a coordinated interaction between regional gamma-band synchronizations and desynchronizations, possibly reflecting enhanced versus reduced local neural communication.     

The effect of prior visual information on recognition of speech and sounds

To identify and categorize complex stimuli such as familiar objects or speech, the human brain integrates information that is abstracted at multiple levels from its sensory inputs. Using cross-modal priming for spoken words and sounds, this functional magnetic resonance imaging study identified 3 distinct classes of visuoauditory incongruency effects: visuoauditory incongruency effects were selective for 1) spoken words in the left superior temporal sulcus (STS), 2) environmental sounds in the left angular gyrus (AG), and 3) both words and sounds in the lateral and medial prefrontal cortices (IFS/mPFC). From a cognitive perspective, these incongruency effects suggest that prior visual information influences the neural processes underlying speech and sound recognition at multiple levels, with the STS being involved in phonological, AG in semantic, and mPFC/IFS in higher conceptual processing. In terms of neural mechanisms, effective connectivity analyses (dynamic causal modeling) suggest that these incongruency effects may emerge via greater bottom-up effects from early auditory regions to intermediate multisensory integration areas (i.e., STS and AG). This is consistent with a predictive coding perspective on hierarchical Bayesian inference in the cortex where the domain of the prediction error (phonological vs. semantic) determines its regional expression (middle temporal gyrus/STS vs. AG/intraparietal sulcus).     

A developmental fMRI study of reading and repetition reveals changes in phonological and visual mechanisms over age

In this study of reading development, children (ages 7-10) and adults (ages 18-32) performed overt single-word reading and aural repetition tasks on high-frequency word stimuli during functional magnetic resonance imaging. Most regions showed similar activity across age groups. These widespread regions of similarity indicate that children and adults use largely overlapping mechanisms when processing high-frequency words. Significant task-related differences included greater activity in occipital cortex for the read task, and greater activity in temporal cortex for the repeat task; activity levels in these regions were similar for adults and children. However, age group differences were found in several posterior regions, including a set of regions implicated in adult reading: the left supramarginal gyrus, the left angular gyrus, and bilateral anterior extrastriate cortex. The angular and supramarginal gyrus regions, hypothesized to play a role in phonology, showed decreased activity in adults relative to children for high-frequency words. The extrastriate regions had significant activity for both the visual read task and auditory repeat task in children, but just for the read task in adults, showing significant task and age interactions. These results are consistent with decreasing reliance on phonological processing, and increasing tuning of visual mechanisms, with age.     

Neural interactions at the core of phonological and semantic priming of written words

Word processing is often probed with experiments where a target word is primed by preceding semantically or phonologically related words. Behaviorally, priming results in faster reaction times, interpreted as increased efficiency of cognitive processing. At the neural level, priming reduces the level of neural activation, but the actual neural mechanisms that could account for the increased efficiency have remained unclear. We examined whether enhanced information transfer among functionally relevant brain areas could provide such a mechanism. Neural activity was tracked with magnetoencephalography while subjects read lists of semantically or phonologically related words. Increased priming resulted in reduced cortical activation. In contrast, coherence between brain regions was simultaneously enhanced. Furthermore, while the reduced level of activation was detected in the same area and time window (superior temporal cortex [STC] at 250-650 ms) for both phonological and semantic priming, the spatiospectral connectivity patterns appeared distinct for the 2 processes. Causal interactions further indicated a driving role for the left STC in phonological processing. Our results highlight coherence as a neural mechanism of priming and dissociate semantic and phonological processing via their distinct connectivity profiles.     

Cerebral mechanisms involved in word reading in dyslexic children: a magnetic source imaging approach

The purpose of the present investigation was to describe spatiotemporal brain activation profiles during word reading using magnetic source imaging (MSI). Ten right-handed dyslexic children with severe phonological decoding problems and eight age-matched non-impaired readers were tested in two recognition tasks, one involving spoken and the other printed words. Dyslexic children's activation profiles during the printed word recognition task consistently featured activation of the left basal temporal cortices followed by activation of the right temporoparietal areas (including the angular gyrus). Non-impaired readers showed predominant activation of left basal followed by left temporoparietal activation. In addition, we were able to rule out the hypothesis that hypoactivation of left temporoparietal areas in dyslexics was due to a more general cerebral dysfunction in these areas. Rather, it seems likely that reading difficulties in developmental dyslexia are associated with an aberrant pattern of functional connectivity between brain areas normally involved in reading, namely ventral visual association cortex and temporoparietal areas in the left hemisphere. The interindividual consistency of activation profiles characteristic of children with dyslexia underlines the potential utility of this technique for examining neurophysiological changes in response to specific educational intervention approaches.     

Human temporal lobe activation by speech and nonspeech sounds

Functional organization of the lateral temporal cortex in humans is not well understood. We recorded blood oxygenation signals from the temporal lobes of normal volunteers using functional magnetic resonance imaging during stimulation with unstructured noise, frequency-modulated (FM) tones, reversed speech, pseudowords and words. For all conditions, subjects performed a material-nonspecific detection response when a train of stimuli began or ceased. Dorsal areas surrounding Heschl's gyrus bilaterally, particularly the planum temporale and dorsolateral superior temporal gyrus, were more strongly activated by FM tones than by noise, suggesting a role in processing simple temporally encoded auditory information. Distinct from these dorsolateral areas, regions centered in the superior temporal sulcus bilaterally were more activated by speech stimuli than by FM tones. Identical results were obtained in this region using words, pseudowords and reversed speech, suggesting that the speech-tones activation difference is due to acoustic rather than linguistic factors. In contrast, previous comparisons between word and nonword speech sounds showed left-lateralized activation differences in more ventral temporal and temporoparietal regions that are likely involved in processing lexical-semantic or syntactic information associated with words. The results indicate functional subdivision of the human lateral temporal cortex and provide a preliminary framework for understanding the cortical processing of speech sounds.     

Word reading and posterior temporal dysfunction in amnestic mild cognitive impairment

Patient studies that combine functional magnetic resonance imaging with chronometric analysis of language dysfunction may reveal the critical contribution of brain areas to language processes as well as shed light on disease pathogenesis. In amnestic mild cognitive impairment (MCI), a prodromal stage of Alzheimer's disease, we examined whether the brain system for associative-semantic judgments with words or with pictures is affected and how this relates to off-line chronometric analysis of word reading and picture naming. A consecutive memory clinic-based series of 13 amnestic MCI patients as well as 13 matched controls participated. One area, the lower bank of the posterior third of the left superior temporal sulcus (STS), showed a significant group-by-task interaction: In controls, it was activated during the associative-semantic condition with words compared with the visuoperceptual control condition but not when the same tasks were compared with pictures as input. In MCI, this word-specific activation was significantly reduced. Response amplitude correlated (r = 0.90) with the steepness of the slope of the time-accuracy curve for word reading. Our data provide converging evidence for a critical contribution of the lower bank of the left posterior STS to mapping word form onto word meaning (lexical-semantic retrieval).     

Differential sensitivity to words and shapes in ventral occipito-temporal cortex

Efficient extraction of shape information is essential for proficient reading but the role of cortical mechanisms of shape analysis in word reading is not well understood. We studied cortical responses to written words while parametrically varying the amount of visual noise applied to the word stimuli. In only a few regions along the ventral surface, cortical responses increased with word visibility. We found consistently increasing responses in bilateral posterior occipito-temporal sulcus (pOTS), at an anatomical location that closely matches the "visual word form area". In other cortical regions, such as V1, responses remained constant regardless of the noise level. We performed 3 additional tests to assess the functional specialization of pOTS responses for written word processing. We asked whether pOTS responses are 1) left lateralized, 2) more sensitive to words than to line drawings or false fonts, and 3) invariant for visual hemifield of words but not other stimuli. We found that left and right pOTS response functions both had highest sensitivity for words, intermediate for line drawings, and lowest for false fonts. Visual hemifield invariance was similar for words and line drawings. These results suggest that left and right pOTS are both involved in shape processing, with enhanced efficiency for processing visual word forms.     

The effects of age on the neural correlates of episodic encoding

Young and old adults underwent positron emission tomographic scans while encoding pictures of objects and words using three encoding strategies: deep processing (a semantic living/nonliving judgement), shallow processing (size judgement) and intentional learning. Picture memory exceeded word memory in both young and old groups, and there was an age-related decrement only in word recognition. During the encoding tasks three brain activity patterns were found that differentiated stimulus type and the different encoding strategies. The stimulus-specific pattern was characterized by greater activity in extrastriate and medial temporal cortices during picture encoding, and greater activity in left prefrontal and temporal cortices during encoding of words. The older adults showed this pattern to a significantly lesser degree. A pattern distinguishing deep processing from intentional learning of words and pictures was identified, characterized mainly by differences in prefrontal cortex, and this pattern also was of significantly lesser magnitude in the old group. A final pattern identified areas with increased activity during deep processing and intentional learning of pictures, including left prefrontal and bilateral medial temporal regions. There was no group difference in this pattern. These results indicate age-related dysfunction in several encoding networks, with sparing of one specifically involved in more elaborate encoding of pictures. These age-related changes appear to affect verbal memory more than picture memory.     

The role of semantics and grammatical class in the neural representation of words

On the basis of neuropsychological and functional imaging evidence, meaning and grammatical class (particularly the verb-noun distinction) have been proposed as organizational principles of linguistic knowledge in the brain. However, previous studies investigating verb and noun processing have been confounded by the presence of systematic correlations between word meaning and grammatical class. In this positron emission tomography study, we investigated implicit word processing using stimuli that allowed the effects of semantic and grammatical properties to be examined independently, without grammatical-semantic confounds. We found that left hemisphere cortical activation during single-word processing was modulated by word meaning, but not by grammatical class. Motor word processing produced significant activation in left precentral gyrus, whereas sensory word processing produced significant activation in left inferior temporal and inferior frontal regions. In contrast to previous studies, there were no effects of grammatical class in left inferior frontal gyrus (IFG). Instead, we found semantic-based differences within left IFG: anterior, but not posterior, left IFG regions responded preferentially to sensory words. These findings demonstrate that the neural substrates of implicit word processing are determined by semantic rather than grammatical properties and suggest that word comprehension involves the activation of modality-specific representations linked to word meaning.     

Cross-modal binding and activated attentional networks during audio-visual speech integration: a functional MRI study

We evaluated the neural substrates of cross-modal binding and divided attention during audio-visual speech integration using functional magnetic resonance imaging. The subjects (n = 17) were exposed to phonemically concordant or discordant auditory and visual speech stimuli. Three different matching tasks were performed: auditory-auditory (AA), visual-visual (VV) and auditory-visual (AV). Subjects were asked whether the prompted pair were congruent or not. We defined the neural substrates for the within-modal matching tasks by VV-AA and AA-VV. We defined the cross-modal area as the intersection of the loci defined by AV-AA and AV-VV. The auditory task activated the bilateral anterior superior temporal gyrus and superior temporal sulcus, the left planum temporale and left lingual gyrus. The visual task activated the bilateral middle and inferior frontal gyrus, right occipito-temporal junction, intraparietal sulcus and left cerebellum. The bilateral dorsal premotor cortex, posterior parietal cortex (including the bilateral superior parietal lobule and the left intraparietal sulcus) and right cerebellum showed more prominent activation during AV compared with AA and VV. Within these areas, the posterior parietal cortex showed more activation during concordant than discordant stimuli, and hence was related to cross-modal binding. Our results indicate a close relationship between cross-modal attentional control and cross-modal binding during speech reading.     

Category-specific conceptual processing of color and form in left fronto-temporal cortex

To investigate the cortical basis of color and form concepts, we examined event-related functional magnetic resonance imaging (fMRI) responses to matched words related to abstract color and form information. Silent word reading elicited activity in left temporal and frontal cortex, where category-specific activity differences were also observed. Whereas color words preferentially activated anterior parahippocampal gyrus, form words evoked category-specific activity in fusiform and middle temporal gyrus as well as premotor and dorsolateral prefrontal areas in inferior and middle frontal gyri. These results demonstrate that word meanings and concepts are not processed by a unique cortical area, but by different sets of areas, each of which may contribute differentially to conceptual semantic processing. We hypothesize that the anterior parahippocampal activation to color words indexes computation of the visual feature conjunctions and disjunctions necessary for classifying visual stimuli under a color concept. The predominant premotor and prefrontal activation to form words suggests action-related information processing and may reflect the involvement of neuronal elements responding in an either-or fashion to mirror neurons related to adumbrating shapes.     

Mental visual synthesis is originated in the fronto-temporal network of the left hemisphere

Mental visual synthesis is the capacity for experiencing, constructing, or manipulating 'mental imagery'. To investigate brain networks involved in mental visual synthesis, brain activity was measured in right-handed healthy volunteers during mental imagery tasks, in which the subjects were instructed to imagine a novel object, that does not exist in the real world, by composing it from two visually presented words associated with a real object or two achromatic line drawings of a real object, using functional magnetic resonance imaging (fMRI). Both tasks activated the same areas in the inferior frontal and inferior temporal cortices of the left hemisphere. Our results indicate that the source of mental visual synthesis may be formed by activity of a brain network consisting of these areas, which are also involved in semantic operations and visual imagery.     

Spatiotemporal interaction between sound form and meaning during spoken word perception

Cortical dynamics of spoken word perception is not well understood. The possible interplay between analysis of sound form and meaning, in particular, remains elusive. We used magnetoencephalography to study cortical manifestation of phonological and semantic priming. Ten subjects listened to lists of 4 words. The first 3 words set a semantic or phonological context, and the list-final word was congruent or incongruent with this context. Attenuation of activation by priming during the first 3 words and increase of activation to semantic or phonological mismatch in the list-final word provided converging evidence: The superior temporal cortex bilaterally was involved in both analysis of sound form and meaning but the role of each hemisphere varied over time. Sensitivity to sound form was observed at approximately 100 ms after word onset, followed by sensitivity to semantic aspects from approximately 250 ms onwards, in the left hemisphere. From approximately 450 ms onwards, the picture was changed, with semantic effects now present bilaterally, accompanied by a subtle late effect of sound form in the right hemisphere. Present MEG data provide a detailed spatiotemporal account of neural mechanisms during speech perception that may underlie characterizations obtained with other neuroimaging methods less sensitive in temporal or spatial domain.     

Where, when and why brain activation differs for bilinguals and monolinguals during picture naming and reading aloud

Using functional magnetic resonance imaging, we found that when bilinguals named pictures or read words aloud, in their native or nonnative language, activation was higher relative to monolinguals in 5 left hemisphere regions: dorsal precentral gyrus, pars triangularis, pars opercularis, superior temporal gyrus, and planum temporale. We further demonstrate that these areas are sensitive to increasing demands on speech production in monolinguals. This suggests that the advantage of being bilingual comes at the expense of increased work in brain areas that support monolingual word processing. By comparing the effect of bilingualism across a range of tasks, we argue that activation is higher in bilinguals compared with monolinguals because word retrieval is more demanding; articulation of each word is less rehearsed; and speech output needs careful monitoring to avoid errors when competition for word selection occurs between, as well as within, language.     

The putative visual word form area is functionally connected to the dorsal attention network

The putative visual word form area (pVWFA) is the most consistently activated region in single word reading studies (i.e., Vigneau et al. 2006), yet its function remains a matter of debate. The pVWFA may be predominantly used in reading or it could be a more general visual processor used in reading but also in other visual tasks. Here, resting-state functional connectivity magnetic resonance imaging (rs-fcMRI) is used to characterize the functional relationships of the pVWFA to help adjudicate between these possibilities. rs-fcMRI defines relationships based on correlations in slow fluctuations of blood oxygen level-dependent activity occurring at rest. In this study, rs-fcMRI correlations show little relationship between the pVWFA and reading-related regions but a strong relationship between the pVWFA and dorsal attention regions thought to be related to spatial and feature attention. The rs-fcMRI correlations between the pVWFA and regions of the dorsal attention network increase with age and reading skill, while the correlations between the pVWFA and reading-related regions do not. These results argue the pVWFA is not used predominantly in reading but is a more general visual processor used in other visual tasks, as well as reading.     

Sound to language: different cortical processing for first and second languages in elementary school children as revealed by a large-scale study using fNIRS

A large-scale study of 484 elementary school children (6-10 years) performing word repetition tasks in their native language (L1-Japanese) and a second language (L2-English) was conducted using functional near-infrared spectroscopy. Three factors presumably associated with cortical activation, language (L1/L2), word frequency (high/low), and hemisphere (left/right), were investigated. L1 words elicited significantly greater brain activation than L2 words, regardless of semantic knowledge, particularly in the superior/middle temporal and inferior parietal regions (angular/supramarginal gyri). The greater L1-elicited activation in these regions suggests that they are phonological loci, reflecting processes tuned to the phonology of the native language, while phonologically unfamiliar L2 words were processed like nonword auditory stimuli. The activation was bilateral in the auditory and superior/middle temporal regions. Hemispheric asymmetry was observed in the inferior frontal region (right dominant), and in the inferior parietal region with interactions: low-frequency words elicited more right-hemispheric activation (particularly in the supramarginal gyrus), while high-frequency words elicited more left-hemispheric activation (particularly in the angular gyrus). The present results reveal the strong involvement of a bilateral language network in children's brains depending more on right-hemispheric processing while acquiring unfamiliar/low-frequency words. A right-to-left shift in laterality should occur in the inferior parietal region, as lexical knowledge increases irrespective of language.