Pain-Discriminating Information Decoded From Spatiotemporal Patterns of Hemodynamic Responses Measured by fMRI in the Human Brain

IF 3.5 2区 医学 Q1 NEUROIMAGING Human Brain Mapping Pub Date : 2024-11-01 DOI:10.1002/hbm.70065
Yingchao Song, Xiuzhi Wang, Qian Su, Rui Zhao, Juan Zhang, Wen Qin, Chunshui Yu, Meng Liang
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Abstract

Functional magnetic resonance imaging (fMRI) has been widely used in studying the neural mechanisms of pain in the human brain, primarily focusing on where in the brain pain-elicited neural activities occur (i.e., the spatial distribution of pain-related brain activities). However, the temporal dynamics of pain-elicited hemodynamic responses (HDRs) measured by fMRI may also contain information specific to pain processing but have been largely neglected. Using high temporal resolution fMRI (TR = 0.8 s) data acquired from 62 healthy participants, in the present study we aimed to test whether pain-distinguishing information could be decoded from the spatial pattern of the temporal dynamics (i.e., the spatiotemporal pattern) of HDRs elicited by painful stimuli. Specifically, the peak latency and the response duration were used to characterize the temporal dynamics of HDRs to painful laser stimuli and non-painful electric stimuli, and then were compared between the two conditions (i.e., pain and no-pain) using a voxel-wise univariate analysis and a multivariate pattern analysis. Furthermore, we also tested whether the two temporal characteristics of pain-elicited HDRs and their spatial patterns were associated with pain-related behaviors. We found that the spatial patterns of HDR peak latency and response duration could successfully discriminate pain from no-pain. Interestingly, we also observed that the Pain Vigilance and Awareness Questionnaire (PVAQ) scores were correlated with the average response duration in bilateral insula and secondary somatosensory cortex (S2) and could also be predicted from the across-voxel spatial patterns of response durations in the middle cingulate cortex and middle frontal gyrus only during painful condition but not during non-painful condition. These findings indicate that the spatiotemporal pattern of pain-elicited HDRs may contain pain-specific information and highlight the importance of studying the neural mechanisms of pain by taking advantage of the high sensitivity of fMRI to both spatial and temporal information of brain responses.

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从 fMRI 测量的人脑血流动力学反应时空模式解码疼痛鉴别信息
功能磁共振成像(fMRI)已被广泛用于研究人脑疼痛的神经机制,主要集中于大脑中疼痛诱发神经活动发生的位置(即与疼痛相关的大脑活动的空间分布)。然而,fMRI 测量的痛觉激发的血流动力学反应(HDR)的时间动态也可能包含疼痛处理的特定信息,但却在很大程度上被忽视了。在本研究中,我们利用从 62 名健康参与者那里获得的高时间分辨率 fMRI(TR = 0.8 秒)数据,旨在测试是否能从疼痛刺激引起的血液动力学反应的时间动态空间模式(即时空模式)中解码出疼痛区分信息。具体来说,我们使用峰值潜伏期和反应持续时间来描述疼痛激光刺激和非疼痛电刺激引起的 HDR 的时间动态,然后使用体素单变量分析和多变量模式分析对两种条件(即疼痛和无疼痛)进行比较。此外,我们还测试了疼痛诱发的 HDRs 的两个时间特征及其空间模式是否与疼痛相关行为有关。我们发现,HDR 峰值潜伏期和反应持续时间的空间模式可以成功区分疼痛与非疼痛。有趣的是,我们还观察到,疼痛警觉和意识问卷(PVAQ)的得分与双侧岛叶和次级体感皮层(S2)的平均反应时长相关,并且还可以通过扣带回中层和额叶中回反应时长的跨象素空间模式预测疼痛状态,而非疼痛状态则无法预测。这些发现表明,疼痛诱发的HDR的时空模式可能包含疼痛特异性信息,并强调了利用fMRI对大脑反应的空间和时间信息的高灵敏度研究疼痛神经机制的重要性。
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来源期刊
Human Brain Mapping
Human Brain Mapping 医学-核医学
CiteScore
8.30
自引率
6.20%
发文量
401
审稿时长
3-6 weeks
期刊介绍: Human Brain Mapping publishes peer-reviewed basic, clinical, technical, and theoretical research in the interdisciplinary and rapidly expanding field of human brain mapping. The journal features research derived from non-invasive brain imaging modalities used to explore the spatial and temporal organization of the neural systems supporting human behavior. Imaging modalities of interest include positron emission tomography, event-related potentials, electro-and magnetoencephalography, magnetic resonance imaging, and single-photon emission tomography. Brain mapping research in both normal and clinical populations is encouraged. Article formats include Research Articles, Review Articles, Clinical Case Studies, and Technique, as well as Technological Developments, Theoretical Articles, and Synthetic Reviews. Technical advances, such as novel brain imaging methods, analyses for detecting or localizing neural activity, synergistic uses of multiple imaging modalities, and strategies for the design of behavioral paradigms and neural-systems modeling are of particular interest. The journal endorses the propagation of methodological standards and encourages database development in the field of human brain mapping.
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