Purpose

To investigate the predictive brain mechanism underlying the effortless and efficient information exchange via speech, and to reveal how prior expectation influences the sound-to-meaning mapping at the neuroanatomical level in a natural language context.

Methods

Thirty right-handed native Mandarin Chinese speakers were enrolled in this study(aged 21-28, 15 male). Three types of auditory stimuli, i.e., expected phrases (EPs),unexpected phrases (UPs), and time-reversed phrases (TPs), were presented. Subjects were asked to judge the gender of speakers. Chinese idioms generally have a high transitional probability, therefore, by manipulating the last portion of a Chinese idiom,expectation violations can be naturally induced. The EPs were normal Chinese idioms,while the UPs were created by keeping the first portion of an idiom and replacing the last portion with character(s) of another irrelevant idiom. The TPs were derived equally from both EPs and UPs to create a low-level acoustical match. Theexperimental procedure was adopted from a previous study¹. MRI data were acquired using a MAGNETOM Trio 3T MR scanner (Siemens, Erlangen, Germany) with a 12-channel head coil. Thirty-five axial slices that covered the whole brain were acquired using a T2*-weighted gradient-echo EPI sequence with the following parameters: TR/TE/FA = 2080ms/30ms/90o, matrix size = 64 x 64, in-plane image resolution = 3mm x 3mm, slice thickness = 3mm, slice gap = 0.75mm. Fifteen subjects participated in a post-scan dictation to write down the phrases they heard inthe scanner after fMRI experiment.Both univariate and multivariate pattern analyses (MVPA) were conducted to give a comprehensive description of the involved neural substrates (Fig. 1). The voxel-wise Mahalanobis distances (MDs), which take the covariance structure into consideration and reduce the contribution from noisy voxels, between different task conditions were used as features for training SVM classifiers. According to the dual-stream model^2,3,seven regions of interest in the left hemisphere (i.e., the anterior superior temporal gyrus (aSTG), superior temporal pole (STP), posterior middle temporal gyrus (pMTG), primary auditory cortex (PAC), pars triangularis of the IFG (IFGtr), pars opercularis of the IFG (IFGop), and supplementary motor areas (SMA)) were selected for further psychophysiological interaction (PPI)⁴ and dynamic causal modelling(DCM)^5,6 analysis.

Results

The results of univariate and multivariate analyses are separately shown in Fig. 2A&B. PPI analysis revealed that the left IFGtr tended to exhibit stronger functional connectivity with both streams for UPs than for EPs (Fig. 3). We found that the strengths of the two connections with IFGtr were both positively correlated with subjects’ performance in the dictation, one of them was along the ventral stream(IFGtr-aSTG; r = 0.78, P < 0.001; r = 0.54, P = 0.039; Fig. 4A&B), and the other connection located within the dorsal stream (IFGtr-IFGop; r = 0.55, P = 0.035; Fig.4B). Moreover, the strengthened connectivity between aSTG and STP for processing UPs relative to TPs showed a positive correlation with the dictation accuracy for UPs(r = 0.83, P < 0.001; Fig. 4A). The winning model and the modulations of EPs and UPs obtained from the post-hoc DCM analysis are shown in Fig. 5.

Discussion

We found that Ups can induce more significant activations relative to EPs in the left aSTG and IFGtr; moreover, stronger functional connectivity between them could predict better dictation performances when expectations were violated. These results suggest the aSTG plays an important role in facilitating rapid sound-to-meaning mapping with top-down constraints. Furthermore, the cortical dynamic activation indicates enhanced modulation on IFGtr-to-aSTG, aSTG-to-STP, and reciprocal IFGtr-to-STP connections in response to UPs. The enhanced feedback connections from the IFGtr may be attributed to the additional requirements of top-down constraints which help to determine the word identity or the lack of higher-level information to accomplish semantic integration/retrieval. The results of pattern analysis suggest that the pMTG might also encode information at a lower level for further top-down modulation of speech processing. Consistent with this perspective,we identified an enhanced feedback connection from the left IFGop to pMTG and another enhanced forward connection from the pMTG to IFGop via SMA during the processing of UPs. Functional connectivity results suggest that the IFG subserves the integration of dorsal and ventral streams⁷ by showing corresponding enhanced connections. Moreover, enhanced information flow from IFGtr to IFGop was discovered for both EPs and UPs, which may be attributed to a transformation from category-invariant representations into motor-articulatory representations for intelligible speech³.

Conclusion

The results of this study suggest that the human brain relies on adjacent cortical areas and their interconnections for efficient back-and-forth processing of local and contextual information, which facilitates speech processing in a predictive manner.

Acknowledgements

This work was supported by China’s National Strategic Basic Research Program (973; Grant 2012CB720700), National Natural Science Foundation of China (Grants 31200761, 31421003, 81227003, and 81430037), Beijing Municipal Science & Technology Commission (Grant Z161100000216152), and Shenzhen Peacock Plan (GrantKQTD2015033016104926).