Fumitaka Homae

From Perception to Sentence Comprehension: The Convergence of Auditory and Visual Information of Language in the Left Inferior Frontal Cortex

We used functional magnetic resonance imaging (fMRI) to characterize cortical activation associated with sentence processing, thereby elucidating where in the brain auditory and visual inputs of words converge during sentence comprehension. Within one scanning session, subjects performed three types of tasks with different linguistic components from perception to sentence comprehension: nonword (N(AV); auditory and visual), phrase (P; either auditory or visual), and sentence (S; either auditory or visual) tasks. In a comparison of the P and N(AV) tasks, the angular and supramarginal gyri showed bilateral activation, whereas the inferior and middle frontal gyri showed left-lateralized activation. A comparison of the S and P tasks, together with a conjunction analysis, revealed a ventral region of the left inferior frontal gyrus (F3t/F3O), which was sentence-processing selective and modality-independent. These results unequivocally demonstrated that the left F3t/F3O is involved in the selection and integration of semantic information that are separable from lexico-semantic processing.

Functional differentiation in the human auditory and language areas revealed by a dichotic listening task.

The human auditory cortex plays a special role in speech recognition. It is therefore necessary to clarify the functional roles of individual auditory areas. We applied functional magnetic resonance imaging (fMRI) to examine cortical responses to speech sounds, which were presented under the dichotic and diotic (binaural) listening conditions. We found two different response patterns in multiple auditory areas and language-related areas. In the auditory cortex, the medial portion of the secondary auditory area (A2), as well as a part of the planum temporale (PT) and the superior temporal gyrus and sulcus (ST), showed greater responses under the dichotic condition than under the diotic condition. This dichotic selectivity may reflect acoustic differences and attention-related factors such as spatial attention and selective attention to targets. In contrast, other parts of the auditory cortex showed comparable responses to the dichotic and diotic conditions. We found similar functional differentiation in the inferior frontal (IF) cortex. These results suggest that multiple auditory and language areas may play a pivotal role in integrating the functional differentiation for speech recognition.

Prosodic processing in the developing brain.

Speech prosody is considered to be one of the most important sources of information for infants in acquiring their native language. Using multi-channel near-infrared spectroscopy in 10-month-old infants, we examined cortical activation when normal and flattened speech sounds were presented to the infants. The flattened speech sound was generated by eliminating changes in the pitch contours of the original utterance. We found bilateral activation under both speech conditions. In a direct comparison between the two conditions, the right temporal and temporoparietal regions, and bilateral prefrontal regions showed more prominent activation in response to flattened speech than to normal speech. These results demonstrate that the unfamiliar pitch contours of flattened speech induce additional processing in the cortical regions of 10-month-old infants, suggesting that 10-month-old infants already have neural mechanisms for the processing of at least a part of the prosodic structures in their native language. To investigate developmental changes in cortical activation patterns, we compared the present results with those of our previous study using the same paradigm with 3-month-old infants. We propose that speech processing in the infant brain develops from analyzing pitch information per se, to comparing and integrating information in input speech sounds with acquired prosodic structures.

Sentence processing in the cerebral cortex.

Human language is a unique faculty of the mind. It has been the ultimate mystery throughout the history of neuroscience. Despite many aphasia and functional imaging studies, the exact correlation between cortical language areas and subcomponents of the linguistic system has not been established. One notable drawback is that most functional imaging studies have tested language tasks at the word level, such as lexical decision and word generation tasks, thereby neglecting the syntactic aspects of the language faculty. As proposed by Chomsky, the critical knowledge of language involves universal grammar (UG), which governs the syntactic structure of sentences. In this article, we will review recent advances made by functional neuroimaging studies of language, focusing especially on sentence processing in the cerebral cortex. We also present the recent results of our functional magnetic resonance imaging (fMRI) study intended to identify cortical areas specifically involved in syntactic processing. A study of sentence processing that employs a newly developed technique, optical topography (OT), is also presented. Based on these findings, we propose a modular specialization of Brocas area, Wernickes area, and the angular gyrus/supramarginal gyrus. The current direction of research in neuroscience is beginning to establish the existence of distinct modules responsible for our knowledge of language.

Prefrontal Cortical Involvement in Young Infants’ Analysis of Novelty

Our knowledge of infant perception and cognition is primarily based on habituation and dishabituation, but the underlying neural mechanisms for these processes per se remain unclear. It has been argued that habituation is related to building internal representations of repeated stimuli in the central nervous system, whereas dishabituation is related to an increased attention to novel items and events. This leads to a hypothesis that a distributed network including the sensory, association and prefrontal cortical regions of young infants is involved in those processes, in contrast with the classical developmental view that onset of the functioning of the prefrontal cortex is delayed. Here we examined the time evolution of spatio-temporal hemodynamic responses related to the auditory habituation and dishabituation in the temporal and prefrontal regions of 3-month-old infants by using multichannel near-infrared spectroscopy. We found that the temporal regions remained activated by repetitive auditory stimuli; however, the prefrontal regions exhibited phasic activation in relation to novel stimuli. The dissociated activation pattern between the temporal and prefrontal regions suggests that distinct cortical regions play distinct functional roles in auditory habituation and dishabituation, and that the prefrontal cortex is involved in perceiving invariance or novelty of the immediate environment in early infancy.

Functional activation in diverse regions of the developing brain of human infants.

To understand the functional organization of the human cortex during the early postnatal period, we performed neuroimaging studies for visual perception in awake 3-month-old infants. Cortical hemodynamic responses to 2 different video images, moving mobile objects and black-and-white checkerboard pattern reversals, were observed using multichannel near-infrared spectroscopy (NIRS). Although a focal region of the occipital cortex was equally activated by both stimuli, the occipitotemporal region was activated only by the mobile objects. A possible explanation of the result is that the former and the latter regions are involved in the primary processing of visual stimuli and perception of objects with complex visual features, respectively. Furthermore, the prefrontal region was distinctly activated by the mobile objects. These results suggest that the early sensory region and the higher sensory/association and prefrontal regions are functionally differentiated by 3 months of age and that diverse regions of the cortex including the prefrontal region function during perception of visual events.

Selective enhancement of functional connectivity in the left prefrontal cortex during sentence processing.

We present the results of correlation analyses for identifying temporally correlated activations between multiple regions of interest. We focused on functional connectivity for two regions in the prefrontal cortex: the left inferior frontal gyrus (L. F3t/F3O) and the left precentral sulcus (L. PrCS). Temporal correlations of functional magnetic resonance imaging signals were separately examined during a sentence comprehension task and a lexical decision task, thereby averaging data throughout all voxels within a region of interest used as a reference region. We found that the reciprocal connectivity between L. F3t/F3O and L. PrCS was significantly enhanced during sentence processing, but not during lexico-semantic processing, which was confirmed under both auditory and visual conditions. Furthermore, significantly correlated regions were mostly concentrated in the left prefrontal cortex during the sentence task. These results demonstrate that the functional connectivity within the left prefrontal cortex is selectively enhanced for processing sentences, which may subserve the use of syntactic information for integrating lexico-semantic information.

Spatiotemporal properties of cortical haemodynamic response to auditory stimuli in sleeping infants revealed by multi-channel near-infrared spectroscopy

Multi-channel near-infrared spectroscopy (NIRS) has been used as a neuroimaging tool to study functional activation of the developing brain in infants. In this paper, we focus on spatiotemporal dynamics of cortical oxygenation changes during sensory processing in young infants. We use a 94-channel NIRS system to assess the activity of wide regions of the cortex in quietly sleeping three-month-old infants. Auditory stimuli composed of a random sequence of pure tones induced haemodynamic changes not only in the temporal auditory regions, but also in the occipital and frontal regions. Analyses of phase synchronization showed that mutual synchronizations of signal changes among the cortical regions were much stronger than the stimulus-induced synchronizations of signal changes. Furthermore, analyses of phase differences among cortical regions revealed phase advancement of the bilateral temporal auditory regions, and phase gradient in a posterior direction from the temporal auditory regions to the occipital regions and in an anterior direction within the frontal regions. We argue that multi-channel NIRS is capable of detecting the precise timing of cortical activation and its flow in the global network of the developing brain.

Sentence processing is uniquely human.

In this article, we will focus on three fundamental issues concerning language processing in the human brain, and update recent advances made by functional neuroimaging and magnetic stimulation studies of language. First, we will provide the first experimental evidence that the neural basis of sentence comprehension is indeed specialized. Specifically, our recent functional magnetic resonance imaging (fMRI) study has clarified that the human left prefrontal cortex (PFC) is more specialized in the syntactic processes of sentence comprehension than other domain-general processes such as short-term memory. Second, the distinction between explicit and implicit syntactic processes will be clarified, based on our fMRI studies that elucidate syntactic specialization in the left PFC. Third, we will advance a hypothesis stating that distinct subregions of the left PFC are recruited for the syntactic integration of lexico-semantic information. The current direction of research in the neuroscience of language is beginning to reveal the uniqueness of the human mind.

Anticipatory cortical activation precedes auditory events in sleeping infants.

Background Behavioral studies have shown that infants can form associations between environmental events and produce anticipatory actions for the predictable event, but the neural mechanisms for the learning and anticipation of events in infants are not known. Recent neuroimaging studies revealed that the association cortices of infants show activation related to auditory-stimulus discrimination and novelty detection during sleep. In the present study, we expected that when an auditory cue (beeps) predicted an auditory event (a female voice), specific regions of the infant cortex would show anticipatory activation before the event onset even while sleeping. Methodology/Principal Findings We examined the cortical activation of 3-month-old infants during delays between the cue and the event by using multi-channel near-infrared spectroscopy. To investigate spatiotemporal changes in cortical activation over the experimental session, we divided the session into two phases (early and late phase) and analyzed each phase separately. In the early phase, the frontal regions showed activation in response to the cue that was followed by the event compared with another cue that was not followed by any event. In the late phase, the temporoparietal region, in addition to the frontal region, showed prominent activation in response to the cue followed by the event. In contrast, when the cue was followed by an event and no-event in equal proportions, cortical activation in response to the cue was not observed in any phase. Conclusions Sleeping 3-month-old infants showed anticipatory cortical activation in the temporoparietal and frontal regions only in response to the cue predicting the event, suggesting that infants can implicitly form associations between temporally separated events and generate the anticipatory activation before the predictable event. Furthermore, the different time evolution of activation in the temporoparietal and frontal regions suggests that these regions may be involved in different aspects of learning and predicting future events.