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临床研究
rtfMRI-NF技术调控杏仁核改善失眠障碍的作用
张淼 武肖玲 李中林 邹智 周菁 申雨 祁菲 谷宇昂 贾淑蕾 窦社伟 闫峰山 李永丽

Cite this article as: ZHANG M, WU X L, LI Z L, et al. Regulation of amygdala by rtfMRI-NF technique in improving insomnia disorder[J]. Chin J Magn Reson Imaging, 2023, 14(7): 5-9.本文引用格式:张淼, 武肖玲, 李中林, 等. rtfMRI-NF技术调控杏仁核改善失眠障碍的作用[J]. 磁共振成像, 2023, 14(7): 5-9. DOI:10.12015/issn.1674-8034.2023.07.002.


[摘要] 目的 探讨实时功能磁共振成像的神经反馈(real-time functional magnetic resonance imaging neurofeedback, rtfMRI-NF)技术调控失眠障碍(insomnia disorder, ID)患者杏仁核改善ID的作用。材料与方法 招募ID患者33名,采用rtfMRI-NF技术干预3周(1次/周),采集干预前后静息态脑功能数据和匹兹堡睡眠质量指数(Pittsburgh Sleep Quality Index, PSQI)、失眠严重程度指数量表(Insomnia severity index scale, ISI)、汉密尔顿抑郁量表(Hamilton Depression Scale, HAMD)、贝克抑郁症量表(Beck Depression Inventory, BDI)和汉密尔顿焦虑量表(Hamilton Anxiety Scale, HAMA)。以双侧杏仁核为种子点,计算其与全脑体素的功能连接(functional connectivity, FC),使用配对样本t检验比较干预前后差异有统计学意义的脑区,提取干预后差异有统计学意义脑区的FC值,与临床量表评分进行相关性分析。结果 rtfMRI-NF技术干预后ID患者PSQI、ISI、HAMA、HAMD评分均低于干预前(P<0.05),BDI评分与干预前比较差异无统计学意义;ID患者干预后左侧杏仁核与左侧颞中回、左侧额内侧回、右侧楔前叶、右侧楔叶的FC值增大;左侧杏仁核与右侧顶上回、右侧颞上回、左侧额中回的FC值减小(GRF校正,体素水平P<0.001,团块水平 P<0.05)。并且干预后左侧杏仁核-右侧楔前叶的FC值与PSQI评分呈负相关(r=-0.477,P<0.01),左侧杏仁核-右侧顶上回FC值与HAMA评分呈负相关(r=-0.586,P<0.01)。结论 rtfMRI-NF技术可改善ID患者睡眠质量和情绪状态,其机制可能是左侧杏仁核和默认网络、情绪调节、认知相关脑区之间的FC变化有关。
[Abstract] Objective To investigate the effect of real-time functional magnetic resonance imaging neurofeedback (rtfMRI-NF) on amygdala in patients with insomnia disorder (ID).Materials and Methods Twenty-nine patients with ID were recruited, and the rtfMRI-NF technique was used for intervention for 3 weeks (once per week). Rest-state functional magnetic resonance imaging data and Pittsburgh Sleep Quality Index (PSQI), Insomnia severity index scale (ISI), Hamilton Depression Scale (HAMD), Beck Depression Inventory (BDI), Hamilton Anxiety Scale (HAMA) were collected before and after the intervention. The bilateral amygdala was used as the seed point to calculate functional connectivity (FC) between the amygdala and the whole brain voxels. The paired t-test was used to compare the statistically significant difference brain areas before and after the intervention, and the FC values of the statistically significant difference brain areas after the intervention were extracted to conduct correlation analysis with clinical scale scores.Results PSQI, ISI, HAMA and HAMD scores of patients with ID were lower after rtfMRI-NF technique intervention than before intervention (P<0.05), and there was no statistical significance in BDI scores compared with before intervention. After intervention, the FC values of the left amygdala with left middle temporal gyrus, left medial frontal gyrus, right precuneus and right precuneus increased in patients with ID. FC values decreased in the left amygdala with right parietal gyrus, right superior temporal gyrus, and left middle frontal gyrus (GRF correction, voxel level P<0.001, mass level P<0.05). And after intervention, the FC values of the left amygdala with the right precuneus were negatively correlated with PSQI scores (r=-0.477, P<0.01), and the FC values of the left amygdala with the right top gyrus were negatively correlated with HAMA scores (r=-0.586, P<0.01).Conclusions rtfMRI-NF technology can improve the sleep quality and emotional state of the patients with ID, and the mechanism may be related to the changes of functional connections between the left amygdala with the default network, emotional regulation, and cognitive brain regions.
[关键词] 失眠障碍;实时功能磁共振成像的神经反馈;杏仁核;功能连接;静息态功能磁共振成像;磁共振成像
[Keywords] insomnia disorder;real-time functional magnetic resonance imaging neurofeedback;amygdala;functional connectivity;rest-state functional magnetic resonance imaging;magnetic resonance imaging

张淼 1   武肖玲 2   李中林 1   邹智 1   周菁 3   申雨 1   祁菲 1   谷宇昂 4   贾淑蕾 4   窦社伟 1   闫峰山 1   李永丽 3*  

1 郑州大学人民医院/河南省人民医院医学影像科,郑州 450003

2 河南省人民医院/郑州大学人民医院核医学科,郑州 450003

3 河南省人民医院健康管理科,郑州 450003

4 新乡医学院 河南省人民医院医学影像科,郑州 450000

通信作者:李永丽,E-mail:shyliyongli@126.com

作者贡献声明:李永丽设计本研究的方案,对稿件重要内容进行了修改;张淼起草和撰写稿件,获取、分析或解释本研究的数据;武肖玲、李中林、邹智、周菁、申雨、祁菲、谷宇昂、贾淑蕾、窦社伟、闫峰山获取本研究的数据,对稿件重要内容进行了修改。李永丽、武肖玲、李中林、邹智、周菁获得国家科学自然基金项目、河南省中青年卫生健康科技创新人才项目、河南省科技攻关项目资助。全体作者都同意发表最后的修改稿,同意对本研究的所有方面负责,确保本研究的准确性和诚信。


基金项目: 国家自然科学基金 82071884 河南省中青年卫生健康科技创新人才项目 YXKC2020004 河南省科技攻关项目 222102310198
收稿日期:2023-01-19
接受日期:2023-06-25
中图分类号:R445.2  R338.63 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2023.07.002
本文引用格式:张淼, 武肖玲, 李中林, 等. rtfMRI-NF技术调控杏仁核改善失眠障碍的作用[J]. 磁共振成像, 2023, 14(7): 5-9. DOI:10.12015/issn.1674-8034.2023.07.002.

0 前言

       最新世界卫生组织在一个大规模调研中发现,有高达30%以上的中国人存在失眠问题[1]。长期失眠会增加精神障碍[2, 3]、心脑血管疾病[4]、代谢性疾病[5]、肿瘤[6]等的发生率,严重影响人类的生活健康。临床长期药物治疗具有药物依赖及一系列副作用。目前临床上非药物辅助治疗失眠障碍(insomnia disorder, ID)的主要是认知行为疗法(cognitive behavioral therapy, CBT)和神经反馈[7, 8]。但CBT目前存在一定的盲目性,不能实时观察大脑活动的变化,无法阐明其有效的神经生物学机制。实时功能磁共振成像的神经反馈(real-time functional magnetic resonance imaging neurofeedback, rtfMRI-NF)具有空间分辨率和定位精度高等优点,可以实时分析、快速采集、有针对性地同步反馈给受试者大脑神经活动信息,受试者根据接收到的反馈信息进行训练并自主调节脑靶区激活水平,进而提高受试者神经可塑性及学习能力[9, 10, 11, 12]。BAGLIONI等[13]和SCHIEL等[14]认为,ID患者的杏仁核对负面刺激的调节能力降低,杏仁核对情绪和压力的调节不良可能导致ID的发生。研究报道ID患者双侧杏仁核功能异常,可能是ID患者产生情绪调节障碍、认知障碍等的机制之一[15]。许多使用rtfMRI-NF训练的研究通过回忆积极的自传体记忆帮助患者调节左侧杏仁核的活动,成功改变了大脑功能与临床症状[16, 17, 18]。本研究采用rtfMRI-NF技术上调ID患者左侧杏仁核活动,比较干预前后双侧杏仁核与全脑体素功能连接(functional connectivity, FC)的变化,对rtfMRI-NF技术改善ID的静息态功能磁共振成像(rest-state functional magnetic resonance imaging, rs-fMRI)作用进行研究,揭示ID大脑神经生物学水平变化,为rtfMRI-NF技术改善ID提供客观的神经影像学依据。

1 材料与方法

1.1 一般资料

       招募2021年12月至2022年12月于河南省人民医院诊治的ID患者。纳入标准:(1)符合《中国精神障碍分类与诊断标准(第三版)》和《美国精神疾病诊断与统计手册(第五版)》中有关ID的诊断标准;(2)年龄18~60岁;(3)匹兹堡睡眠质量指数(Pittsburgh Sleep Quality Index, PSQI)评分≥7分[19];(4)常规头颅MRI检查正常;(5)受教育经历初中或初中以上;(6)右利手。排除标准:(1)由于睡眠障碍性疾病导致的失眠(如睡眠周期性肢体运动、阻塞性睡眠呼吸暂停综合征等导致的失眠);(2)有神经疾病病史、头部外伤史;(3)正在妊娠;(4)患有严重的自杀意念,严重精神障碍;(5)有烟酒和药物滥用史;(6)有重大躯体疾病史。本研究遵守《赫尔辛基宣言》,得到河南省人民医院伦理委员会批准(伦理批准号:2021伦审第67号),研究对象均签署知情同意书,遵循自愿法则。最终招募33例ID被试,其中男7例,女26例;年龄19~60(45.8±12.9)岁。

1.2 方法

1.2.1 试验方案

       rtfMRI-NF技术干预前采集:被试相关量表信息PSQI、失眠严重程度指数量表(Insomnia severity index scale, ISI)、汉密尔顿抑郁量表(Hamilton Depression Scale, HAMD)、贝克抑郁症量表(Beck Depression Inventory, BDI)和汉密尔顿焦虑量表(Hamilton Anxiety Scale, HAMA)以及rs-fMRI数据;在头颅MRI扫描当晚行多导睡眠图(polysomnography, PSG)检查,排除患有隐匿性睡眠障碍的被试。然后进行为期3周的rtfMRI-NF干预(1次/周),干预后数据采集内容同干预前。

1.2.2 rtfMRI-NF方法

       rtfMRI-NF干预前嘱ID被试至少准备三件与自己密切相关的高兴记忆事件。一次完整rtfMRI-NF流程:(1)rs-fMRI扫描(嘱被试尽量保持大脑放空状态,记录大脑的静息状态活动);(2)测试训练(让被试熟悉流程,当屏幕呈现“静息”时,嘱被试大脑放空,保持静息状态30 s;当屏幕呈现“高兴”时,嘱被试回忆高兴事件30 s,交替进行6次);(3)连续3组线上反馈训练(选取情绪中枢关键脑区杏仁核为靶区,指导被试通过回忆高兴记忆事件调动情绪,进而使杏仁核活动升高。反馈信号以屏幕上绿色线条形式呈现,当绿色线条升高时,表示该情绪调节策略有效);(4)线上无反馈训练[同流程(2)];(5)干预后rs-fMRI扫描[同流程(1)]。

1.2.3 头颅MRI扫描

       所有被试头颅MRI均由河南省人民医院放射科专业技术人员扫描,使用德国Siemens公司的Prisma 3.0 T磁共振扫描机器,64通道头线圈。常规MRI扫描序列为T1WI(TR 25 ms,TE 2.4 ms,视野230 mm×230 mm,层数18,层厚6 mm)、T2WI(TR 5000 ms,TE 96 ms,视野 230 mm×230 mm,层数18,层厚6 mm)、FLAIR(TR 7500 ms,TE 81 ms,视野 230 mm×230 mm,层数18,层厚6 mm)轴位扫描,排除颅脑器质性病变后使被试保持静息状态,同时采集rs-fMRI数据(使用梯度回波结合单次激发回波平面成像技术,210个体积持续420 s。相应的采集参数设置如下:TR 2000 ms,TE 30 ms,视野224 mm×224 mm,矩阵112×112,层数27,层厚2 mm)。

1.2.4 脑功能成像数据处理

       基于MATLAB 2018a平台和DPABI(http://rfmri.org/DPABI),进行rs-fMRI数据的预处理和FC分析。预处理具体步骤包括:(1)将图像DICOM格式转换成NIFTI文件格式;(2)剔除前10个时间点;(3)头动校正;(4)空间标准化,将单个高分辨率T1解剖图像记录到平均rs-fMRI数据中;(5)空间平滑(半峰全宽为6 mm×6 mm×6 mm进行高斯平滑)以增加图像信噪比;(6)去线性漂移、时间滤波(带宽0.01~0.08 Hz);(7)去除在任意方向上头动平移>2 mm、旋转角度>2°的图像数据。排除4名头动>2 mm、旋转角度>2°的ID被试。

1.2.5 FC分析

       根据预处理好的rs-fMRI数据,使用DPABI软件从Automated Anatomical Labeling(AAL)中选取双侧杏仁核(左侧:X=-24、Y=-1、Z=-17;右侧:X=26、Y=1、Z=-18)为感兴趣区(region of interest, ROI),以双侧杏仁核坐标半径6 mm的球形种子点,计算其与全脑所有体素的时间序列的相关性,并进行Fisher Z转换,最终得到标准化的FC值。

1.2.6 统计学方法

       使用DPABI软件(http://rfmri.org/DPABI)对ID被试干预3周前后FC值进行配对样本t检验分析,并进行GRF校正,单个体素P<0.001,校正后P<0.05的区域定义为与杏仁核FC有统计学意义的差异脑区。使用SPSS 23.0软件采用配对t检验比较ID被试rtfMRI-NF技术干预前后PSQI、ISI、HAMA、HAMD、BDI评分变化,P<0.05表示差异具有统计学意义;对干预后差异脑区的FC值与临床量表评分进行Pearson相关分析,P<0.01为差异有统计学意义,|r|值越大,表示相关性越强。

2 结果

2.1 ID被试干预3周前后临床量表评分比较

       与干预前比,ID被试干预3周后PSQI、ISI、HAMA、HAMD评分降低,差异具有统计学意义(P<0.05),BDI评分与干预前比较差异无统计学意义(P>0.05),见表1

表1  ID干预3周前后临床量表评分比较
Tab. 1  Comparison of clinical scale scores before and after ID intervention

2.2 rs-fMRI FC结果

       以右侧杏仁核为种子点时,未发现ID被试干预前后有统计学意义差异的脑区。以左侧杏仁核为种子点时,与干预前相比,ID患者被试干预后左侧杏仁核与左侧颞中回、左侧额内侧回、右侧楔前叶、右侧楔叶的FC值增大;左侧杏仁核与右侧顶上回、右侧颞上回、左侧额中回的FC值减小(GRF校正,体素水平P<0.001,团块水平P<0.05),见表2图1

图1  与干预前相比,干预后ID患者与左侧杏仁核FC差异具有统计学意义的脑区(GRF 校正,体素水平P<0.001,团块水平P<0.05)。暖色代表干预后FC 值增大,冷色代表干预后FC 值减小。ID:失眠障碍;FC:功能连接。
Fig. 1  Compared with pre-intervention, there is a statistically significant difference between the FC of the left amygdala in patients with ID after intervention (GRF-adjusted, voxel level P<0.001, mass level P<0.05). Warm color represents the increase of FC value after intervention, while cool color represents the decrease of FC value after intervention. ID: insomnia disorder; FC: functional connection.
表2  失眠障碍被试患者干预前后左侧杏仁核与全脑功能连接差异的脑区分布
Tab. 2  Brain region distribution of the difference between the left amygdala with the whole brain functional connectivity in patients with insomnia disorder before and after intervention

2.3 左侧杏仁核-差异脑区FC强度与临床量表的相关性

       干预后左侧杏仁核-右侧楔前叶的FC值与PSQI评分呈负相关(r=-0.477,P<0.01),左侧杏仁核-右侧顶上回的FC值与HAMA评分(r=-0.586,P<0.01)呈负相关,见图2

图2  rtfMRI-NF技术干预后,左侧杏仁核-右侧楔前叶(2A)、左侧杏仁核-右侧顶上回FC值(2B)与临床量表评分的相关性散点图。rtfMRI-NF:实时功能磁共振成像的神经反馈;PSQI:匹兹堡睡眠量表;HAMA:汉密尔顿焦虑量表;FC:功能连接。
Fig. 2  Scatter plot of correlation between FC value of left amygdala with right precuneus and left amygdala with right apex gyrus and clinical scale score after intervention with rtfMRI-NF technique. rtfMRI-NF: Neurofeedback in real-time functional magnetic resonance imaging; PSQI: Pittsburgh Sleep Scale; HAMA: Hamilton Anxiety Scale; FC: functional connection.

3 讨论

       本研究通过采用基于ROI的全脑FC的分析方法评估rtfMRI-NF技术调控ID患者双侧杏仁核与全脑体素FC的变化。本研究结果显示,rtfMRI-NF技术不仅可以改善ID患者的睡眠质量、情绪状态,并且干预后左侧杏仁核与左侧颞中回、左侧额内侧回、右侧楔前叶、右侧楔叶的FC值增大;左侧杏仁核与右侧顶上回、右侧颞上回、左侧额中回的FC值减小,该研究从神经影像学角度证实了rtfMRI-NF技术在改善ID方面的重要临床价值。

3.1 rtfMRI-NF技术可改变ID患者左侧杏仁核与默认网络的FC

       默认网络(default mode network, DMN)与睡眠剥夺、情绪调节以及认知的处理和整合有关[14,20, 21, 22]。此外,ID患者中DMN的FC增强可能与高度觉醒的应对障碍有关[14]。颞中回、额内侧回、楔前叶属于DMN,其中颞中回与情绪调节、语义记忆处理等认知功能有关,并且被认为参与快速眼动(rapid eye movement, REM)和非REM睡眠中的梦境的编码与回忆[23, 24]。YAN等[25]发现ID患者左侧颞中回度中心度值减低。左侧颞中回FC异常,可能是ID患者疾病过程中的重要神经影像学标记。rtfMRI-NF技术改善ID可能与左侧杏仁核与左侧颞中回的FC重塑有关。额内侧回是内侧前额叶的重要组成部分,与情绪的加工、对内外环境的监测、情景记忆等认知活动密切相关[26]。内侧前额叶不仅在功能上,而且在结构上和杏仁核之间存在联系[27],在情绪产生和调节中具有重要作用。研究发现,楔前叶和杏仁核之间的FC,参与了注意力部署过程中的情绪调节[28]。另外,有研究表明楔前叶与ID患者的失眠严重程度相关[29]。本研究结果显示ID患者经干预后左侧杏仁核-右侧楔前叶FC值与PSQI评分呈现负相关,证明rtfMRI-NF技术或通过重塑左侧杏仁核与右侧楔前叶FC进而改善ID患者的睡眠质量。

3.2 rtfMRI-NF技术重塑ID患者左侧杏仁核与情绪调节、认知相关脑区的FC

       楔叶位于枕叶,属于高级视觉中枢,它涉及与工作记忆和/或视觉记忆巩固[30, 31]。最近一项动物研究证实枕叶皮层参与睡眠状态的控制[32]。一项rs-fMRI研究发现ID患者涉及楔叶功能失调[33]。顶上回属于额顶网络区域与空间认知和感觉运动整合有关[34]。本研究结果显示rtfMRI-NF技术干预后左侧杏仁核-右侧顶上回FC值与抑郁情绪相关,然而关于顶上回与ID的研究较少,未来还需更多研究重复验证。既往rs-fMRI研究发现右侧颞上回高度参与了情绪加工和社会认知[35]。WANG等[36]发现颞上回皮层厚度与睡眠质量较差有关,颞上回皮层厚度介导了情绪症状与睡眠质量之间的关联。YE等[37]发现,与失眠症状不严重的抑郁症患者相比,失眠症状严重的抑郁症患者杏仁核与双侧颞上回的FC增高,本研究结果发现rtfMRI-NF技术干预后左侧杏仁核-右侧颞上回FC值减小,说明ID患者经rtfMRI-NF技术干预后脑区功能重塑好转。左侧额中回属于背外侧前额叶,是认知控制网络的重要脑区,参与执行功能、认知控制功能和情绪的产生、调节相关[26,38]。rs-fMRI研究发现睡眠剥夺后的健康被试双侧杏仁核与双侧额中回的FC增强[39]。本研究结果显示,干预后左侧杏仁核与左侧额中回FC减少,说明了经rtfMRI-NF技术可重塑ID患者静息态脑FC。

3.3 本研究局限性

       本研究属于无控制组,未来将设立安慰剂控制组[40]进一步验证rtfMRI-NF技术改善ID的临床价值。此外,rtfMRI-NF技术改善ID的长期效应,还需随访进一步验证。

4 结论

       综上所述,推测rtfMRI-NF技术可能通过调节左侧杏仁核与DMN以及情绪、认知处理相关脑区间的FC,从而改善ID患者的睡眠质量、情绪状态。这项研究有利于为rtfMRI-NF技术改善ID患者临床症状提供一定神经影像学依据。

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