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.     

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.     

Positron emission tomography study of letter and object processing: empirical findings and methodological considerations.

The study of functional-anatomical correlations of higher-order cognitive processing has benefited from recent advances in brain imaging techniques such as positron emission tomography (PET) measurements of regional cerebral blood flow (CBF). Comparisons of CBF changes by paired image subtraction provide the opportunity to isolate cerebral areas participating in the realization of the processes that differentiate two tasks. However, the subtraction method is based on assumptions that are not entirely compatible with cerebral cognitive processing, and the derived pattern of activation specifically associated with the processes that differentiate two tasks is relative to the activation associated with the subtracted task and may therefore vary as a function of the processes actually performed in this subtracted task. To examine the implications of this procedure, a PET study with the 15O water bolus technique was carried out on normal adults. Subjects performed three tasks that made nonoverlapping cognitive processing demands: a semantic categorization of visual objects, a spatial discrimination of visually presented letters, and a phonological decision on visually presented single letters. Each task produced distinct patterns of activation consistent with evidence from neurological patients, specifically in the left occipital cortex in the semantic categorization of objects, in the parietal cortex of both hemispheres in the letter-spatial task, and in the left frontal and superior temporal cortex in the letter-sound task. However, the comparisons between the two letter tasks did not result in the expected CBF changes even though these two tasks make distinct processing requirements and are dissociable by brain injury. In addition, the phonological task resulted in activation of areas of the frontal cortex that earlier PET studies had identified as participating in semantic operations, whereas letters have no semantic property. These results suggest that the interpretation of patterns of activation is confronted with difficulties due to the automatic, and uncontrolled, processing of verbal stimuli that raises the threshold for significant CBF changes between two conditions that use the same stimuli but different task demands.     

The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes

An event-related functional magnetic resonance imaging (fMRI) paradigm was used to specify those brain areas supporting the processing of sentence-level semantic and syntactic information. Hemodynamic responses were recorded while participants listened to correct, semantically incorrect and syntactically incorrect sentences. Both anomalous conditions recruited larger portions of the superior temporal region than correct sentences. Processing of semantic violations relied primarily on the mid-portion of the superior temporal region bilaterally and the insular cortex bilaterally, whereas processing of syntactic violations specifically involved the anterior portion of the left superior temporal gyrus, the left posterior frontal operculum adjacent to Broca's area and the putamen in the left basal ganglia. A comparison of the two anomalous conditions revealed higher levels of activation for the syntactic over the semantic condition in the left basal ganglia and for the semantic over the syntactic condition in the mid-portion of the superior temporal gyrus, bilaterally. These data indicate that both semantic and syntactic processes are supported by a temporo-frontal network with distinct areas specialized for semantic and syntactic processes.     

Selective attention to semantic and syntactic features modulates sentence processing networks in anterior temporal cortex

Numerous studies have identified an anterior temporal lobe (ATL) region that responds preferentially to sentence-level stimuli. It is unclear, however, whether this activity reflects a response to syntactic computations or some form of semantic integration. This distinction is difficult to investigate with the stimulus manipulations and anomaly detection paradigms traditionally implemented. The present functional magnetic resonance imaging study addresses this question via a selective attention paradigm. Subjects monitored for occasional semantic anomalies or occasional syntactic errors, thus directing their attention to semantic integration, or syntactic properties of the sentences. The hemodynamic response in the sentence-selective ATL region (defined with a localizer scan) was examined during anomaly/error-free sentences only, to avoid confounds due to error detection. The majority of the sentence-specific region of interest was equally modulated by attention to syntactic or compositional semantic features, whereas a smaller subregion was only modulated by the semantic task. We suggest that the sentence-specific ATL region is sensitive to both syntactic and integrative semantic functions during sentence processing, with a smaller portion of this area preferentially involved in the later. This study also suggests that selective attention paradigms may be effective tools to investigate the functional diversity of networks involved in sentence processing.     

Two distinct neural mechanisms for category-selective responses

The cognitive and neural mechanisms mediating category-selective responses in the human brain remain controversial. Using functional magnetic resonance imaging and effective connectivity analyses (Dynamic Causal Modelling), we investigated animal- and tool-selective responses by manipulating stimulus modality (pictures versus words) and task (implicit versus explicit semantic). We dissociated two distinct mechanisms that engender category selectivity: in the ventral occipito-temporal cortex, tool-selective responses were observed irrespective of task, greater for pictures and mediated by bottom-up effects. In a left temporo-parietal action system, tool-selective responses were observed irrespective of modality, greater for explicit semantic tasks and mediated by top-down modulation from the left prefrontal cortex. These distinct activation and connectivity patterns suggest that the two systems support different cognitive operations, with the ventral occipito-temporal regions engaged in structural processing and the dorsal visuo-motor system in strategic semantic processing. Consistent with current semantic theories, explicit semantic processing of tools might thus rely on reactivating their associated action representations via top-down modulation. In terms of neuronal mechanisms, the category selectivity may be mediated by distinct top-down (task-dependent) and bottom-up (stimulus-dependent) mechanisms.     

Cortical representation of verb processing in sentence comprehension: number of complements, subcategorization, and thematic frames

The processing of various attributes of verbs is crucial for sentence comprehension. Verb attributes include the number of complements the verb selects, the number of different syntactic phrase types (subcategorization options), and the number of different thematic roles (thematic options). Two functional magnetic resonance imaging experiments investigated the cerebral location and pattern of activation of these attributes. Experiment 1 tested the effect of number of complements. Experiment 2 tested the number of options of subcategorization and of thematic frames. A group of mismatch verbs with different number of options for subcategorization and thematic frames was included to distinguish between the effects of these attributes. Fourteen Hebrew speakers performed a semantic decision task on auditorily presented sentences. Parametric analysis revealed graded activations in the left superior temporal gyrus and the left inferior frontal gyrus in correlation with the number of options. By contrast, the areas that correlated with the number of complements, the right precuneus and the right cingulate, were not conventionally linguistic. This suggests that processing the number of options is more specifically linguistic than processing the number of complements. The mismatch verbs showed a pattern of activation similar to that of the subcategorization group but unlike that of the thematic frames group. By implication, and contrary to claims by some linguists, subcategorization seems indispensable in verb processing.     

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.     

Response execution in lexical decision tasks obscures sex-specific lateralization effects in language processing: evidence from event-related potential measures during word reading

A common hypothesis about sex differences in language processing attributes these differences to a bilateral contribution of language-related brain areas in females and a left-hemispheric dominated activation in males. However, most imaging studies failed to find such a generalized lateralization effect and reported a left-lateralized activation in both sexes instead. In a previous semantic priming study, we found a sustained (approximately 190-640 ms) bilateral positivity in the ERP waveforms, which was larger for the female group. Word reading and lexical decision were confounded in that study. In the present study we used a delayed response to separate semantic processing from response selection and execution. The modification of the task design, together with a dense sensor array, showed that females developed a bilateral sustaining posterior positivity/frontal negativity during reading/semantic processing. In contrast, males showed an attenuated positivity at left posterior sites and an attenuated negativity at right frontal sites. This sex-specific lateralization effect disappeared during response processing, evoking a bilaterally distributed activation for both sexes (frontal negative and posterior positive), which was larger for the female subjects. We conclude that, at least under specific conditions, language processing evokes a bilateral activation in females and a lateralization effect in males. However, the processing of the response, which is dominated by a 'P300-like' component evoked by this process, evokes a larger activation in both sexes which obscures the sex-specific lateralization effect when semantic processing and response processing are not separated.     

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.     

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 bases of sentence comprehension: a fMRI examination of syntactic and lexical processing

One of the challenges to functional neuroimaging is to understand how the component processes of reading comprehension emerge from the neural activity in a network of brain regions. In this study, functional magnetic resonance imaging (fMRI) was used to examine lexical and syntactic processing in reading comprehension by independently manipulating the cognitive demand on each of the two processes of interest. After establishing a consistency with earlier research showing the involvement of the left perisylvian language areas in both lexical access and syntactic processing, the study produced new findings that are surprising in two ways: (i) the lexical and syntactic factors each impact not just individual areas, but they affect the activation in a network of left-hemisphere areas, suggesting that changing the computational load imposed by a given process produces a cascade of effects in a number of collaborating areas; and (ii) the lexical and syntactic factors usually interact in determining the amount of activation in each affected area, suggesting that comprehension processes that operate on different levels of language may nevertheless draw on a shared infrastructure of cortical resources. The results suggest that many processes in sentence comprehension involve multiple brain regions, and that many brain regions contribute to more than one comprehension process. The implication is that the language network consists of brain areas which each have multiple relative specializations and which engage in extensive interarea collaborations.     

Human neural systems for conceptual knowledge of proper object use: a functional magnetic resonance imaging study

Ideational apraxia is characterized by impaired knowledge of action concepts and proper object usage. The present functional magnetic resonance imaging study aimed at investigating the neural system underlying conceptual knowledge for proper object use in healthy subjects, when the effects of visuospatial properties and perceptual modality were taken into account. Subjects performed semantic decision tasks requiring retrieval of knowledge about either object functional purposes (functional task) or visuospatial object properties (visuospatial task) and perceptual control tasks. The semantic tasks were performed with pairs of either written object names or object drawings. Activation for the functional task in common for words and pictures, compared with the visuospatial and control tasks, was found in left parietal-temporal-occipital (PTO) junction, inferior frontal, anterior dorsal premotor, and presupplementary motor areas. Ventral inferior frontal cortex activation correlated negatively with reaction time in the functional condition. No specific activation characterized the visuospatial task compared with the functional task. The conceptual tasks, compared with the control tasks, demonstrated overlapping activation in left PTO junction, prefrontal, dorsal premotor, cuneus, and inferior temporal areas. These results outline the neural processes underlying conceptual knowledge for proper object use. The left ventral inferior frontal gyrus might facilitate behavioral decisions regarding functional/pragmatical object properties.     

Monitoring and the controlled processing of meaning: distinct prefrontal systems

Distinct prefrontal regions are specialized for the controlled processing of semantic information. We have dissociated components of this system used in semantic decision-making across different perceptual conditions. Nineteen subjects were presented with auditory word sequences, on which they made semantic or syllabic decisions, while neural activity was measured using PET. Contrasting the semantic with syllabic tasks, there was activation within left rostral prefrontal cortex (RPFC) when the stimuli were presented as clear speech, reducing when the stimuli were presented in acoustically degraded form. In contrast, activation of the right dorsolateral prefrontal cortex (DLPFC) was observed with the degraded stimuli, an effect that inversely correlated with accuracy on the task. We have thus demonstrated two prefrontal systems where activity is differentially modulated by the "quality" of information held in working memory. This dissociation is likely to represent an alteration in the type of cognitive operations employed during task performance, where left RPFC is activated during extensive semantic elaboration and right DLPFC is recruited as the monitoring demands, associated with items held in working memory, increase. The function of these separate systems is integrated during the performance of verbal problem-solving tasks although they are differentially sensitive to stimulus degradation.     

Medial temporal lobe involvement in an implicit memory task: evidence of collaborating implicit and explicit memory systems from FMRI and Alzheimer's disease

We used a prototype extraction task to assess implicit learning of a meaningful novel visual category. Cortical activation was monitored in young adults with functional magnetic resonance imaging. We observed occipital deactivation at test consistent with perceptually based implicit learning, and lateral temporal cortex deactivation reflecting implicit acquisition of the category's semantic nature. Medial temporal lobe (MTL) activation during exposure and test suggested involvement of explicit memory as well. Behavioral performance of Alzheimer's disease (AD) patients and healthy seniors was also assessed, and AD performance was correlated with gray matter volume using voxel-based morphometry. AD patients showed learning, consistent with preserved implicit memory, and confirming that AD patients' implicit memory is not limited to abstract patterns. However, patients were somewhat impaired relative to healthy seniors. Occipital and lateral temporal cortical volume correlated with successful AD patient performance, and thus overlapped with young adults' areas of deactivation. Patients' severe MTL atrophy precluded involvement of this region. AD patients thus appear to engage a cortically based implicit memory mechanism, whereas their relative deficit on this task may reflect their MTL disease. These findings suggest that implicit and explicit memory systems collaborate in neurologically intact individuals performing an ostensibly implicit memory task.     

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.     

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.     

FMRI study of emotional speech comprehension

Little is known about the neural correlates of affective prosody in the context of affective semantic discourse. We used functional magnetic resonance imaging to investigate this issue while subjects performed 1) affective classification of sentences having an affective semantic content and 2) grammatical classification of sentences with neutral semantic content. Sentences of each type were produced half by actors and half by a text-to-speech software lacking affective prosody. Compared with neutral sentences processing, sentences with affective semantic content--with or without affective prosody--led to an increase in activation of a left inferior frontal area involved in the retrieval of semantic knowledge. In addition, the posterior part of the left superior temporal sulcus (STS) together with the medial prefrontal cortex were recruited, although not activated by neutral sentences classification. Interestingly, these areas have been described as implicated during self-reflection or other's mental state inference that possibly occurred during the affective classification task. When affective prosody was present, additional rightward activations of the human-selective voice area and the posterior part of STS were observed, corresponding to the processing of speaker's voice emotional content. Accurate affective communication, central to social interactions, requires the cooperation of semantics, affective prosody, and mind-reading neural networks.     

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.     

Face repetition effects in implicit and explicit memory tests as measured by fMRI.

Recent parallels between neurophysiological and neuroimaging findings suggest that repeated stimulus processing produces decreased responses in brain regions associated with that processing--a 'repetition suppression' effect. In the present study, volunteers performed two tasks on repeated presentation of famous and unfamiliar faces during functional magnetic resonance imaging (fMRI). In the implicit task, they made fame-judgements (regardless of repetition); in the explicit task, they made episodic recognition judgements (regardless of familiarity). Only in the implicit task was repetition suppression observed: for famous faces in a right lateral fusiform region, and for both famous and unfamiliar faces in a left inferior occipital region. Repetition suppression is therefore not an automatic consequence of repeated perceptual processing of stimuli.