Prefrontal-Temporal Pathway Mediates the Cross-Modal and Cognitive Reorganization in Sensorineural Hearing Loss With or Without Tinnitus: A Multimodal MRI Study

Prefrontal-Temporal Pathway Mediates the Cross-Modal and Cognitive Reorganization in Sensorineural Hearing Loss With or Without Tinnitus: A Multimodal MRI Study
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DOI:
10.3389/fnins.2019.00222
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发表时间:
2019-03-12
影响因子:
4.3
通讯作者:
Teng, Gao-Jun
Teng, Gao-Jun
中科院分区:
医学2区
文献类型:
--
作者:
Luan, Ying;Wang, Congxiao;Teng, Gao-Jun

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目的:听力损失是耳鸣和听觉亢进的主要危险因素之一,被认为与中枢功能异常有关。听觉皮层在非听觉感觉和高阶认知加工中的招募已经在听力剥夺的大脑中得到证实。背外侧前额叶皮层(dlPFC)与听觉通路有紧密的解剖联系,在多感觉整合、听觉调节和认知加工中起着至关重要的作用。本研究旨在通过结合功能和结构测量来验证dlPFC在长期感音神经性听力损失(SNHL)中听觉皮层的跨模态重组和认知参与中的作用。方法:35例长期双侧SNHL患者和35例匹配的健康对照者进行了结构成像、静息状态功能磁共振成像(rs-fMRI)、弥散张量成像(DTI)和神经心理学评估。10例SNHL患者伴有主观性耳鸣。结果:SNHL组和对照组在dlPFC的灰质体积、自发神经活动或扩散特征上没有差异。SNHL患者dlPFC与听觉皮层和视觉区域(如楔状、梭状、舌皮层和钙根沟)之间的功能连通性(FC)增加。方差分析和事后检验显示,与听力正常对照相比,伴有和不伴有耳鸣的SNHL患者的FC变化相似,伴有和不伴有耳鸣的SNHL患者的dlPFC FC没有差异。SNHL患者听觉皮层FC与符号数字模态测试(SDMT)得分相关,反映了注意功能、加工速度和视觉工作记忆。与听力相关的FC与dlPFC在舌皮质中发现。基于束的空间统计(TBSS)分析显示,分数各向异性(FA)值下降,主要发生在颞下额枕束(IFOF),与SNHL患者的平均听力阈值呈显著负相关。结论:长期SNHL后,dlPFC与听觉和视觉区域之间的功能耦合增强,并伴随着连接额叶皮层和枕颞区的IFOF沿线FA减少,可能通过自上而下的调节调节跨模态可塑性,促进听觉皮层参与高阶认知加工。
Objective: Hearing loss, one main risk factor of tinnitus and hyperacusis, is believed to involve significant central functional abnormalities. The recruitment of the auditory cortex in non-auditory sensory and higher-order cognitive processing has been demonstrated in the hearing-deprived brain. The dorsolateral prefrontal cortex (dlPFC), which has dense anatomical connections with the auditory pathway, is known to play a crucial role in multi-sensory integration, auditory regulation, and cognitive processing. This study aimed to verify the role of the dlPFC in the cross-modal reorganization and cognitive participation of the auditory cortex in long-term sensorineural hearing loss (SNHL) by combining functional and structural measurements.Methods: Thirty five patients with long-term bilateral SNHL and 35 matched healthy controls underwent structural imaging, resting-state functional magnetic resonance imaging (rs-fMRI), diffusion tensor imaging (DTI), and neuropsychological assessments. Ten SNHL patients were with subjective tinnitus.Results: No differences in gray matter volume, spontaneous neural activity, or diffusion characteristics in the dlPFC were found between the SNHL and control groups. The functional connectivity (FC) between the dlPFC and the auditory cortex and visual areas, such as the cuneus, fusiform, lingual cortex, and calcarine sulcus was increased in patients with SNHL. ANOVA and post hoc tests revealed similar FC alterations in the SNHL patients with and without tinnitus when compared with the normal hearing controls, and SNHL patients with and without tinnitus showed no difference in the dlPFC FC. The FC in the auditory cortex was associated with the symbol digit modality test (SDMT) scores in the SNHL patients, which reflect attentional function, processing speed, and visual working memory. Hearing-related FC with the dlPFC was found in the lingual cortex. A tract-based spatial statistics (TBSS) analysis revealed decreased fractional anisotropy (FA) values, mainly in the temporal inferior fronto-occipital fasciculus (IFOF), which showed remarkable negative correlations with the mean hearing thresholds in SNHL.Conclusion: Higher functional coupling between the dlPFC and auditory and visual areas, accompanied by decreased FA along the IFOF connecting the frontal cortex and the occipito-temporal area, might mediate cross-modal plasticity via top-down regulation and facilitate the involvement of the auditory cortex in higher-order cognitive processing following long-term SNHL.