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 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).     

Separable effects of semantic priming and imageability on word processing in human cortex

Understanding the neural representation of semantic concepts is at the core of understanding human knowledge and experience. Competing cognitive theories suggest that these neural representations are based on either a unitary semantic code or on multiple semantic codes. We contrasted these theories using event-related fMRI in a semantic priming study. Pairs of words were presented that were either semantically related or unrelated and were either high or low imageable. The unitary view predicts that there should be little or no difference between neural activity evoked by high and low imageable words when presented in a related context, but large differences in neural activity when there is an unrelated context. In contrast to this view, we provide evidence for functionally and anatomically separable effects of context and imageability in human cortex, suggesting that semantic knowledge consists of multiple representational codes.     

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.     

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.     

Conjoint and extended neural networks for the computation of speech codes: the neural basis of selective impairment in reading words and pseudowords

The computation of speech codes (i.e. phonology) is an important aspect of word reading. Understanding the neural systems and mech- anisms underlying phonological processes provides a foundation for the investigation of language in the brain. We used high-resolution three-dimensional positron emission tomography (PET) to investigate neural systems essential for phonological processes. The burden of neural activities on the computation of speech codes was maximized by three rhyming tasks (rhyming words, pseudowords and words printed in mixed letter cases). Brain activation patterns associated with these tasks were compared with those of two baseline tasks involving visual feature detection. Results suggest strong left lateralized epicenters of neural activity in rhyming irrespective of gender. Word rhyming activated the same brain regions engaged in pseudoword rhyming, suggesting conjoint neural networks for phonological processing of words and pseudowords. However, pseudoword rhyming induced the largest change in cerebral blood flow and activated more voxels in the left posterior prefrontal regions and the left inferior occipital-temporal junction. In addition, pseudoword rhyming activated the left supramarginal gyrus, which was not apparent in word rhyming. These results suggest that rhyming pseudowords requires active participation of extended neural systems and networks not observed for rhyming words. The implications of the results on theories and models of visual word reading and on selective reading dysfunctions after brain lesions are discussed.     

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.     

Influence of syllabic lengthening on semantic processing in spoken French: behavioral and electrophysiological evidence

The present work investigates the relationship between semantic and prosodic (metric) processing in spoken language under 2 attentional conditions (semantic and metric tasks) by analyzing both behavioral and event-related potential (ERP) data. Participants listened to short sentences ending in semantically and/or metrically congruous or incongruous trisyllabic words. In the metric task, ERP data showed that metrically incongruous words elicited both larger early negative and late positive components than metrically congruous words, thereby demonstrating the online processing of the metric structure of words. Moreover, in the semantic task, metrically incongruous words also elicited an early negative component with similar latency and scalp distribution as the classical N400 component. This finding highlights the automaticity of metrical structure processing. Moreover, it demonstrates that violations of a word's metric structure may hinder lexical access and word comprehension. This interpretation is supported by the behavioral data showing that participants made more errors for semantically congruous but metrically incongruous words when they were attending to the semantic aspects of the sentence. Finally, the finding of larger N400 components to semantically incongruous than congruous words, in both the semantic and metric tasks, suggests that the N400 component reflects automatic aspects of semantic processing.     

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.     

Exploring the neural dynamics underpinning individual differences in sentence comprehension

This study used functional magnetic resonance imaging to investigate individual differences in the neural underpinnings of sentence comprehension, with a focus on neural adaptability (dynamic configuration of neural networks with changing task demands). Twenty-seven undergraduates, with varying working memory capacities and vocabularies, read sentences that were either syntactically simple or complex under conditions of varying extrinsic working memory demands (sentences alone or preceded by to-be-remembered words or nonwords). All readers showed greater neural adaptability when extrinsic working memory demands were low, suggesting that adaptability is related to resource availability. Higher capacity readers showed greater neural adaptability (greater increase in activation with increasing syntactic complexity) across conditions than did lower capacity readers. Higher capacity readers also showed better maintenance of or increase in synchronization of activation between brain regions as tasks became more demanding. Larger vocabulary was associated with more efficient use of cortical resources (reduced activation in frontal regions) in all conditions but was not associated with greater neural adaptability or synchronization. The distinct characterizations of verbal working memory capacity and vocabulary suggest that dynamic facets of brain function such as adaptability and synchronization may underlie individual differences in more general information processing abilities, whereas neural efficiency may more specifically reflect individual differences in language experience.     

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.     

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.     

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.     

Lateralization is predicted by reduced coupling from the left to right prefrontal cortex during semantic decisions on written words

Over 90% of people activate the left hemisphere more than the right hemisphere for language processing. Here, we show that the degree to which language is left lateralized is inversely related to the degree to which left frontal regions drive activity in homotopic right frontal regions. Lateralization was assessed in 60 subjects using functional magnetic resonance imaging (fMRI) activation for semantic decisions on verbal (written words) and nonverbal (pictures of objects) stimuli. Regional interactions between left and right ventral and dorsal frontal regions were assessed using dynamic causal modeling (DCM), random-effects Bayesian model selection at the family level, and Bayesian model averaging at the connection level. We found that 1) semantic decisions on words and pictures modulated interhemispheric coupling between the left and right dorsal frontal regions, 2) activation was more left lateralized for words than pictures, and 3) for words only, left lateralization was greater when the coupling from the left to right dorsal frontal cortex was reduced. These results have theoretical implications for understanding how left and right hemispheres communicate with one another during the processing of lateralized functions.     

Effects of domain-specific interference on brain activation associated with verbal working memory task performance

Previous neuroimaging studies have identified brain regions that underlie verbal working memory in humans. According to these studies a phonological store is located in the left inferior parietal cortex, and a complementary subvocal rehearsal mechanism is implemented by mostly left-hemispheric speech areas. In the present functional magnetic resonance imaging study, classical interfering and non-interfering dual-task situations were used to investigate further the neural correlates of verbal working memory. Verbal working memory performance under non-interfering conditions activated Broca's area, the left premotor cortex, the cortex along the left intraparietal sulcus and the right cerebellum, thus replicating the results from previous studies. By contrast, no significant memory- related activation was found in these areas when silent articulatory suppression prevented the subjects from rehearsal. Instead, this non-articulatory maintenance of phonological information was associated with enhanced activity in several other, particularly anterior prefrontal and inferior parietal, brain areas. These results suggest that phonological storage may be a function of a complex prefronto-parietal network, and not localized in only one, parietal brain region. Further possible implications for the functional organization of human working memory are discussed.     

Analogical reasoning and prefrontal cortex: evidence for separable retrieval and integration mechanisms

The present study examined the contributions of prefrontal cortex (PFC) subregions to two component processes underlying verbal analogical reasoning: semantic retrieval and integration. Event-related functional magnetic resonance imaging data were acquired while subjects performed propositional analogy and semantic decision tasks. On each trial, subjects viewed a pair of words (pair 1), followed by an instructional cue and a second word pair (pair 2). On analogy trials, subjects evaluated whether pair 2 was semantically analogous to pair 1. On semantic trials, subjects indicated whether the pair 2 words were semantically related to each other. Thus, analogy--but not semantic--trials required integration across multiple retrieved relations. To identify regions involved in semantic retrieval, we manipulated the associative strength of pair 1 words in both tasks. Anterior left inferior PFC (aLIPC) was modulated by associative strength, consistent with a role in controlled semantic retrieval. Left frontopolar cortex was insensitive to associative strength, but was more sensitive to integration demands than was aLIPC, consistent with a role in integrating the products of semantic retrieval to evaluate whether distinct representations are analogous. Right dorsolateral PFC exhibited a profile consistent with a role in response selection rather than retrieval or integration. These findings indicate that verbal analogical reasoning depends on multiple, PFC-mediated computations.     

Fractionating language: different neural subsystems with different sensitive periods.

Theoretical considerations and psycholinguistic studies have alternatively provided criticism and support for the proposal that semantic and grammatical functions are distinct subprocesses within the language domain. Neurobiological evidence concerning this hypothesis was sought by (1) comparing, in normal adults, event-related brain potentials (ERPs) elicited by words that provide primarily semantic information (open class) and grammatical information (closed class) and (2) comparing the effects of the altered early language experience of congenitally deaf subjects on ERPs to open and closed class words. In normal-hearing adults, the different word types elicited qualitatively different ERPs that were compatible with the hypothesized different roles of the word classes in language processing. In addition, whereas ERP indices of semantic processing were virtually identical in deaf and hearing subjects, those linked to grammatical processes were markedly different in deaf and hearing subjects. The results suggest that nonidentical neural systems with different developmental vulnerabilities mediate these different aspects of language. More generally, these results provide neurobiological support for the distinction between semantic and grammatical functions.     

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.     

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.