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Direct evidence from intraoperative electrocortical stimulation indicates shared and distinct speech production center between Chinese and English languages.

ABSTRACT: Chinese processing has been suggested involving distinct brain areas from English. However, current functional localization studies on Chinese speech processing use mostly "indirect" techniques such as functional magnetic resonance imaging and electroencephalography, lacking direct evidence by means of electrocortical recording. In this study, awake craniotomies in 66 Chinese-speaking glioma patients provide a unique opportunity to directly map eloquent language areas. Intraoperative electrocortical stimulation was conducted and the positive sites for speech arrest, anomia, and alexia were identified separately. With help of stereotaxic neuronavigation system and computational modeling, all positive sites elicited by stimulation were integrated and a series of two- and three-dimension Chinese language probability maps were built. We performed statistical comparisons between the Chinese maps and previously derived English maps. While most Chinese speech arrest areas located at typical language production sites (i.e., 50% positive sites in ventral precentral gyrus, 28% in pars opercularis and pars triangularis), which also serve English production, an additional brain area, the left middle frontal gyrus (Brodmann's areas 6/9), was found to be unique in Chinese production (P < 0.05). Moreover, Chinese speakers' inferior ventral precentral gyrus (Brodmann's area 6) was used more than that in English speakers. Our finding suggests that Chinese involves more perisylvian region (extending to left middle frontal gyrus) than English. This is the first time that direct evidence supports cross-cultural neurolinguistics differences in human beings. The Chinese language atlas will also helpful in brain surgery planning for Chinese-speakers.

SUBMITTER: Wu J

PROVIDER: S-EPMC6869327 | biostudies-literature | 2015 Dec

REPOSITORIES: biostudies-literature

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Direct evidence from intraoperative electrocortical stimulation indicates shared and distinct speech production center between Chinese and English languages.

Wu Jinsong J Lu Junfeng J Zhang Han H Zhang Jie J Yao Chengjun C Zhuang Dongxiao D Qiu Tianming T Guo Qihao Q Hu Xiaobing X Mao Ying Y Zhou Liangfu L

Human brain mapping 20150909 12

Chinese processing has been suggested involving distinct brain areas from English. However, current functional localization studies on Chinese speech processing use mostly "indirect" techniques such as functional magnetic resonance imaging and electroencephalography, lacking direct evidence by means of electrocortical recording. In this study, awake craniotomies in 66 Chinese-speaking glioma patients provide a unique opportunity to directly map eloquent language areas. Intraoperative electrocort ...[more]

PMID: 26351094

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Project description:Cortical regions supporting speech production are commonly established using neuroimaging techniques in both research and clinical settings. However, for neurosurgical purposes, structural function is routinely mapped peri-operatively using direct electrocortical stimulation. While this method is the gold standard for identification of eloquent cortical regions to preserve in neurosurgical patients, there is lack of specificity of the actual underlying cognitive processes being interrupted. To address this, we propose mapping the temporal dynamics of speech arrest across peri-sylvian cortices by quantifying the latency between stimulation and speech deficits. In doing so, we are able to substantiate hypotheses about distinct region-specific functional roles (e.g., planning versus motor execution). In this retrospective observational study, we analyzed 20 patients (12 female; age range 14-43) with refractory epilepsy who underwent continuous extra-operative intracranial EEG monitoring of an automatic speech task during clinical bedside language mapping. Latency to speech arrest was calculated as time from stimulation onset to speech arrest onset, controlling for individual speech rate. Most instances of motor-based arrest (87.5% of 96 instances) were in sensorimotor cortex with mid-range latencies to speech arrest with a distributional peak at 0.47 seconds. Speech arrest occurred in numerous regions, with relatively short latencies in supramarginal gyrus (0.46 seconds), superior temporal gyrus (0.51 seconds), and middle temporal gyrus (0.54 seconds), followed by relatively long latencies in sensorimotor cortex (0.72 seconds) and especially long latencies in inferior frontal gyrus (0.95 seconds). Nonparametric testing for speech arrest revealed that region predicted latency; latencies in supramarginal gyrus and in superior temporal gyrus were shorter than in sensorimotor cortex and in inferior frontal gyrus. Sensorimotor cortex is primarily responsible for motor-based arrest. Latencies to speech arrest in supramarginal gyrus and superior temporal gyrus (and to a lesser extent middle temporal gyrus) align with latencies to motor-based arrest in sensorimotor cortex. This pattern of relatively quick cessation of speech suggests that stimulating these regions interferes with the outgoing motor execution. In contrast, the latencies to speech arrest in inferior frontal gyrus and in ventral regions of sensorimotor cortex were significantly longer than those in temporoparietal regions. Longer latencies in the more frontal areas (including inferior frontal gyrus and ventral areas of precentral gyrus and postcentral gyrus) suggest that stimulating these areas interrupts a higher-level speech production process involved in planning. These results implicate the ventral specialization of sensorimotor cortex (including both precentral and postcentral gyri) for speech planning above and beyond motor execution.

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Direct evidence from intraoperative electrocortical stimulation indicates shared and distinct speech production center between Chinese and English languages.

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Direct evidence from intraoperative electrocortical stimulation indicates shared and distinct speech production center between Chinese and English languages.

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