Elsevier

Neuroscience Letters

Volume 584, 1 January 2015, Pages 351-355
Neuroscience Letters

Short communication
Task-dependent modulation of regions in the left temporal cortex during auditory sentence comprehension

https://doi.org/10.1016/j.neulet.2014.10.054Get rights and content

Highlights

  • The left lateral temporal cortex is sensitive to sentence intelligibility.

  • The anterior and posterior STS/MTG regions are involved in both passive and active sentence comprehension.

  • The middle STS/MTG regions respond to sentence intelligibility only during the active task.

Abstract

Numerous studies have revealed the essential role of the left lateral temporal cortex in auditory sentence comprehension along with evidence of the functional specialization of the anterior and posterior temporal sub-areas. However, it is unclear whether task demands (e.g., active vs. passive listening) modulate the functional specificity of these sub-areas. In the present functional magnetic resonance imaging (fMRI) study, we addressed this issue by applying both independent component analysis (ICA) and general linear model (GLM) methods. Consistent with previous studies, intelligible sentences elicited greater activity in the left lateral temporal cortex relative to unintelligible sentences. Moreover, responses to intelligibility in the sub-regions were differentially modulated by task demands. While the overall activation patterns of the anterior and posterior superior temporal sulcus and middle temporal gyrus (STS/MTG) were equivalent during both passive and active tasks, a middle portion of the STS/MTG was found to be selectively activated only during the active task under a refined analysis of sub-regional contributions. Our results not only confirm the critical role of the left lateral temporal cortex in auditory sentence comprehension but further demonstrate that task demands modulate functional specialization of the anterior–middle–posterior temporal sub-areas.

Introduction

Recent neurolinguistic work has highlighted the critical role of the left lateral temporal cortex in auditory sentence comprehension [1], [13], [14], [23], [30]. Neural models for speech comprehension hold that the left lateral temporal cortex together with the left frontal areas such as par triangularis and par orbitalis forms the ventral pathway responsible for auditory-to-meaning processing [12], [26]. However, there is evidence that sub-regions of the left lateral temporal cortex are functionally specialized, although the specific functions of the different areas in auditory sentence comprehension are still being debated. For example, the posterior areas are considered to be critical for semantic store at the lexical level, whereas the anterior regions are more involved in combinatorial semantic processes [3], [16], [23]. There may even exist subtle separation of functions within the left anterior temporal region, with the most anterior portion of the superior temporal sulcus and middle temporal gyrus (STS/MTG) primarily responding to syntactic structure and a region directly posterior to it reflecting the interaction of syntactic and semantic information [13].

The existing studies on functional heterogeneity of the left lateral temporal cortex have used stimulus manipulations in either a passive listening condition [1], [25], [30] or active anomaly detection/selective attention conditions [10], [20], [23]. These studies adopted the strategy of comparing activation across different types of stimuli or across active tasks to isolate semantic and syntactic processing in either passive or active listening conditions. While the results helped to disentangle functional divisions of the sub-regions in the left lateral temporal cortex and how they were associated with syntactic and sentence-level semantic processing, the previous studies have not successfully addressed how task demands may differentially affect the functional specificity of the sub-regions in this important brain area. To our knowledge, only one study has made direct comparison between passive and active sentence comprehension [11]. By use of sentence repetition paradigm, this study reported null findings on this issue as similar activation reductions were found in the lateral aspects of STS/MTG for the different tasks.

In the current study, we attempted to further address whether and how passive vs. active task-related effects contribute to different activation patterns in various sub-regions of the left temporal cortex during auditory sentence comprehension. Of these sub-regions, the middle area is of special interest because functions of this area in auditory sentence comprehension have not been clearly specified, although it is implicated as an important part of the ventral pathway subserving semantic processing [8]. We asked participants to listen to normal and time-reversed sentences in both passive and active task conditions. In the passive listening task, participants were told to listen to sentences carefully without overt responses, and in the active comprehension task, they were instructed to comprehend the sentences attentively and to press a button whenever they detected an anomalous sentence. We first adopted probabilistic independent component analysis (ICA) [2] to identify the functional regions of interest (ROIs) in order to avoid the issues of circularity that may characterize the traditional two-step model-driven identifications of ROIs [15], [29]. And then anatomical parcellation masks from Freesurfer [7] were used to create sub-ROIs in order to examine the possible functional heterogeneity of the left lateral temporal cortex that is modulated by passive and active task demands.

Section snippets

Participants

Twenty undergraduate and postgraduate students (11 females) with a mean age of 20.8 years (range 18–25) participated in this study. They were all native Chinese speakers, and were right-handed according to a modified Chinese version of the Edinburgh Handedness Inventory [21]. No participant reported a history of a hearing, neurological or psychiatric disorder. Written informed consent was obtained from all participants after they were given a complete description of the study and all received

Behavioral data

For the active task runs, behavioral responses of all the participants approached ceiling-level performance (mean accuracy = 99%), indicating that the participants maintained vigilance during the task and that the anomaly detection paradigm successfully directed participants’ attention to semantic integration of the sentences.

Intelligibility and task effects

Of the twenty-eight independent components decomposed by ICA analysis, five components were identified as stimulus-related (significantly correlated with any type of

Discussion

Although multiple methodological approaches have identified the left lateral temporal cortex as one of the most important areas responsible for sentence-level speech comprehension, there remain substantial disagreements in the literature with respect to the precise functions of its sub-regions [1], [12], [13], [23], [25], [30]. Specifically, it is unclear whether and how functions of the various sub-regions are modulated by passive/active task demands during auditory sentence comprehension. To

Conclusion

In sum, our fMRI data indicate the existence of two classes of sub-regions in the left lateral temporal cortex that are differentially sensitive to sentence intelligibility depending on the demands of the listening task. First, the anterior and posterior sub-regions respond similarly to intelligibility of spoken sentences regardless of task demands. Second, the middle sub-regions selectively respond to controlled processing of intelligibility that requires overt behavioral response. Thus,

Acknowledgements

This research was supported by Program for New Century Excellent Talents in University (NCET-13-0691), the Natural Science Foundation of China (31271082), and the Natural Science Foundation of Beijing (7132119).

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    L.Z. and Q.Y. contributed equally to this work.

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