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.     

Task-specific repetition priming in left inferior prefrontal cortex

Previous neuroimaging studies have shown that activation in left inferior prefrontal cortices (LIPC) is reduced during repeated (primed) relative to initial (unprimed) stimulus processing. These reductions in anterior (approximately BA 45/47) and posterior (approximately BA 44/6) LIPC activation have been interpreted as reflecting implicit memory for initial semantic or phonological processing. However, prior studies do not unambiguously indicate that LIPC priming effects are specific to the recapitulation of higher-level (semantic and/or phonological), rather than lower-level (perceptual), processes. Moreover, no prior study has shown that the patterns of priming in anterior and posterior LIPC regions are dissociable. To address these issues, the present fMRI study examined the nature of priming in LIPC by examining the task-specificity of these effects. Participants initially processed words in either a semantic or a nonsemantic manner. Subsequently, participants were scanned while they made semantic decisions about words that had been previously processed in a semantic manner (within-task repetition), words that had been previously processed in a nonsemantic manner (across-task repetition), and words that had not been previously processed (novel words). Behaviorally, task-specific priming was observed: reaction times to make the semantic decision declined following prior semantic processing but not following prior nonsemantic processing of a word. Priming in anterior LIPC paralleled these results with signal reductions being observed following within-task, but not following across-task, repetition. Importantly, neural priming in posterior LIPC demonstrated a different pattern: priming was observed following both within-task and across-task repetition, with the magnitude of priming tending to be greater in the within-task condition. Direct comparison between anterior and posterior LIPC regions revealed a significant interaction. These findings indicate that anterior and posterior LIPC demonstrate distinct patterns of priming, with priming in the anterior region being task-specific, suggesting that this facilitation derives from repeated semantic processing of a stimulus.     

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.     

The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity

A number of regions of the temporal and frontal lobes are known to be important for spoken language comprehension, yet we do not have a clear understanding of their functional role(s). In particular, there is considerable disagreement about which brain regions are involved in the semantic aspects of comprehension. Two functional magnetic resonance studies use the phenomenon of semantic ambiguity to identify regions within the fronto-temporal language network that subserve the semantic aspects of spoken language comprehension. Volunteers heard sentences containing ambiguous words (e.g. 'the shell was fired towards the tank') and well-matched low-ambiguity sentences (e.g. 'her secrets were written in her diary'). Although these sentences have similar acoustic, phonological, syntactic and prosodic properties (and were rated as being equally natural), the high-ambiguity sentences require additional processing by those brain regions involved in activating and selecting contextually appropriate word meanings. The ambiguity in these sentences goes largely unnoticed, and yet high-ambiguity sentences produced increased signal in left posterior inferior temporal cortex and inferior frontal gyri bilaterally. Given the ubiquity of semantic ambiguity, we conclude that these brain regions form an important part of the network that is involved in computing the meaning of spoken sentences.     

Watching the brain during meaning acquisition

Acquiring the meaning of a new word in a foreign language can be achieved either by rote memorizing or, similar to meaning acquisition during infancy, by extracting it from context. Little is known about the brain mechanisms involved in word learning. Here we demonstrate, using event-related brain potentials, the rapid development of a brain signature related to lexical and semantic processing during contextual word learning. Healthy volunteers engaged in a simple word-learning task were required to discover the meaning of a novel word from a context during silent reading. After 3 exposures, brain potentials to novel words in meaningful contexts were indistinguishable from real words, although this acquisition effect was not observed for novel words, for which sentence contexts allowed no meaning derivation. Furthermore, when the learned novel words were presented in isolation, an activation of their corresponding meaning was observed, although this process was slower than for real words.     

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.     

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.     

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).     

The functional neuroanatomy of metrical stress evaluation of perceived and imagined spoken words

We hypothesized that areas in the temporal lobe that have been implicated in the phonological processing of spoken words would also be activated during the generation and phonological processing of imagined speech. We tested this hypothesis using functional magnetic resonance imaging during a behaviorally controlled task of metrical stress evaluation. Subjects were presented with bisyllabic words and had to determine the alternation of strong and weak syllables. Thus, they were required to discriminate between weak-initial words and strong-initial words. In one condition, the stimuli were presented auditorily to the subjects (by headphones). In the other condition the stimuli were presented visually on a screen and subjects were asked to imagine hearing the word. Results showed activation of the supplementary motor area, inferior frontal gyrus (Broca's area) and insula in both conditions. In the superior temporal gyrus (STG) and in the superior temporal sulcus (STS) strong activation was observed during the auditory (perceptual) condition. However, a region located in the posterior part of the STS/STG also responded during the imagery condition. No activation of this same region of the STS was observed during a control condition which also involved processing of visually presented words, but which required a semantic decision from the subject. We suggest that processing of metrical stress, with or without auditory input, relies in part on cortical interface systems located in the posterior part of STS/STG. These results corroborate behavioral evidence regarding phonological loop involvement in auditory-verbal imagery.     

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.     

Mood states modulate activity in semantic brain areas during emotional word encoding

It is controversially discussed whether or not mood-congruent recall (i.e., superior recall for mood-congruent material) reflects memory encoding processes or reduces to processes during retrieval. We therefore investigated the neurophysiological correlates of mood-dependent memory during emotional word encoding. Event-related potentials (ERPs) were recorded while participants in good or bad mood states encoded words of positive and negative valence. Words were either complete or had to be generated from fragments. Participants had to memorize words for subsequent recall. Mood-congruent recall tended to be largest in good mood for generated words. Starting at 200 ms, mood-congruent ERP effects of word valence were obtained in good, but not in bad mood. Only for good mood, source analysis revealed valence-related activity in ventral temporal cortex and for generated words also in prefrontal cortex. These areas are known to be involved in semantic processing. Our findings are consistent with the view that mood-congruent recall depends on the activation of mood-congruent semantic knowledge during encoding. Incoming stimuli are more readily transformed according to stored knowledge structures in good mood particularly during generative encoding tasks. The present results therefore show that mood-congruent memory originates already during encoding and cannot be reduced to strategic processes during retrieval.     

Reading salt activates gustatory brain regions: FMRI evidence for semantic grounding in a novel sensory modality

Because many words are typically used in the context of their referent objects and actions, distributed cortical circuits for these words may bind information about their form with perceptual and motor aspects of their meaning. Previous work has demonstrated such semantic grounding for sensorimotor, visual, auditory, and olfactory knowledge linked to words, which is manifest in activation of the corresponding areas of the cortex. Here, we explore the brain basis of gustatory semantic links of words whose meaning is primarily related to taste. In a blocked functional magnetic resonance imaging design, Spanish taste words and control words matched for a range of factors (including valence, arousal, imageability, frequency of use, number of letters and syllables) were presented to 59 right-handed participants in a passive reading task. Whereas all the words activated the left inferior frontal (BA44/45) and the posterior middle and superior temporal gyri (BA21/22), taste-related words produced a significantly stronger activation in these same areas and also in the anterior insula, frontal operculum, lateral orbitofrontal gyrus, and thalamus among others. As these areas comprise primary and secondary gustatory cortices, we conclude that the meaning of taste words is grounded in distributed cortical circuits reaching into areas that process taste sensations.     

Common and dissociable activation patterns associated with controlled semantic and phonological processing: evidence from FMRI adaptation

Recent evidence suggests specialization of anterior left inferior prefrontal cortex (aLIPC; approximately BA 45/47) for controlled semantics and of posterior LIPC (pLIPC; approximately BA 44/6) for controlled phonology. However, the more automated phonological tasks commonly used raise the possibility that some of the typically extensive aLIPC activation during semantic tasks may relate to controlled language processing beyond the semantic domain. In the present study, an event-related fMRI adaptation paradigm was employed that used a standard controlled semantic task and a phonological task that also emphasized controlled processing. When compared with letter (baseline) processing, significant fMRI task and adaptation effects in the aLIPC and pLIPC regions ( approximately BA 45/47, approximately BA 44) were observed during both semantic and phonological processing, with aLIPC showing the strongest effects during semantic processing. A left frontal region ( approximately BA 6) showed task and relative adaptation effects preferential for phonological processing, and a left temporal region ( approximately BA 21) showed task and relative adaptation effects preferential for semantic processing. Our results demonstrate that aLIPC and pLIPC regions are involved in controlled processing across multiple language domains, arguing against a domain-specific LIPC model and for domain-preferentiality in left posterior frontal and temporal regions.     

Segregating semantic and syntactic aspects of processing in the human brain: an fMRI investigation of different word types

The processing of single words that varied in their semantic (concrete/abstract word) and syntactic (content/function word) status was investigated under different task demands (semantic/ syntactic task) in an event-related functional magnetic resonance imaging experiment. Task demands to a large degree determined which subparts of the neuronal network supporting word processing were activated. Semantic task demands selectively activated the left pars triangularis of the inferior frontal gyrus (BA 45) and the posterior part of the left middle/superior temporal gyrus (BA 21/22/37). In contrast, syntactic processing requirements led to an increased activation in the inferior tip of the left frontal operculum (BA 44) and the cortex lining the junction of the inferior frontal and inferior precentral sulcus (BA 44/6). Moreover, for these latter areas a word class by concreteness interaction was observed when a syntactic judgement was required. This interaction can be interpreted as a prototypicality effect: non-prototypical members of a word class, i.e. concrete function words and abstract content words, showed a larger activation than prototypical members, i.e. abstract function words and concrete content words. The combined data suggest that the activation pattern underlying word processing is predicted neither by syntactic class nor semantic concreteness but, rather, by task demands focusing either on semantic or syntactic aspects. Thus, our findings that semantic and syntactic aspects of processing are both functionally distinct and involve different subparts of the neuronal network underlying word processing support a domain-specific organization of the language system.     

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.     

Hemispheric specialization for processing auditory nonspeech stimuli

The left hemisphere specialization for speech perception might arise from asymmetries at more basic levels of auditory processing. In particular, it has been suggested that differences in "temporal" and "spectral" processing exist between the hemispheres. Here we used functional magnetic resonance imaging to test this hypothesis further. Fourteen healthy volunteers listened to sequences of alternating pure tones that varied in the temporal and spectral domains. Increased temporal variation was associated with activation in Heschl's gyrus (HG) bilaterally, whereas increased spectral variation activated the superior temporal gyrus (STG) bilaterally and right posterior superior temporal sulcus (STS). Responses to increased temporal variation were lateralized to the left hemisphere; this left lateralization was greater in posteromedial HG, which is presumed to correspond to the primary auditory cortex. Responses to increased spectral variation were lateralized to the right hemisphere specifically in the anterior STG and posterior STS. These findings are consistent with the notion that the hemispheres are differentially specialized for processing auditory stimuli even in the absence of linguistic information.     

Sex differences in semantic processing: event-related brain potentials distinguish between lower and higher order semantic analysis during word reading

Behavioral studies suggest that women and men differ in the strategic elaboration of verbally encoded information especially in the absence of external task demand. However, measuring such covert processing requires other than behavioral data. The present study used event-related potentials to compare sexes in lower and higher order semantic processing during the passive reading of semantically related and unrelated word pairs. Women and men showed the same early context effect in the P1-N1 transition period. This finding indicates that the initial lexical-semantic access is similar in men and women. In contrast, sexes differed in higher order semantic processing. Women showed an earlier and longer lasting context effect in the N400 accompanied by larger signal strength in temporal networks similarly recruited by men and women. The results suggest that women spontaneously conduct a deeper semantic analysis. This leads to faster processing of related words in the active neural networks as reflected in a shorter stability of the N400 map in women. Taken together, the findings demonstrate that there is a selective sex difference in the controlled semantic analysis during passive word reading that is not reflected in different functional organization but in the depth of processing.     

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.     

A role for the motor system in binding abstract emotional meaning

Sensorimotor areas activate to action- and object-related words, but their role in abstract meaning processing is still debated. Abstract emotion words denoting body internal states are a critical test case because they lack referential links to objects. If actions expressing emotion are crucial for learning correspondences between word forms and emotions, emotion word-evoked activity should emerge in motor brain systems controlling the face and arms, which typically express emotions. To test this hypothesis, we recruited 18 native speakers and used event-related functional magnetic resonance imaging to compare brain activation evoked by abstract emotion words to that by face- and arm-related action words. In addition to limbic regions, emotion words indeed sparked precentral cortex, including body-part-specific areas activated somatotopically by face words or arm words. Control items, including hash mark strings and animal words, failed to activate precentral areas. We conclude that, similar to their role in action word processing, activation of frontocentral motor systems in the dorsal stream reflects the semantic binding of sign and meaning of abstract words denoting emotions and possibly other body internal states.     

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.