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1.  Development of a selective left-hemispheric fronto-temporal network for processing syntactic complexity in language comprehension 
Neuropsychologia  2016;83:274-282.
The development of language comprehension abilities in childhood is closely related to the maturation of the brain, especially the ability to process syntactically complex sentences. Recent studies proposed that the fronto-temporal connection within left perisylvian regions, supporting the processing of syntactically complex sentences, is still immature at preschool age. In the current study, resting state functional magnetic resonance imaging data were acquired from typically developing 5-year-old children and adults to shed further light on the brain functional development. Children additionally performed a behavioral syntactic comprehension test outside the scanner. The amplitude of low-frequency fluctuations was analyzed in order to identify the functional correlation networks of language-relevant brain regions. Results showed an intrahemispheric correlation between left inferior frontal gyrus (IFG) and left posterior superior temporal sulcus (pSTS) in adults, whereas an interhemispheric correlation between left IFG and its right-hemispheric homolog was predominant in children. Correlation analysis between resting-state functional connectivity and sentence processing performance in 5-year-olds revealed that local connectivity within the left IFG is associated with competence of processing syntactically simple canonical sentences, while long-range connectivity between IFG and pSTS in left hemisphere is associated with competence of processing syntactically relatively more complex non-canonical sentences. The present developmental data suggest that a selective left fronto-temporal connectivity network for processing complex syntax is already in functional connection at the age of 5 years when measured in a non-task situation. The correlational findings provide new insight into the relationship between intrinsic functional connectivity and syntactic language abilities in preschool children.
Highlights
•resting state ALFF correlated in adults between left IFG and left pSTS.•resting state ALFF correlated in children between left IFG and right homolog area.•intrahemispheric connectivity co-varies with syntactic processing skills in children.
doi:10.1016/j.neuropsychologia.2015.09.003
PMCID: PMC4780430  PMID: 26352468
Language development; Resting-state fMRI; Amplitude of low-frequency fluctuation; Functional connectivity; Syntactic complexity
2.  The Dorsal Rather than Ventral Pathway Better Reflects Individual Syntactic Abilities in Second Language 
The left inferior frontal gyrus (IFG) has been reported to be critically involved in syntactic processing, not only in first language (L1), but in second language (L2). Indeed, the leftward lateralization of the IFG has been shown to be correlated with the performance of a syntactic task in L2. Given that posterior language-related regions are systematically connected with the left IFG, the next question is which of the dorsal and ventral pathways is more critical to the individual syntactic abilities in L2. Here we used diffusion magnetic resonance imaging (MRI) and tractography with newly developed semi-automatic methods of defining seeds and selecting regions of interest (ROIs). We calculated mean thickness and fractional anisotropy (FA) in each ROI for the arcuate fasciculus (Arcuate) of the dorsal pathway, as well as for the inferior fronto-occipital fasciculus (IFOF) of the ventral pathway. In Experiment I, we performed partial correlation analyses between FA and the accuracy of the syntactic task, removing the effects of the accuracy of a spelling task, gender, and handedness. Among the two pathways in each hemisphere, only FA of the left Arcuate was significantly correlated with individual accuracy of the syntactic task. In Experiment II, we recruited monozygotic twins and examined to what extent their L2 abilities and their structural properties were similar. Within twin pairs, the highest significant correlation was observed for reaction times of the spelling task, while the correlation for the accuracy of the syntactic task was marginal; these two correlation coefficients were significantly different. Moreover, the thickness of the left Arcuate was highly correlated within pairs, while its FA, as well as the thickness/FA in the ventral pathways, was not significantly correlated. The correlation coefficient for the thickness of the left Arcuate was significantly larger than that of the left IFOF. These results suggest that the thickness of the left Arcuate is more associated with the shared genetic/environmental factors, whereas both of mutually correlated FA in the left Arcuate and individual syntactic abilities in L2 may be less prone to these shared factors.
doi:10.3389/fnhum.2016.00295
PMCID: PMC4906050  PMID: 27378889
diffusion MRI; white matter; dorsal and ventral pathways; language acquisition; syntax; monozygotic twins
3.  Cerebral Blood Flow and fMRI BOLD Auditory Language Activation in Temporal Lobe Epilepsy 
Epilepsia  2012;53(4):631-638.
Purpose
BOLD fMRI, an important research and clinical tool, depends on relatively greater transient increases in (cerebral blood flow) rCBF than CMRO2 during neural activity. We investigated whether reduced resting rCBF in patients with TLE affects BOLD signal during fMRI language mapping.
Methods
We used [15O] water PET to measure rCBF, and 3T EPI BOLD fMRI with an auditory description decision task in 33 patients with temporal lobe epilepsy (16 men; age 33.6±10.6 years; epilepsy onset 14.8±10.6 years; mean duration 18.8±13.2 years; 23 left focus, 10 right focus). Anatomical regions drawn on structural MRI, based on the Wake Forest PickAtlas, included Wernicke’s area (WA), inferior frontal gyrus (IFG), middle frontal gyrus (MFG), and hippocampus (HC)]. Laterality indices (LI), and Asymmetry Indices (AI), were calculated on co-registered fMRI and PET.
Key findings
Twelve patients had mesial temporal sclerosis (7 left), two a tumor or malformation of cortical development (both left), one a right temporal cyst and 18 normal MRI (14 left). Decreasing relative left WA CBF correlated with decreased left IFG voxel activation and decreasing left IFG LI. However, CBF WA AI was not related to left WA voxel activation itself or WA LI. There was a weak positive correlation between absolute CBF and fMRI activation in left IFG, right IFG, and left WA. Patients with normal and abnormal MRI did not differ in fMRI activation or rCBF AI.
Significance
Reduced WA rCBF is associated with reduced fMRI activation in IFG but not WA itself, suggesting distributed network effects, but not impairment of underlying BOLD response. Hypoperfusion in TLE does not affect fMRI clinical value.
doi:10.1111/j.1528-1167.2012.03403.x
PMCID: PMC3319237  PMID: 22332720
PET; CBF; fMRI; TLE; language; BOLD
4.  Interhemispheric Plasticity following Intermittent Theta Burst Stimulation in Chronic Poststroke Aphasia  
Neural Plasticity  2016;2016:4796906.
The effects of noninvasive neurostimulation on brain structure and function in chronic poststroke aphasia are poorly understood. We investigated the effects of intermittent theta burst stimulation (iTBS) applied to residual language-responsive cortex in chronic patients using functional and anatomical MRI data acquired before and after iTBS. Lateralization index (LI) analyses, along with comparisons of inferior frontal gyrus (IFG) activation and connectivity during covert verb generation, were used to assess changes in cortical language function. Voxel-based morphometry (VBM) was used to assess effects on regional grey matter (GM). LI analyses revealed a leftward shift in IFG activity after treatment. While left IFG activation increased, right IFG activation decreased. Changes in right to left IFG connectivity during covert verb generation also decreased after iTBS. Behavioral correlations revealed a negative relationship between changes in right IFG activation and improvements in fluency. While anatomical analyses did not reveal statistically significant changes in grey matter volume, the fMRI results provide evidence for changes in right and left IFG function after iTBS. The negative relationship between post-iTBS changes in right IFG activity during covert verb generation and improvements in fluency suggests that iTBS applied to residual left-hemispheric language areas may reduce contralateral responses related to language production and facilitate recruitment of residual language areas after stroke.
doi:10.1155/2016/4796906
PMCID: PMC4736997  PMID: 26881111
5.  Preschoolers' brains rely on semantic cues prior to the mastery of syntax during sentence comprehension 
Neuroimage  2016;126:256-266.
Sentence comprehension requires the integration of both syntactic and semantic information, the acquisition of which seems to have different trajectories in the developing brain. Using functional magnetic resonance imaging, we examined the neural correlates underlying syntactic and semantic processing during auditory sentence comprehension as well as its development in preschool children by manipulating case marking and animacy hierarchy cues, respectively. A functional segregation was observed within Broca's area in the left inferior frontal gyrus for adults, where the pars opercularis was involved in syntactic processing and the pars triangularis in semantic processing. By contrast, five-year-old children sensitive to animacy hierarchy cues showed diffuse activation for semantic processing in the left inferior frontal and posterior temporal cortices. While no main effect of case marking was found in the left fronto-temporal language network, children with better syntactic skills showed greater neural responses for syntactically complex sentences, most prominently in the posterior superior temporal cortex. The current study provides both behavioral and neural evidence that five-year-old children compared to adults rely more on semantic information than on syntactic cues during sentence comprehension, but with the development of syntactic abilities, their brain activation in the left fronto-temporal network increases for syntactic processing.
Highlights
•Adults showed a functional segregation in Broca's area for syntax and semantics.•Brodmann Area (BA) 44 was involved in syntactic and BA 45 in semantic processing.•Preschoolers relied more on semantic animacy than on syntactic case marking cues.•Children showed adult-like left fronto-temporal activation for semantic processing.•The left fronto-temporal activation for syntax correlated with syntactic abilities.
doi:10.1016/j.neuroimage.2015.10.036
PMCID: PMC4739511  PMID: 26497266
fMRI; Syntax; Semantics; Language development; Pars opercularis; Pars triangularis
6.  A little more conversation – the influence of communicative context on syntactic priming in brain and behavior 
We report on an functional magnetic resonance imaging (fMRI) syntactic priming experiment in which we measure brain activity for participants who communicate with another participant outside the scanner. We investigated whether syntactic processing during overt language production and comprehension is influenced by having a (shared) goal to communicate. Although theory suggests this is true, the nature of this influence remains unclear. Two hypotheses are tested: (i) syntactic priming effects (fMRI and behavioral) are stronger for participants in the communicative context than for participants doing the same experiment in a non-communicative context, and (ii) syntactic priming magnitude (behavioral) is correlated with the syntactic priming magnitude of the speaker’s communicative partner. Results showed that across conditions, participants were faster to produce sentences with repeated syntax, relative to novel syntax. This behavioral result converged with the fMRI data: we found repetition suppression effects in the left insula extending into left inferior frontal gyrus (BA 47/45), left middle temporal gyrus (BA 21), left inferior parietal cortex (BA 40), left precentral gyrus (BA 6), bilateral precuneus (BA 7), bilateral supplementary motor cortex (BA 32/8), and right insula (BA 47). We did not find support for the first hypothesis: having a communicative intention does not increase the magnitude of syntactic priming effects (either in the brain or in behavior) per se. We did find support for the second hypothesis: if speaker A is strongly/weakly primed by speaker B, then speaker B is primed by speaker A to a similar extent. We conclude that syntactic processing is influenced by being in a communicative context, and that the nature of this influence is bi-directional: speakers are influenced by each other.
doi:10.3389/fpsyg.2014.00208
PMCID: PMC3957420  PMID: 24672499
syntax; syntactic priming; overt production; comprehension; communication; fMRI; behavior
7.  Development of the Intrinsic Language Network in Preschool Children from Ages 3 to 5 Years 
PLoS ONE  2016;11(11):e0165802.
Resting state studies of spontaneous fluctuations in the functional magnetic resonance imaging (fMRI) blood oxygen level dependent signal have shown great potential in mapping the intrinsic functional connectivity of the human brain underlying cognitive functions. The aim of the present study was to explore the developmental changes in functional networks of the developing human brain exemplified with the language network in typically developing preschool children. To this end, resting-sate fMRI data were obtained from native Chinese children at ages of 3 and 5 years, 15 in each age group. Resting-state functional connectivity (RSFC) was analyzed for four regions of interest; these are the left and right anterior superior temporal gyrus (aSTG), left posterior superior temporal gyrus (pSTG), and left inferior frontal gyrus (IFG). The comparison of these RSFC maps between 3- and 5-year-olds revealed that RSFC decreases in the right aSTG and increases in the left hemisphere between aSTG seed and IFG, between pSTG seed and IFG, as well as between IFG seed and posterior superior temporal sulcus. In a subsequent analysis, functional asymmetry of the language network seeding in aSTG, pSTG and IFG was further investigated. The results showed an increase of left lateralization in both RSFC of pSTG and of IFG from ages 3 to 5 years. The IFG showed a leftward lateralized trend in 3-year-olds, while pSTG demonstrated rightward asymmetry in 5-year-olds. These findings suggest clear developmental trajectories of the language network between 3- and 5-year-olds revealed as a function of age, characterized by increasing long-range connections and dynamic hemispheric lateralization with age. Our study provides new insights into the developmental changes of a well-established functional network in young children and also offers a basis for future cross-culture and cross-age studies of the resting-state language network.
doi:10.1371/journal.pone.0165802
PMCID: PMC5094780  PMID: 27812160
8.  Neural Correlates of Processing Passive Sentences 
Brain Sciences  2013;3(3):1198-1214.
Previous research has shown that comprehension of complex sentences involving wh-movement (e.g., object-relative clauses) elicits activation in the left inferior frontal gyrus (IFG) and left posterior temporal cortex. However, relatively little is known about the neural correlates of processing passive sentences, which differ from other complex sentences in terms of representation (i.e., noun phrase (NP)-movement) and processing (i.e., the time course of syntactic reanalysis). In the present study, 27 adults (14 younger and 13 older) listened to passive and active sentences and performed a sentence-picture verification task using functional Magnetic Resonance Imaging (fMRI). Passive sentences, relative to active sentences, elicited greater activation in bilateral IFG and left temporo-occipital regions. Participant age did not significantly affect patterns of activation. Consistent with previous research, activation in left temporo-occipital cortex likely reflects thematic reanalysis processes, whereas, activation in the left IFG supports processing of complex syntax (i.e., NP-movement). Right IFG activation may reflect syntactic reanalysis processing demands associated with the sentence-picture verification task.
doi:10.3390/brainsci3031198
PMCID: PMC4061884  PMID: 24961525
fMRI; sentence processing; syntactic processing; thematic processing
9.  Syntactic structure building in the anterior temporal lobe during natural story listening 
Brain and Language  2010;120(2):163-173.
The neural basis of syntax is a matter of substantial debate. In particular, the inferior frontal gyrus (IFG), or Broca s area, has been prominently linked to syntactic processing, but anterior temporal lobe has been reported to be activated instead of IFG when manipulating the presence of syntactic structure. These findings are difficult to reconcile because they rely on different laboratory tasks which tap into distinct computations, and may only indirectly relate to natural sentence processing. Here we assessed neural correlates of syntactic structure building in natural language comprehension, free from artificial task demands. Subjects passively listened to Alice in Wonderland during functional magnetic resonance imaging and we correlated brain activity with a word-byword measure of the amount syntactic structure analyzed. Syntactic structure building correlated with activity in the left anterior temporal lobe, but there was no evidence for a correlation between syntactic structure building and activity in inferior frontal areas. Our results suggest that the anterior temporal lobe computes syntactic structure under natural conditions.
doi:10.1016/j.bandl.2010.04.002
PMCID: PMC2947556  PMID: 20472279
Language; Neuroimaging; Syntax; aTL
10.  Task-dependent and task-independent neurovascular responses to syntactic processing⋆ 
The neural basis for syntactic processing was studied using event-related fMRI to determine the locations of BOLD signal increases in the contrast of syntactically complex sentences with center-embedded, object-extracted relative clauses and syntactically simple sentences with right-branching, subject-extracted relative clauses in a group of 15 participants in three tasks. In a sentence verification task, participants saw a target sentence in one of these two syntactic forms, followed by a probe in a simple active form, and determined whether the probe expressed a proposition in the target. In a plausibility judgment task, participants determined whether a sentence in one of these two syntactic forms was plausible or implausible. Finally, in a non-word detection task, participants determined whether a sentence in one of these two syntactic forms contained only real words or a non-word. BOLD signal associated with the syntactic contrast increased in the left posterior inferior frontal gyrus in non-word detection and in a widespread set of areas in the other two tasks. We conclude that the BOLD activity in the left posterior inferior frontal gyrus reflects syntactic processing independent of concurrent cognitive operations and the more widespread areas of activation reflect the use of strategies and the use of the products of syntactic processing to accomplish tasks.
doi:10.1016/j.cortex.2006.06.005
PMCID: PMC2427191  PMID: 18387556
fMRI syntax; Task effects
11.  Left inferior frontal cortex and syntax: function, structure and behaviour in patients with left hemisphere damage 
Brain  2011;134(2):415-431.
For the past 150 years, neurobiological models of language have debated the role of key brain regions in language function. One consistently debated set of issues concern the role of the left inferior frontal gyrus in syntactic processing. Here we combine measures of functional activity, grey matter integrity and performance in patients with left hemisphere damage and healthy participants to ask whether the left inferior frontal gyrus is essential for syntactic processing. In a functional neuroimaging study, participants listened to spoken sentences that either contained a syntactically ambiguous or matched unambiguous phrase. Behavioural data on three tests of syntactic processing were subsequently collected. In controls, syntactic processing co-activated left hemisphere Brodmann areas 45/47 and posterior middle temporal gyrus. Activity in a left parietal cluster was sensitive to working memory demands in both patients and controls. Exploiting the variability in lesion location and performance in the patients, voxel-based correlational analyses showed that tissue integrity and neural activity—primarily in left Brodmann area 45 and posterior middle temporal gyrus—were correlated with preserved syntactic performance, but unlike the controls, patients were insensitive to syntactic preferences, reflecting their syntactic deficit. These results argue for the essential contribution of the left inferior frontal gyrus in syntactic analysis and highlight the functional relationship between left Brodmann area 45 and the left posterior middle temporal gyrus, suggesting that when this relationship breaks down, through damage to either region or to the connections between them, syntactic processing is impaired. On this view, the left inferior frontal gyrus may not itself be specialized for syntactic processing, but plays an essential role in the neural network that carries out syntactic computations.
doi:10.1093/brain/awq369
PMCID: PMC3030769  PMID: 21278407
aphasia; Broca’s area; syntax; language networks; stroke
12.  Left Inferior Frontal Activations Depending on the Canonicity Determined by the Argument Structures of Ditransitive Sentences: An MEG Study 
PLoS ONE  2012;7(5):e37192.
To elucidate the relationships between syntactic and semantic processes, one interesting question is how syntactic structures are constructed by the argument structure of a verb, where each argument corresponds to a semantic role of each noun phrase (NP). Here we examined the effects of possessivity [sentences with or without a possessor] and canonicity [canonical or noncanonical word orders] using Japanese ditransitive sentences. During a syntactic decision task, the syntactic structure of each sentence would be constructed in an incremental manner based on the predicted argument structure of the ditransitive verb in a verb-final construction. Using magnetoencephalography, we found a significant canonicity effect on the current density in the left inferior frontal gyrus (IFG) at 530–550 ms after the verb onset. This effect was selective to canonical sentences, and significant even when the precedent NP was physically identical. We suggest that the predictive effects associated with syntactic processing became larger for canonical sentences, where the NPs and verb were merged with a minimum structural distance, leading to the left IFG activations. For monotransitive and intransitive verbs, in which structural computation of the sentences was simpler than that of ditransitive sentences, we observed a significant effect selective to noncanonical sentences in the temporoparietal regions during 480–670 ms. This effect probably reflects difficulty in semantic processing of noncanonical sentences. These results demonstrate that the left IFG plays a predictive role in syntactic processing, which depends on the canonicity determined by argument structures, whereas other temporoparietal regions would subserve more semantic aspects of sentence processing.
doi:10.1371/journal.pone.0037192
PMCID: PMC3358340  PMID: 22629366
13.  Higher Language Ability is Related to Angular Gyrus Activation Increase During Semantic Processing, Independent of Sentence Incongruency 
This study investigates the relation between individual language ability and neural semantic processing abilities. Our aim was to explore whether high-level language ability would correlate to decreased activation in language-specific regions or rather increased activation in supporting language regions during processing of sentences. Moreover, we were interested if observed neural activation patterns are modulated by semantic incongruency similarly to previously observed changes upon syntactic congruency modulation. We investigated 27 healthy adults with a sentence reading task—which tapped language comprehension and inference, and modulated sentence congruency—employing functional magnetic resonance imaging (fMRI). We assessed the relation between neural activation, congruency modulation, and test performance on a high-level language ability assessment with multiple regression analysis. Our results showed increased activation in the left-hemispheric angular gyrus extending to the temporal lobe related to high language ability. This effect was independent of semantic congruency, and no significant relation between language ability and incongruency modulation was observed. Furthermore, there was a significant increase of activation in the inferior frontal gyrus (IFG) bilaterally when the sentences were incongruent, indicating that processing incongruent sentences was more demanding than processing congruent sentences and required increased activation in language regions. The correlation of high-level language ability with increased rather than decreased activation in the left angular gyrus, a region specific for language processing, is opposed to what the neural efficiency hypothesis would predict. We can conclude that no evidence is found for an interaction between semantic congruency related brain activation and high-level language performance, even though the semantic incongruent condition shows to be more demanding and evoking more neural activation.
doi:10.3389/fnhum.2016.00110
PMCID: PMC4786547  PMID: 27014040
fMRI; semantic processing; congruency; sentence reading; language ability; inferior frontal gyrus; angular gyrus
14.  Articulation-based sound perception in verbal repetition: a functional NIRS study 
Verbal repetition is a fundamental language capacity where listening and speaking are inextricably coupled with each other. We have recently reported that the left inferior frontal gyrus (IFG) harbors articulation-based codes, as evidenced by activation during repetition of meaningless speech sounds, i.e., pseudowords. In this study, we aimed at confirming this finding and further investigating the possibility that sound perception as well as articulation is subserved by neural circuits in this region. Using functional near-infrared spectroscopy (fNIRS), we monitored changes of hemoglobin (Hb) concentration at IFG bilaterally, while subjects verbally repeated pseudowords and words. The results revealed that the proportion of oxygenated hemoglobin (O2Hb) over total Hb was significantly higher at the left IFG during repetition of pseudowords than that of words, replicating the observation by functional MRI and indicating that the region processes articulatory codes for verbal repetition. More importantly for this study, hemodynamic modulations were observed at both IFG during passive listening without repetition to various sounds, including natural environmental sounds, animal vocalizations, and human non-speech sounds. Furthermore, the O2Hb concentration increased at the left IFG but decreased at the right IFG for both speech and non-speech sounds. These findings suggest that both speech and non-speech sounds may be processed and maintained by a neural mechanism for sensorimotor integration using articulatory codes at the left IFG.
doi:10.3389/fnhum.2013.00540
PMCID: PMC3763229  PMID: 24046741
verbal repetition; inferior frontal gyrus; articulation-based codes; sound perception; functional near-infrared spectroscopy; hemoglobin concentration; sensorimotor integration
15.  Aberrant network integrity of the inferior frontal cortex in women with anorexia nervosa 
NeuroImage : Clinical  2014;4:615-622.
Neuroimaging studies investigating the neural profile of anorexia nervosa (AN) have revealed a predominant imbalance between the reward and inhibition systems of the brain, which are also hallmark characteristics of the disorder. However, little is known whether these changes can also be determined independent of task condition, using resting-state functional magnetic resonance imaging, in currently ill AN patients.
Therefore the aim of our study was to investigate resting-state connectivity in AN patients (n = 12) compared to healthy athlete (n = 12) and non-athlete (n = 14) controls. For this purpose, we used degree centrality to investigate functional connectivity of the whole-brain network and then Granger causality to analyze effective connectivity (EC), to understand directional aspects of potential alterations.
We were able to show that the bilateral inferior frontal gyrus (IFG) is a region of special functional importance within the whole-brain network, in AN patients, revealing reduced functional connectivity compared to both healthy control groups. Furthermore, we found decreased EC from the right IFG to the midcingulum and increased EC from the bilateral orbitofrontal gyrus to the right IFG. For the left IFG, we only observed increased EC from the bilateral insula to the left IFG.
These results suggest that AN patients have reduced connectivity within the cognitive control system of the brain and increased connectivity within regions important for salience processing. Due to its fundamental role in inhibitory behavior, including motor response, altered integrity of the inferior frontal cortex could contribute to hyperactivity in AN.
Highlights
•We evaluate resting-state functional (FC) and effective (EC) connectivity.•We compare anorexia nervosa (AN) patients with healthy controls.•AN patients show reduced FC in the inferior frontal gyrus (IFG).•AN patients show reduced EC from the IFG and increased EC to the IFG.•Altered FC patterns correlate with physical activity.
doi:10.1016/j.nicl.2014.04.002
PMCID: PMC4053633  PMID: 24936412
Anorexia nervosa; Functional connectivity; Effective connectivity; Resting-state fMRI
16.  Shifted Inferior Frontal Laterality in Women with Major Depressive Disorder is Related to Emotion Processing Deficits 
Psychological medicine  2013;43(7):1433-1445.
Background
Facial emotion perception (FEP) is a critical human skill for successful social interaction, and a substantial body of literature suggests that explicit FEP is disrupted in Major Depressive Disorder (MDD). Prior research suggests that weakness in FEP may be an important phenomenon underlying patterns of emotion processing challenges in MDD and the disproportionate frequency of MDD in women.
Method
Women with (n = 24) and without (n = 22) MDD, equivalent in age and education, completed a FEP task during fMRI.
Results
The MDD group exhibited greater extents of frontal, parietal, and subcortical activation compared to the control group during FEP. Activation in inferior frontal gyrus (IFG) appeared shifted from a left > right pattern observed in healthy women to a bilateral pattern in MDD women. The ratio of left to right suprathreshold IFG voxels in healthy controls was nearly 3:1, whereas in the MDD group, there was a greater percent of suprathreshold IFG voxels bilaterally, with no leftward bias. In MDD, relatively greater activation in right IFG compared to left IFG (ratio score) was present and predicted FEP accuracy (r = .56, p < .004), with an inverse relationship observed between FEP and subgenual cingulate activation (r = −.46, p = .02).
Conclusions
This study links, for the first time, disrupted IFG activation laterality and increased subgenual cingulate activation with deficient FEP in women with MDD, providing an avenue for imaging-to-assessment translational applications in MDD.
doi:10.1017/S0033291712002176
PMCID: PMC4380502  PMID: 23298715
emotion; faces; depression; neuroimaging; laterality; women; identification
17.  Neural basis of understanding communicative actions: Changes associated with knowing the actor’s intention and the meanings of the actions 
Neuropsychologia  2016;81:230-237.
People can communicate by using hand actions, e.g., signs. Understanding communicative actions requires that the observer knows that the actor has an intention to communicate and the meanings of the actions. Here, we investigated how this prior knowledge affects processing of observed actions. We used functional MRI to determine changes in action processing when non-signers were told that the observed actions are communicative (i.e., signs) and learned the meanings of half of the actions. Processing of hand actions activated the left and right inferior frontal gyrus (IFG, BA 44 and 45) when the communicative intention of the actor was known, even when the meanings of the actions remained unknown. These regions were not active when the observers did not know about the communicative nature of the hand actions. These findings suggest that the left and right IFG play a role in understanding the intention of the actor, but do not process visuospatial features of the communicative actions. Knowing the meanings of the hand actions further enhanced activity in the anterior part of the IFG (BA 45), the inferior parietal lobule and posterior inferior and middle temporal gyri in the left hemisphere. These left-hemisphere language regions could provide a link between meanings and observed actions. In sum, the findings provide evidence for the segregation of the networks involved in the neural processing of visuospatial features of communicative hand actions and those involved in understanding the actor’s intention and the meanings of the actions.
Highlights
•Participants observed hand actions before and after learning that they are signs.•Learning-induced changes in brain activity measured using fMRI.•No activity in mirror neuron system when actions were not known to be communicative.•Knowing the actor’s intention to communicate activated IFG and IPL.•Knowing meanings of the actions increased activity in left IFG (BA 45), IPL and MTG.
doi:10.1016/j.neuropsychologia.2016.01.002
PMCID: PMC4749541  PMID: 26752450
Action observation; Mirror neuron system; Mirror neurons; Sign language; Communication; Inferior frontal cortex; Inferior parietal lobule
18.  Musical Expertise Modulates Early Processing of Syntactic Violations in Language 
Syntactic violations in speech and music have been shown to elicit an anterior negativity (AN) as early as 100 ms after violation onset and a posterior positivity that peaks at roughly 600 ms (P600/LPC). The language AN is typically reported as left-lateralized (LAN), whereas the music AN is typically reported as right-lateralized (RAN). However, several lines of evidence suggest syntactic processing of language and music rely on overlapping neural systems. The current study tested the hypothesis that syntactic processing of speech and music share neural resources by examining whether musical proficiency modulates ERP indices of linguistic syntactic processing. ERPs were measured in response to syntactic violations in sentences and chord progressions in musicians and non-musicians. Violations in speech were insertion errors in normal and semantically impoverished English sentences. Violations in music were out-of-key chord substitutions from distantly and closely related keys. Phrase-structure violations elicited an AN and P600 in both groups. Harmonic violations elicited an LPC in both groups, blatant harmonic violations also elicited a RAN in musicians only. Cross-domain effects of musical proficiency were similar to previously reported within-domain effects of linguistic proficiency on the distribution of the language AN; syntactic violations in normal English sentences elicited a LAN in musicians and a bilateral AN in non-musicians. The late positivities elicited by violations differed in latency and distribution between domains. These results suggest that initial processing of syntactic violations in language and music relies on shared neural resources in the general population, and that musical expertise results in more specialized cortical organization of syntactic processing in both domains.
doi:10.3389/fpsyg.2012.00603
PMCID: PMC3542524  PMID: 23335905
expertise; syntax; music; language; sentence processing; ERAN; LAN; P600
19.  Subliminal enhancement of predictive effects during syntactic processing in the left inferior frontal gyrus: an MEG study 
Predictive syntactic processing plays an essential role in language comprehension. In our previous study using Japanese object-verb (OV) sentences, we showed that the left inferior frontal gyrus (IFG) responses to a verb increased at 120–140 ms after the verb onset, indicating predictive effects caused by a preceding object. To further elucidate the automaticity of the predictive effects in the present magnetoencephalography study, we examined whether a subliminally presented verb (“subliminal verb”) enhanced the predictive effects on the sentence-final verb (“target verb”) unconsciously, i.e., without awareness. By presenting a subliminal verb after the object, enhanced predictive effects on the target verb would be detected in the OV sentences when the transitivity of the target verb matched with that of the subliminal verb (“congruent condition”), because the subliminal verb just after the object could determine the grammaticality of the sentence. For the OV sentences under the congruent condition, we observed significantly increased left IFG responses at 140–160 ms after the target verb onset. In contrast, responses in the precuneus and midcingulate cortex (MCC) were significantly reduced for the OV sentences under the congruent condition at 110–140 and 280–300 ms, respectively. By using partial Granger causality analyses for the OV sentences under the congruent condition, we revealed a bidirectional interaction between the left IFG and MCC at 60–160 ms, as well as a significant influence from the MCC to the precuneus. These results indicate that a top-down influence from the left IFG to the MCC, and then to the precuneus, is critical in syntactic decisions, whereas the MCC shares its task-set information with the left IFG to achieve automatic and predictive processes of syntax.
doi:10.3389/fnsys.2014.00217
PMCID: PMC4217366  PMID: 25404899
MEG; sentence processing; syntax; frontal cortex; prediction; consciousness
20.  The Neuronal Correlates of Indeterminate Sentence Comprehension: An fMRI Study 
Sentences such as The author started the book are indeterminate because they do not make explicit what the subject (the author) started doing with the object (the book). In principle, indeterminate sentences allow for an infinite number of interpretations. One theory, however, assumes that these sentences are resolved by semantic coercion, a linguistic process that forces the noun book to be interpreted as an activity (e.g., writing the book) or by a process that interpolates this activity information in the resulting enriched semantic composition. An alternative theory, pragmatic, assumes classical semantic composition, whereby meaning arises from the denotation of words and how they are combined syntactically, with enrichment obtained via pragmatic inferences beyond linguistic-semantic processes. Cognitive neuroscience studies investigating the neuroanatomical and functional correlates of indeterminate sentences have shown activations either at the ventromedial pre-frontal cortex (vmPFC) or at the left inferior frontal gyrus (L-IFG). These studies have supported the semantic coercion theory assuming that one of these regions is where enriched semantic composition takes place. Employing functional magnetic resonance imaging (fMRI), we found that indeterminate sentences activate bilaterally the superior temporal gyrus (STG), the right inferior frontal gyrus (R-IFG), and the anterior cingulate cortex (ACC), more so than control sentences (The author wrote the book). Activation of indeterminate sentences exceeded that of anomalous sentences (…drank the book) and engaged more left- and right-hemisphere areas than other sentence types. We suggest that the widespread activations for indeterminate sentences represent the deployment of pragmatic-inferential processes, which seek to enrich sentence content without necessarily resorting to semantic coercion.
doi:10.3389/fnhum.2016.00614
PMCID: PMC5168646  PMID: 28066204
indeterminate sentences; semantic coercion; compositionality; pragmatics; fMRI; inferior frontal gyrus; superior temporal gyrus; anterior cingulate cortex
21.  Semantic Processing and Thought Disorder in Childhood-Onset Schizophrenia: Insights from fMRI 
Journal of neurolinguistics  2010;23(3):204-222.
Impairments in language processing and thought disorder are core symptoms of schizophrenia. Here we used fMRI to investigate functional abnormalities in the neural networks subserving sentence-level language processing in childhood-onset schizophrenia (COS). Fourteen children with COS (mean age: 13.34; IQ: 95) and 14 healthy controls (HC; mean age: 12.37; IQ: 104) underwent fMRI while performing a semantic judgment task previously shown to differentially engage semantic and syntactic processes. We report four main results. First, different patterns of functional specialization for semantic and syntactic processing were observed within each group, despite similar level of task performance. Second, after regressing out IQ, significant between-group differences were observed in the neural correlates of semantic and, to a lesser extent, syntactic processing, with HC children showing overall greater activity than COS children. Third, while these group differences were not related to effects of medications, a significant negative correlation was observed in the COS group between neuroleptic dosage and activity in the left inferior frontal gyrus for the semantic condition. Finally, COS children's level of thought disorder was significantly correlated with task-related activity in language-relevant networks. Taken together, these findings suggest that children with COS exhibit aberrant patterns of neural activity during semantic, and to a lesser extent syntactic, processing and that these functional abnormalities in language-relevant networks are significantly related to severity of thought disorder.
doi:10.1016/j.jneuroling.2009.07.004
PMCID: PMC3229826  PMID: 22147958
22.  ‘Syntactic Perturbation’ During Production Activates the Right IFG, but not Broca’s Area or the ATL 
Research on the neural organization of syntax – the core structure-building component of language – has focused on Broca’s area and the anterior temporal lobe (ATL) as the chief candidates for syntactic processing. However, these proposals have received considerable challenges. In order to better understand the neural basis of syntactic processing, we performed a functional magnetic resonance imaging experiment using a constrained sentence production task. We examined the BOLD response to sentence production for active and passive sentences, unstructured word lists, and syntactic perturbation. Perturbation involved cued restructuring of the planned syntax of a sentence mid utterance. Perturbation was designed to capture the effects of syntactic violations previously studied in sentence comprehension. Our experiment showed that Broca’s area and the ATL did not exhibit response profiles consistent with syntactic operations – we found no increase of activation in these areas for sentences > lists or for perturbation. Syntactic perturbation activated a cortical-subcortical network including robust activation of the right inferior frontal gyrus (RIFG). This network is similar to one previously shown to be involved in motor response inhibition. We hypothesize that RIFG activation in our study and in previous studies of sentence comprehension is due to an inhibition mechanism that may facilitate efficient syntactic restructuring.
doi:10.3389/fpsyg.2016.00241
PMCID: PMC4763068  PMID: 26941692
syntax; sentence processing; language; fMRI; inferior frontal gyrus; Broca’s area; ATL; production
23.  Contributions to singing ability by the posterior portion of the superior temporal gyrus of the non-language-dominant hemisphere: First evidence from subdural cortical stimulation, Wada testing, and fMRI 
INTRODUCTION
Although the substrates that mediate singing abilities in the human brain are not well understood, invasive brain mapping techniques used for clinical decision making such as intracranial electrocortical testing and Wada testing offer a rare opportunity to examine music-related function in a select group of subjects, affording exceptional spatial and temporal specificity.
METHODS
We studied eight patients with medically refractory epilepsy undergoing indwelling subdural electrode seizure focus localization. All patients underwent Wada testing for language lateralization. Functional assessment of language and music tasks was done by electrode grid cortical stimulation. One patient was also tested non-invasively with functional MRI. Functional organization of singing ability compared to language ability was determined based on four regions-ofinterest: left and right inferior frontal gyrus (IFG), and left and right posterior superior temporal gyrus (pSTG).
RESULTS
In some subjects, electrical stimulation of dominant pSTG can interfere with speech and not singing, whereas stimulation of non-dominant pSTG area can interfere with singing and not speech. Stimulation of the dominant IFG tends to interfere with both musical and language expression, while non-dominant IFG stimulation was often observed to cause no interference with either task; and finally, that stimulation of areas adjacent to but not within non-dominant pSTG typically does not affect either ability. FMRI mappings of one subject revealed similar music/language dissociation with respect to activation asymmetry within the regions-of-interest.
CONCLUSION
Despite inherent limitations with respect to strictly research objectives, invasive clinical techniques offer a rare opportunity to probe musical and language cognitive processes of the brain in a select group of patients.
doi:10.1016/j.cortex.2009.04.010
PMCID: PMC2821975  PMID: 19570530
singing laterality; cortical stimulation; fMRI; Wada test; music ability
24.  Does Co-Morbid Obsessive–Compulsive Disorder Modify the Abnormal Language Processing in Schizophrenia Patients? An fMRI Study 
Background: Impaired language processing is one of the most replicated findings in functional brain studies of schizophrenia (SCH). This is demonstrated by reduced activations in left prefrontal language areas (i.e., BA44/45, the inferior frontal gyrus, IFG) presented as decreased language lateralization. This finding was documented both in chronic as well as in first-episode SCH patients, arguing for a neurobiological marker for SCH. In a previous study, we demonstrated the specificity of this finding to SCH patients when compared to obsessive–compulsive disorder (OCD) patients in whom language processing was similar to healthy controls. Since a sizable proportion of SCH patients also meet DSM-IV criteria for OCD, we further sought to elucidate whether OCD attenuates abnormal prefrontal language lateralization in this unique group of schizo-obsessive patients compared to their non-OCD-SCH counterparts.
Methods: We used functional magnetic resonance imaging (fMRI) to investigate regional activation and language lateralization in the left and right IFG and inter-hemispheric functional connectivity (FC) during a language task of auditory verb generation in 14 SCH patients with OCD, compared to 17 SCH patients without OCD, 13 OCD patients and 14 healthy controls.
Results: No between-group differences were found in the behavioral measurements of word generation. However, while OCD patients were indistinguishable from healthy volunteers, a similarly reduced lateralization in the IFG and diminished inter-hemispheric FC was noted in the two SCH groups with and without OCD.
Conclusion: The co-occurrence of OCD in SCH does not attenuate abnormal processing of language as reflected by regional IFG activity and FC. These results further support the notion that these language processing abnormalities are characteristic of SCH and that SCH–OCD combined psychopathology is more akin to SCH than to OCD.
doi:10.3389/fnhum.2014.00560
PMCID: PMC4114205  PMID: 25120459
language; fMRI; inferior frontal gyrus; schizo-obsessive; schizophrenia; OCD
25.  Music and Language Syntax Interact in Broca’s Area: An fMRI Study 
PLoS ONE  2015;10(11):e0141069.
Instrumental music and language are both syntactic systems, employing complex, hierarchically-structured sequences built using implicit structural norms. This organization allows listeners to understand the role of individual words or tones in the context of an unfolding sentence or melody. Previous studies suggest that the brain mechanisms of syntactic processing may be partly shared between music and language. However, functional neuroimaging evidence for anatomical overlap of brain activity involved in linguistic and musical syntactic processing has been lacking. In the present study we used functional magnetic resonance imaging (fMRI) in conjunction with an interference paradigm based on sung sentences. We show that the processing demands of musical syntax (harmony) and language syntax interact in Broca’s area in the left inferior frontal gyrus (without leading to music and language main effects). A language main effect in Broca’s area only emerged in the complex music harmony condition, suggesting that (with our stimuli and tasks) a language effect only becomes visible under conditions of increased demands on shared neural resources. In contrast to previous studies, our design allows us to rule out that the observed neural interaction is due to: (1) general attention mechanisms, as a psychoacoustic auditory anomaly behaved unlike the harmonic manipulation, (2) error processing, as the language and the music stimuli contained no structural errors. The current results thus suggest that two different cognitive domains—music and language—might draw on the same high level syntactic integration resources in Broca’s area.
doi:10.1371/journal.pone.0141069
PMCID: PMC4633113  PMID: 26536026

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