Generating predictions: Lesion evidence on the role of left inferior frontal cortex in rapid syntactic analysis

A well-documented phenomenon in event-related electroencephalography (EEG) and magnetoencephalography (MEG) studies on language processing is that syntactic violations of different types elicit negativities as early as 100 msec after the violation point. Recently, these responses have been associated with activations in or very close to sensory cortices, suggesting the involvement of basic sensory mechanisms in the detection of syntactic violations. The present study investigated whether intact auditory cortices and adjacent temporal regions are sufficient to generate early syntactic negativities in the auditory event-related potential (ERP). We tested ten clinically non-aphasic patients with left inferior frontal lesions, but intact temporal cortices in a passive auditory ERP paradigm that had reliably elicited early negativities in response to violations of subject-verb agreement and word category in the past. Subject-verb agreement violations failed to elicit early grammaticality effects in these patients, whereas a group of ten age-matched controls showed a reliable early negativity. This finding supports the idea that sensory aspects of syntactic analysis as reflected in early syntactic negativities critically depend on top-down predictions generated by the left inferior frontal cortex. In contrast, word category violations elicited a small, marginally significant early negativity both in controls and patients, suggesting an additional involvement of temporal regions in early phrase structure processing. In an additional auditory oddball experiment patients showed a regular P300, but no N2b component in response to deviant tones, indicating that their deficit in generating sensory predictions extends beyond the language domain.     

Propofol disrupts functional interactions between sensory and high-order processing of auditory verbal memory

Current theories suggest that disrupting cortical information integration may account for the mechanism of general anesthesia in suppressing consciousness. Human cognitive operations take place in hierarchically structured neural organizations in the brain. The process of low-order neural representation of sensory stimuli becoming integrated in high-order cortices is also known as cognitive binding. Combining neuroimaging, cognitive neuroscience, and anesthetic manipulation, we examined how cognitive networks involved in auditory verbal memory are maintained in wakefulness, disrupted in propofol-induced deep sedation, and re-established in recovery. Inspired by the notion of cognitive binding, an functional magnetic resonance imaging-guided connectivity analysis was utilized to assess the integrity of functional interactions within and between different levels of the task-defined brain regions. Task-related responses persisted in the primary auditory cortex (PAC), but vanished in the inferior frontal gyrus (IFG) and premotor areas in deep sedation. For connectivity analysis, seed regions representing sensory and high-order processing of the memory task were identified in the PAC and IFG. Propofol disrupted connections from the PAC seed to the frontal regions and thalamus, but not the connections from the IFG seed to a set of widely distributed brain regions in the temporal, frontal, and parietal lobes (with exception of the PAC). These later regions have been implicated in mediating verbal comprehension and memory. These results suggest that propofol disrupts cognition by blocking the projection of sensory information to high-order processing networks and thus preventing information integration. Such findings contribute to our understanding of anesthetic mechanisms as related to information and integration in the brain.     

Auditory perception and syntactic cognition: brain activity-based decoding within and across subjects

The present magnetoencephalography study investigated whether the brain states of early syntactic and auditory-perceptual processes can be decoded from single-trial recordings with a multivariate pattern classification approach. In particular, it was investigated whether the early neural activation patterns in response to rule violations in basic auditory perception and in high cognitive processes (syntax) reflect a functional organization that largely generalizes across individuals or is subject-specific. On this account, subjects were auditorily presented with correct sentences, syntactically incorrect sentences, correct sentences including an interaural time difference change, and sentences containing both violations. For the analysis, brain state decoding was carried out within and across subjects with three pairwise classifications. Neural patterns elicited by each of the violation sentences were separately classified with the patterns elicited by the correct sentences. The results revealed the highest decoding accuracies over temporal cortex areas for all three classification types. Importantly, both the magnitude and the spatial distribution of decoding accuracies for the early neural patterns were very similar for within-subject and across-subject decoding. At the same time, across-subject decoding suggested a hemispheric bias, with the most consistent patterns in the left hemisphere. Thus, the present data show that not only auditory-perceptual processing brain states but also cognitive brain states of syntactic rule processing can be decoded from single-trial brain activations. Moreover, the findings indicate that the neural patterns in response to syntactic cognition and auditory perception reflect a functional organization that is highly consistent across individuals.     

Effect of syntactic similarity on cortical activation during second language processing: a comparison of English and Japanese among native Korean trilinguals

In this study of native Korean trilinguals we examined the effect of syntactic similarity between first (L1) and second (L2) languages on cortical activation during the processing of Japanese and English, which are, respectively, very similar to and different from Korean. Subjects had equivalent proficiency in Japanese and English. They performed auditory sentence comprehension tasks in Korean, Japanese, and English during functional MRI (fMRI). The bilateral superior temporal cortex was activated during the comprehension of three languages. The pars triangularis of the left inferior frontal gyrus (IFG) was additionally activated for L2 processing. Furthermore, the right cerebellum, the pars opercularis of the left IFG, and the posteriomedial part of the superior frontal gyrus were activated during the English tasks only. We observed significantly greater activation in the pars opercularis of the left IFG, the right cerebellum, and the right superior temporal cortex during the English than Japanese task; activation in these regions did not differ significantly between Korean and Japanese. Differential activation of the pars opercularis of the left IFG and the right cerebellum likely reflects syntactic distance and differential activation in the right superior temporal cortex may reflect the prosodic distance between English from Korean and Japanese. Furthermore, in the pars oparcularis of the left IFG and the right cerebellum, significant negative correlation between the activation and duration of exposure was observed for English, but not for Japanese. Our research supports the notion that linguistic similarity between L1 and L2 affects the cortical processing of second language.     

Functional neuroanatomy of non-verbal semantic sound processing in humans

Summary. Environmental sounds convey specific meanings and the neural circuitry for their recognition may have preceded language. To dissociate semantic mnemonic from sensory perceptual processing of non-verbal sound stimuli we systematically altered the inherent semantic properties of non-verbal sounds from natural and man-made sources while keeping their acoustic characteristics closely matched. We hypothesized that acoustic analysis of complex non-verbal sounds would be right lateralized in auditory cortex regardless of meaning content and that left hemisphere regions would be engaged when meaningful concept could be extracted. Using H₂¹⁵O-PET imaging and SPM data analysis, we demonstrated that activation of the left superior temporal and left parahippocampal gyrus along with left inferior frontal regions was specifically associated with listening to meaningful sounds. In contrast, for both types of sounds, acoustic analysis was associated with activation of right auditory cortices. We conclude that left hemisphere brain regions are engaged when sounds are meaningful or intelligible.     

fMRI of syntactic processing in typically developing children: structural correlates in the inferior frontal gyrus

Development of syntactic processing was examined to evaluate maturational processes including left language lateralization functions and increased specialization of brain regions important for syntactic processing. We utilized multimodal methods, including indices of brain activity from fMRI during a syntactic processing task, cortical thickness measurements from structural MRI, and neuropsychological measures. To evaluate hypotheses about increasing lateralization and specialization with development, we examined relationships between cortical thickness and magnitude and spatial activation extent within the left inferior frontal gyrus (IFG) and its right hemisphere homologue. We predicted that increased activation in the left and decreased activation in the right IFG would be associated with increased syntactic proficiency. As predicted, a more mature pattern of increased thickness in the right pars triangularis was associated with decreased activation intensity and extent in the right IFG. These findings suggest a maturational shift towards decreased involvement of the right IFG for syntactic processing. Better syntactic skills were associated with increased activation in the left IFG independent from age, suggesting increased specialization of the left IFG with increased proficiency. Overall, our findings show relationships between structural and functional neurodevelopment that co-occur with improved syntactic processing in critical language regions of the IFG in typically developing children.     

Towards a standard model of musical improvisation

Musical improvisation is a sophisticated cognitive process that combines creativity, goal‐directed action, sensory monitoring and social interaction. With a renewed interest in quantifying creative processes facilitated by recent advances in neuroimaging technology, musical improvisation has emerged as an ideal paradigm to study creativity. However, many studies isolate the top‐down processes related to creativity from those related to production and auditory perception, leaving the question of how creative behaviours integrate sensory information with higher cognitive processes unanswered. The bottom‐up neural correlates of music perception have been extensively quantified, comprising networks for auditory processing and parsing semantic and syntactic content. In studies of spontaneously generated music and domain‐general creativity, executive control and goal‐directed movement networks are added to the perceptual foundation. This review summarises previous work on music perception and improvisation and presents a conceptual model of musical improvisation with known neural correlates. We make recommendations on future directions for the study of improvisation and discuss the challenges posed by this endeavour.     

Functional anatomy of syntactic and semantic processing in language comprehension

A functional magnetic resonance imaging (fMRI) study was conducted to map syntactic and semantic processes onto the brain. Chinese-English bilingual subjects performed two experimental tasks: a syntactic plausibility judgment task in which they decided whether a viewed verb phrase was syntactically legal, and a semantic plausibility judgment task in which they decided whether a viewed phrase was semantically acceptable. A font size judgment task was used as baseline. It is found that a large-scale distributed neural network covering the left mid-inferior frontal and mid-superior temporal cortices was responsible for the processing of Chinese phrases. The right homologue areas of these left cortical sites were also active, although the brain activity was obviously left-lateralized. Unlike previous research with monolingual English speakers that showed that distinct brain regions mediate syntactic and semantic processing of English, the cortical sites contributing to syntactic analysis of Chinese phrases coincided with the cortical sites relevant to semantic analysis. Stronger brain activity, however, was seen in the left middle frontal cortex for syntactic processing (relative to semantic processing), whereas for semantic processing stronger cortical activations were shown in the left inferior prefrontal cortex and the left mid-superior temporal gyri. The overall pattern of results indicates that syntactic processing is less independent in reading Chinese. This is attributable to the linguistic nature of the Chinese language that semantics and syntax are not always clearly demarcated. Equally interesting, we discovered that when our bilingual subjects performed syntactic and semantic acceptability judgments of English phrases, they applied the cerebral systems underlying Chinese reading to the processing of English.     

The temporal interaction of modality specific and process specific neural networks supporting simple working memory tasks

Several theories of brain function emphasize distinctions between sensory and cognitive systems. We hypothesized, instead, that sensory and cognitive systems interact to instantiate the task at the neural level. We tested whether input modality interacts with working memory operations in that, despite similar cognitive demands, differences in the anatomical locations or temporal dynamics of activations following auditory or visual input would not be limited to the sensory cortices. We recorded event-related brain potentials (ERPs) while participants performed simple short-term memory tasks involving visually or auditorily presented bandpass-filtered noise stimuli. Our analyses suggested that working memory operations in each modality had a very similar spatial distribution of current sources outside the sensory cortices, but differed in terms of time course. Specifically, information for visual processing was updated and held online in a manner that was different from auditory processing, which was done mostly after the offset of the final stimulus. Our results suggest that the neural networks that support working memory operations have different temporal dynamics for auditory and visual material, even when the stimuli are matched in term of discriminability, and are designed to undergo very similar transformations when they are encoded and retrieved from memory.     

Auditory and visual connectivity gradients in frontoparietal cortex

A frontoparietal network of brain regions is often implicated in both auditory and visual information processing. Although it is possible that the same set of multimodal regions subserves both modalities, there is increasing evidence that there is a differentiation of sensory function within frontoparietal cortex. Magnetic resonance imaging (MRI) in humans was used to investigate whether different frontoparietal regions showed intrinsic biases in connectivity with visual or auditory modalities. Structural connectivity was assessed with diffusion tractography and functional connectivity was tested using functional MRI. A dorsal–ventral gradient of function was observed, where connectivity with visual cortex dominates dorsal frontal and parietal connections, while connectivity with auditory cortex dominates ventral frontal and parietal regions. A gradient was also observed along the posterior–anterior axis, although in opposite directions in prefrontal and parietal cortices. The results suggest that the location of neural activity within frontoparietal cortex may be influenced by these intrinsic biases toward visual and auditory processing. Thus, the location of activity in frontoparietal cortex may be influenced as much by stimulus modality as the cognitive demands of a task. It was concluded that stimulus modality was spatially encoded throughout frontal and parietal cortices, and was speculated that such an arrangement allows for top–down modulation of modality‐specific information to occur within higher‐order cortex. This could provide a potentially faster and more efficient pathway by which top–down selection between sensory modalities could occur, by constraining modulations to within frontal and parietal regions, rather than long‐range connections to sensory cortices. Hum Brain Mapp 38:255–270, 2017. © 2016 Wiley Periodicals, Inc.     

Response of anterior temporal cortex to syntactic and prosodic manipulations during sentence processing

Previous research has implicated a portion of the anterior temporal cortex in sentence-level processing. This region activates more to sentences than to word-lists, sentences in an unfamiliar language, and environmental sound sequences. The current study sought to identify the relative contributions of syntactic and prosodic processing to anterior temporal activation. We presented auditory stimuli where the presence of prosodic and syntactic structure was independently manipulated during functional magnetic resonance imaging (fMRI). Three "structural" conditions included normal sentences, sentences with scrambled word order, and lists of content words. These three classes of stimuli were presented either with sentence prosody or with flat supra-lexical (list-like) prosody. Sentence stimuli activated a portion of the left anterior temporal cortex in the superior temporal sulcus (STS) and extending into the middle temporal gyrus, independent of prosody, and to a greater extent than any of the other conditions. An interaction between the structural conditions and prosodic conditions was seen in a more dorsal region of the anterior temporal lobe bilaterally along the superior temporal gyrus (STG). A post-hoc analysis revealed that this region responded either to syntactically structured stimuli or to nonstructured stimuli with sentence-like prosody. The results suggest a parcellation of anterior temporal cortex into 1) an STG region that is sensitive both to the presence of syntactic information and is modulated by prosodic manipulations (in nonsyntactic stimuli); and 2) a more inferior left STS/MTG region that is more selective for syntactic structure.     

Neurocognition of auditory sentence comprehension: event related fMRI reveals sensitivity to syntactic violations and task demands

The present study investigates the sensitivity of distinct brain regions to the syntactic processing of running speech. Experimental conditions varied the grammaticality of sentence types (correct vs. incorrect). Moreover, two different groups of subjects listened to the same sentence material, but followed two different task instructions. All participants were asked to listen to the auditory stimuli and to perform in a grammaticality judgment-task, whereas only half of the subjects were instructed to additionally repair incorrect sentences covertly. Significantly increased brain responses occurred in several left temporal areas as a function of sentences' grammaticality, particularly, in the 'pure' judgment-group. Spatial extent as well as the strength of focal brain activation changed as a function of grammaticality and task demand. A generally enhanced pattern of local blood supply to the right peri-sylvian cortex could be observed when individuals additionally realized the repair-task. In particular, the right inferior frontal gyrus (pars opercularis and pars triangularis) and the right temporal transverse gyrus (Heschl's gyrus) were more strongly affected by the repair-task demand. In contrast, an anterior portion of the superior temporal gyrus (planum polare) displayed increased activation bilaterally. Although left hemisphere activation varied clearly as a function of a sentence's grammaticality, the present findings demonstrate an involvement of the right peri-sylvian cortex, in particular, when task demands explicitly require an on-line repair. The results as a whole suggest a reconsideration of the notion that auditory language comprehension is restricted to the left hemisphere. The underlying mechanisms and the respective roles of both the left and the right hemisphere during speech processing are discussed.     

Setting the stage for automatic syntax processing: the mismatch negativity as an indicator of syntactic priming

The present study investigated the automaticity of morphosyntactic processes and processes of syntactic structure building using event-related brain potentials. Two experiments were conducted, which contrasted the impact of local subject-verb agreement violations (Experiment 1) and word category violations (Experiment 2) on the mismatch negativity, an early event-related brain potential component reflecting automatic auditory change detection. The two violation types were realized in two-word utterances comparable with regard to acoustic parameters and structural complexity. The grammaticality of the utterances modulated the mismatch negativity response in both experiments, suggesting that both types of syntactic violations were detected automatically within 200 msec after the violation point. However, the topographical distribution of the grammaticality effect varied as a function of violation type, which indicates that the brain mechanisms underlying the processing of subject-verb agreement and word category information may be functionally distinct even at this earliest stage of syntactic analysis. The findings are discussed against the background of studies investigating syntax processing beyond the level of two-word utterances.     

Distinct roles of left inferior frontal regions that explain individual differences in second language acquisition

Second language (L2) acquisition is more susceptible to environmental and idiosyncratic factors than first language acquisition. Here, we used functional magnetic resonance imaging for L2 learners of different ages of first exposure (mean: 12.6 and 5.6 years) in a formal school environment, and compared the cortical activations involved in processing English sentences containing either syntactic or spelling errors, where the testing ages and task performances of both groups were matched. We found novel activation patterns in two regions of the left inferior frontal gyrus (IFG) that correlated differentially with the performances of the late and early learners. Specifically, activations of the dorsal and ventral triangular part (F3t) of the left IFG correlated positively with the accuracy of the syntactic task for the late learners, whereas activations of the left ventral F3t correlated negatively with the accuracy for the early learners. In contrast, other cortical regions exhibited differential correlation patterns with the reaction times (RTs) of the syntactic task. Namely, activations of the orbital part (F3O) of the left IFG, as well as those of the left angular gyrus, correlated positively with the RTs for the late learners, whereas those activations correlated negatively with the RTs for the early learners. Moreover, the task‐selective activation of the left F3O was maintained for both the late and early learners. These results explain individual differences in L2 acquisition, such that the acquisition of linguistic knowledge in L2 is subserved by at least two distinct inferior frontal regions of the left F3t and F3O. Hum Brain Mapp, 2009. © 2008 Wiley‐Liss, Inc.     

Neural basis of auditory expectation within temporal cortex

Predictive coding frameworks of perception propose that neural networks form predictions of expected input and generate prediction errors when the external input does not match expectation. We therefore investigated the processing of unexpected sounds and silence in the auditory cortex using fMRI. Unexpected sounds, when compared to expected sounds, evoked greater activation in large areas of the left temporal and insular cortices. Additionally the left middle temporal gyrus exhibited greater activation to unexpected events in general, whether sounds or silence, when compared to the corresponding expected events. These findings support predictive coding models of perception, which suggest that regions of the temporal cortex function to integrate sensory information with predictive signals during auditory perception.     

Grammatical gender in the brain: evidence from an fMRI study on Italian

The grammatical gender of a word is a lexical-syntactic property determining agreement among different sentence parts. Recent fMRI investigations identified the areas involved in the retrieval of grammatical gender near the left Broca's area providing further evidence to confirm the preeminent syntactic role of this area. However, these studies employed categorical designs based on the controversial methodology of the cognitive subtraction of neural activations related to different tasks. In the present study we identified the neural substrates of grammatical gender assignment using an fMRI parametric study. Participants decided the grammatical gender of visually presented Italian words whose gender-to-ending regularity varied. The results showed activation in left and right fronto-temporal areas suggesting an interplay of both hemispheres in the processing of grammatical gender.     

Stepwise Connectivity of the Modal Cortex Reveals the Multimodal Organization of the Human Brain

How human beings integrate information from external sources and internal cognition to produce a coherent experience is still not well understood. During the past decades, anatomical, neurophysiological and neuroimaging research in multimodal integration have stood out in the effort to understand the perceptual binding properties of the brain. Areas in the human lateral occipitotemporal, prefrontal, and posterior parietal cortices have been associated with sensory multimodal processing. Even though this, rather patchy, organization of brain regions gives us a glimpse of the perceptual convergence, the articulation of the flow of information from modality-related to the more parallel cognitive processing systems remains elusive. Using a method called stepwise functional connectivity analysis, the present study analyzes the functional connectome and transitions from primary sensory cortices to higher-order brain systems. We identify the large-scale multimodal integration network and essential connectivity axes for perceptual integration in the human brain.     

Superior Temporal Sulcus Disconnectivity During Processing of Metaphoric Gestures in Schizophrenia

The left superior temporal sulcus (STS) plays an important role in integrating audiovisual information and is functionally connected to disparate regions of the brain. For the integration of gesture information in an abstract sentence context (metaphoric gestures), intact connectivity between the left STS and the inferior frontal gyrus (IFG) should be important. Patients with schizophrenia have problems with the processing of metaphors (concretism) and show aberrant structural connectivity of long fiber bundles. Thus, we tested the hypothesis that patients with schizophrenia differ in the functional connectivity of the left STS to the IFG for the processing of metaphoric gestures. During functional magnetic resonance imaging data acquisition, 16 patients with schizophrenia (P) and a healthy control group (C) were shown videos of an actor performing gestures in a concrete (iconic, IC) and abstract (metaphoric, MP) sentence context. A psychophysiological interaction analysis based on the seed region from a previous analysis in the left STS was performed. In both groups we found common positive connectivity for IC and MP of the STS seed region to the left middle temporal gyrus (MTG) and left ventral IFG. The interaction of group (C>P) and gesture condition (MP>IC) revealed effects in the connectivity to the bilateral IFG and the left MTG with patients exhibiting lower connectivity for the MP condition. In schizophrenia the left STS is misconnected to the IFG, particularly during the processing of MP gestures. Dysfunctional integration of gestures in an abstract sentence context might be the basis of certain interpersonal communication problems in the patients.Key words: coverbal gestures, integration, fMRI, psychophysiological interaction, concretism     

Vowel-specific mismatch responses in the anterior superior temporal gyrus: An fMRI study

There have been many functional imaging studies that have investigated the neural correlates of speech perception by contrasting neural responses to speech and “speech-like” but unintelligible control stimuli. A potential drawback of this approach is that intelligibility is necessarily conflated with a change in the acoustic parameters of the stimuli. The approach we have adopted is to take advantage of the mismatch response elicited by an oddball paradigm to probe neural responses in temporal lobe structures to a parametrically varied set of deviants in order to identify brain regions involved in vowel processing. Thirteen normal subjects were scanned using a functional magnetic resonance imaging (fMRI) paradigm while they listened to continuous trains of auditory stimuli. Three classes of stimuli were used: ‘vowel deviants’ and two classes of control stimuli: one acoustically similar (‘single formants’) and the other distant (tones). The acoustic differences between the standard and deviants in both the vowel and single-formant classes were designed to match each other closely. The results revealed an effect of vowel deviance in the left anterior superior temporal gyrus (aSTG). This was most significant when comparing all vowel deviants to standards, irrespective of their psychoacoustic or physical deviance. We also identified a correlation between perceptual discrimination and deviant-related activity in the dominant superior temporal sulcus (STS), although this effect was not stimulus specific. The responses to vowel deviants were in brain regions implicated in the processing of intelligible or meaningful speech, part of the so-called auditory “what” processing stream. Neural components of this pathway would be expected to respond to sudden, perhaps unexpected changes in speech signal that result in a change to narrative meaning.