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基础研究
复发性与首发性抑郁症杏仁核静息态功能连接的对比研究
孙继飞 马跃 郭春蕾 罗屹 高山山 陈庆燕 洪洋 张国雷 方继良

Cite this article as: Sun JF, Ma Y, Guo CL, et al. Comparative study on resting functional connection of amygdala between recurrent and first-episode depression[J]. Chin J Magn Reson Imaging, 2022, 13(10): 144-149.本文引用格式:孙继飞, 马跃, 郭春蕾, 等. 复发性与首发性抑郁症杏仁核静息态功能连接的对比研究[J]. 磁共振成像, 2022, 13(10): 144-149. DOI:10.12015/issn.1674-8034.2022.10.022.


[摘要] 目的 通过对比复发性抑郁症(recurrent depressive episodes, RDE)与首发性抑郁症(first depressive episode, FDE)杏仁核静息态功能连接(functional connectivity, FC)差异,以探索RDE的FC改变特征。材料与方法 前瞻性纳入RDE患者、FDE患者及健康对照者(healthy controls, HCs)各21例,采集3组受试者静息态脑功能MRI数据,并完成临床抑郁、焦虑及冗思等量表的评定。采用单因素方差分析比较3组双侧杏仁核与全脑FC差异,并对结果进行高斯随机场校正。提取3组间FC有差异脑区的时间序列均值(FC值),对FC值进行事后两两比较,所得结果进行Bonferroni校正(P<0.016)。最后对3组间差异有统计学意义的脑区的FC值与临床量表评分进行Pearson相关分析。结果 (1)与FDE组比较,RDE组左侧杏仁核与左、右侧前扣带回/左侧眶部额上回的FC增强,RDE组右侧杏仁核与右侧中央前回/右侧楔前叶、右侧补充运动区/右侧中扣带回的FC增强。与HC组比较,RDE组左侧杏仁核与左、右侧前扣带回/左侧眶部额上回的FC增强。(2)RDE组左侧杏仁核与左、右侧前扣带回/左侧眶部额上回的FC值与中文版冗思量表(Rumination Response Scale, RRS)评分呈正相关(r=0.460,P=0.033)。结论 RDE与FDE在杏仁核与边缘神经环路、奖赏环路、体感运动区及默认网络的FC值存在差异,且RDE存在更为广泛的FC改变特征,这可能是RDE神经病理机制更为复杂的原因。
[Abstract] Objective To explore the functional connectivity (FC) alterations in RDE by comparing the resting-state FC differences in amygdala in recurrent depressive episodes (RDE) and first depressive episode (FDE) characteristics.Materials and Methods Twenty-one patients with RDE, patients with FDE, and healthy controls (HCs) were included, and resting-state brain function MRI data were collected from the 3 groups of subjects, and clinical depression, anxiety, and redundancy scales were completed. One-way ANOVA was used to compare the differences between bilateral amygdala and whole brain FC in the 3 groups, and the results were corrected for Gaussian random fields. Time series means (FC values) of the brain regions with differences in FC between the 3 groups were extracted and the results were Bonferroni corrected (P<0.016) for post hoc two-by-two comparisons of FC values. Finally, Pearson correlation analysis was performed between FC values and clinical scale scores for the statistically different brain regions among the 3 groups.Results (1) Compared with the FDE group, the FC of the left amygdala with the left and right anterior cingulate gyrus/left orbital part of the superior frontal gyrus was increased in the RDE group, and the FC of the right amygdala with the right precentral gyrus/right precuneus and right supplementary motor area/right middle cingulate gyrus was increased in the RDE group. Compared with the HC group, the FC of the left amygdala with the left and right anterior cingulate gyrus/left orbital part of the superior frontal gyrus was increased in the RDE group. (2) The FC values of the left amygdala and the left and right anterior cingulate/left orbital part of the superior frontal gyrus in the RDE group were positively correlated with the Rumination Response Scale (RRS) scores (r=0.460, P=0.033).Conclusions There were differences in FC between RDE and FDE in the amygdala and limbic circuits, reward circuit, somatosensory-motor areas and default mode network, and a more extensive FC alteration feature was present in RDE, which may be the reason why the neuropathological mechanism of RDE is more complex.
[关键词] 复发性抑郁症;首发性抑郁症;杏仁核;静息态;磁共振成像;功能连接
[Keywords] recurrent depressive episodes;first episode depression;amygdala;resting-state;magnetic resonance imaging;functional connection

孙继飞 1   马跃 1   郭春蕾 1   罗屹 1   高山山 1   陈庆燕 1   洪洋 2   张国雷 2*   方继良 1*  

1 中国中医科学院广安门医院功能成像室,北京 100053

2 中国中医科学院广安门医院放射科,北京 100053

张国雷,E-mail:glzhang2009@126.com 方继良,E-mail:Fangmgh@163.com

作者利益冲突声明:全部作者均声明无利益冲突。


基金项目: 国家自然科学基金面上项目 82174282,81774433 科技部国家重点研发计划 2018YFC1705802 中国中医科学院科技创新工程项目 CI2021A03301
收稿日期:2021-11-24
接受日期:2022-10-13
中图分类号:R445.2  R749.3 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.10.022
本文引用格式:孙继飞, 马跃, 郭春蕾, 等. 复发性与首发性抑郁症杏仁核静息态功能连接的对比研究[J]. 磁共振成像, 2022, 13(10): 144-149. DOI:10.12015/issn.1674-8034.2022.10.022

       2017年世界卫生组织报告表明,全世界已有超过3亿抑郁症(major depression disorder, MDD)患者,患病率高达4.4%,预计到2030年,抑郁症将居全球疾病总负担第一位[1]。更有研究表明[2],MDD患者的大部分负担源于抑郁的反复发作,其复发率高达70%,且个体复发率与发作次数呈正相关。精神病专家逐渐认识到,治疗MDD重要挑战是防止复发[3]。因此,了解RDE神经病理发病机制至关重要。

       近年来,功能磁共振成像(functional magnetic resonance imaging, fMRI)技术逐渐应用到精神及神经疾病领域[4, 5, 6]。静息态fMRI研究发现[7],与首发抑郁症(first depressive episode, FDE)比较,复发抑郁症(recurrent depressive episodes, RDE)在部分相同脑区的局部一致性和低频振幅分布范围更广。Liu等[8]研究发现,与RDE组比较,FDE组默认网络(default mode networks, DMN)、背侧注意网络和躯体运动网络的功能连接(functional connectivity, FC)降低,这表明FDE组可能存在多个脑网络的FC低连接性。任务态fMRI发现[9],与FDE组比较,RDE组在额叶和中央前回表现出异常激活。以上研究均提示RDE和FDE在部分脑区存在异常的神经病理机制差异。然而,目前关于RDE和FDE在边缘系统的FC差异尚缺乏研究。

       边缘系统作为人体复杂的神经网络,在情绪的生成表达、记忆的形成、储存和提取中起着至关重要的作用[10]。杏仁核是边缘系统的重要组成部分,与人体的情绪调控、学习记忆及恐惧攻击等心理行为有着密切关系[11]。既往研究表明[12],MDD患者存在杏仁核的脑结构和功能异常。然而,目前国内外尚缺乏对RDE患者杏仁核FC研究。因此,本研究基于fMRI技术,采用FC方法分析比较RDE、FDE及健康对照者(healthy controls, HCs)全脑自发功能活动差异,并探讨FC改变与临床症状的相关性,以提高临床对RDE的神经病理学机制的理解。

1 材料与方法

1.1 一般资料

       前瞻性纳入2018年1月至2021年10月于中国中医科学院广安门医院心身医学科、北京市第一中西医结合医院精神科确诊的RDE和FDE患者,HCs来源于广告招募。本研究遵守《赫尔辛基宣言》,全体受试者在纳入前需签署知情同意书,且本次研究经过中国中医科学院广安门医院伦理委员会批准(伦理批文号:2017-021-SQ)。

1.2 纳入标准

       RDE组:(1)参照美国精神病学会的《精神障碍诊断及统计手册》第五版(Diagnostic and Statistical Manual of Mental Disorders-Ⅴ, DSM-Ⅴ)中关于MDD的诊断标准;(2)年龄在18~70岁之间;(3)汉密顿抑郁量表17项版(Hamilton Depression Scale-17, HAMD-17)评分>17分;(4)右利手;(5)临床查体及实验室检查无明显异常;(6)经抗抑郁药治疗缓解后现复发,且入组前已停药至少4周。

       FDE组:首次发病,未接受过任何抗抑郁药物治疗,且满足上述RDE组纳入标准中除第6条外。

       HC组:(1)HAMD-17<7分;(2)右利手;(3)实验室检查和临床查体无明显异常,无精神疾病发作史。

1.3 排除标准

       (1)患有严重的神经系统疾病及心、脑、肾等躯体疾病者;(2)有药物毒品或酒精成瘾者;(3)有自杀风险受试者;(4)存在MRI检查禁忌者;(5)孕妇及哺乳期妇女。3组受试者中符合上述一条即予排除。

1.4 临床量表评估

       本研究所有受试者均接受HAMD-17、汉密尔顿焦虑量表(Hamilton Anxiety Scale, HAMA)、中文版冗思量表(Rumination Response Scale, RRS)、焦虑自评量表(Self-rating Anxiety Scale, SAS)、抑郁自评量表(Self-rating Depression Scale, SDS)评定。

1.5 静息态fMRI图像数据采集

       本研究所有受试者接受中国中医科学院广安门医院放射科Magneton Skyra 3.0 T磁共振扫描仪进行数据采集。血氧水平依赖扫描参数:TE 30 ms,TR 2000 ms,层间隔0.6 mm,层厚3.5 mm,32层,视野224 mm×224 mm,FA 90°,矩阵64×64,扫描时间6 min 46 s。高清结构像扫描参数:TE 2.98 ms,TR 2530 ms,层间距1.0 mm,层厚1.0 mm,128层,视野256 mm×256 mm,FA 7°,矩阵64×64,扫描时间6 min 3 s。

1.6 图像数据处理

       采用基于Matlab 2020a平台的DPARSF 5.0工具包,数据预处理如下:(1)将数据从 DICOM转换为NIFTI格式;(2)去除前10个时间点;(3)进行时间层校正及头动校正(去除再任意方向头动大于1.5 mm及运动旋转超过1.5°的患者);(4)空间标准化,将被试经过非线性转换到蒙特利尔神经学研究所(Montreal Neurological Institute, MNI)空间,重采样为3 mm×3 mm×3 mm的空间分辨率;(5)采用平滑核为6 mm进行空间平滑;(6)去线性漂移;(7)将头动、脑脊液信号、白质信号进行线性回归;(8)滤波,将上述预处理的图像进行0.01~0.08 Hz滤波。

       根据既往文献研究[13],将与MDD发病密切相关脑区杏仁核作为种子点。采用WFU_Pick Atlas_v3.0软件的解剖自动标记(anatomical automatic labeling, AAL)模板进行左、右杏仁核种子点提取,计算杏仁核的平均时间序列与全脑其他体素时间序列的相关系数(r),然后利用Fisher Z转换转化为Z值,最终得到FC的强度值。

1.7 统计学方法

       人口统计学资料及临床资料采用SPSS 23.0进行分析,符合正态分布的计量资料以均数±标准差表示,2组间比较采用独立样本t检验,3组间比较采用单因素方差分析,组间进一步两两比较采用最小显著性差异法(least-significantdifference, LSD)t检验,计数资料以例(%)表示,3组间比较采用卡方检验。P<0.05表示差异具有统计学意义。

       图像数据统计采用DPARSF 5.0软件进行分析,3组之间的FC值采用单因素方差分析,将3组被试的性别、年龄、受教育年限及头动参数作为协变量,对3组之间的FC值存在差异的脑区采用GRF校正,簇水平P<0.05、阈值体素水平P<0.005被定义为差异具有统计学意义。提取3组间FC有差异脑区的时间序列均值(FC值),对FC值进行事后两两比较,所得结果进行Bonferroni校正,P<0.016(0.05/3)表示差异具有统计学意义。最后分别对3组间差异有统计学意义的脑区的FC值与临床量表评分进行Pearson相关分析,P<0.05表示差异具有统计学意义。

2 结果

2.1 3组社会人口学资料

       本研究共纳入RDE患者21例、FDE患者21例及HCs 21例,3组性别、年龄及受教育年限相对匹配。RDE组、FDE组及HC组在年龄、性别及受教育年限方面差异均无统计学意义(均P>0.05),见表1

表1  RDE组、FDE组及HC组的社会人口学资料
Tab. 1  Sociodemographic data of RDE group, FDE group and HC group

2.2 3组临床资料比较

       RDE组及FDE组在HAMD-17、HAMA、SDS、SAS、RRS评分上明显高于HC组,差异均具有统计学意义(P均<0.05)(表2)。

表2  RDE组、FDE组及HC组的临床资料比较
Tab. 2  Comparison of clinical data of RDE group, FDE group and HC group

2.3 脑影像学结果

2.3.1 3组间杏仁核功能连接比较

       以年龄、性别、受教育年限及头动参数作为协变量,左侧杏仁核FC的3组间差异脑区为:左、右前扣带回/左侧眶部额上回。右侧杏仁核FC的3组间差异脑区为:右侧中央前回/右侧楔前叶、右侧补充运动区/右侧中扣带回。见表3图12

图1  3组方差分析后,左侧杏仁核功能连接的3组间差异脑区:左、右前扣带回/左侧眶部额上回(-6、36、-3),图A1、A2、A3代表冠状位、矢状位、横断位差异脑区的峰值图。右侧色阶代表color bar F值,颜色由红色到黄色表示FC值由低到高(F值,P<0.005,cluster P<0.05)。柱状图A表示对RDE、FDE、HC组FC值分别进行事后两两比较。*表示两组间比较差异具有统计学意义,经Bonferroni校正,满足P<0.016。FC:功能连接;RDE:复发性抑郁症;FDE:首发性抑郁症;HC:健康对照组。
Fig. 1  After three groups of ANOVA, three intergroup differential brain regions for functional connectivity of the left amygdala: left and right anterior cingulate gyrus/left orbital part of the superior frontal gyrus (-6, 36, -3), Figure A1, A2, A3 represent peak maps of coronal, sagittal, and transverse differential brain regions. Right color scale represents the color bar F value, and the color from red to yellow indicates the degree of FC value from low to high (F value, P<0.005, cluster P<0.05). Bar graph A indicates the comparison of FC values between two groups after doing things for RDE, FDE and HC groups respectively. * indicates a statistically significant difference between the two groups for comparison, meeting P<0.016 with Bonferroni correction. FC: functional connectivity; RDE: recurrent depressive episodes; FDE: first depressive episode; HCs: healthy controls.
图2  3组方差分析后,右侧杏仁FC的3组间差异脑区:右侧中央前回/右侧楔前叶(12、-42、57),右侧补充运动区/右侧中扣带回(6、-15、51),图B1、B2、B3代表右侧中央前回/右侧楔前叶冠状位、矢状位、横断位的峰值图,图C1、C2、C3代表右侧补充运动区/右侧中扣带回冠状位、矢状位、横断位的峰值图。右侧色阶代表color bar F值,颜色由红色到黄色表示FC值由低到高的程度(F值,P<0.005,cluster P<0.05)。柱状图B、C表示对RDE、FDE、HC组FC值分别进行事后两两比较。*表示两组间比较差异具有统计学意义,经Bonferroni校正,满足P<0.016。FC:功能连接;RDE:复发性抑郁症;FDE:首发性抑郁症;HCs:健康对照者。
Fig. 2  After the three groups of ANOVA, the three intergroup differential brain regions of the right amygdala FC: right precentral gyrus/right precuneus (12, -42, 57), right supplementary motor area/right middle cingulate gyrus (6, -15, 51), Figure B1, B2, B3 represent the peak maps of right precentral gyrus/right precuneus coronal, sagittal, and transverse, Figure C1, C2, C3 represent the peak maps of right supplementary motor area/right middle cingulate gyrus coronal, sagittal, and transverse. Right color scale represents color bar F value, color from red to yellow indicates the degree of FC value from low to high (F value, P<0.005, cluster P<0.05). Bar graphs B and C represent two-by-two comparisons of FC values after doing things for RDE, FDE, and HC groups, respectively. * indicates a statistical difference between the two groups for comparison, which was corrected by Bonferroni to meet P<0.016. FC: functional connectivity; RDE: recurrent depressive episodes; FDE: first depressive episode; HCs: healthy controls.
表3  RDE组、FDE组及HC组与左、右侧杏仁核FC异常的脑区统计表
Tab. 3  Statistical table of brain areas with abnormal FC of the left and right amygdala in the RDE group, FDE group and HC group

2.3.2 3组杏仁核功能连接值两两组间比较

       分别对RDE组、FDE组及HC组做事后分析,进行组间两两比较3组双侧杏仁核与全脑有差异脑区的FC值。

       相较于FDE组,RDE组左侧杏仁核与左、右前扣带回/左侧眶部额上回的FC增强。RDE组右侧杏仁核与右侧中央前回/右侧楔前叶、右侧补充运动区/右侧中扣带回的FC增强。

       相较于HC组,RDE组左侧杏仁核与左、右前扣带回/左侧眶部额上回的FC增强。见表3图12

2.3.3 3组间差异脑区低频振幅值与临床量表相关分析

       RDE组左侧杏仁核与左、右前扣带回/左侧眶内额上回的FC值与RRS量表评分呈正相关(P=0.033,r=0.460),见图3

图3  RDE组左侧杏仁核和左、右前扣带回/左侧眶内额上回的FC值与RRS量表评分呈正相关。RDE:复发性抑郁症;FC:功能连接;RRS:中文版冗思量表。
Fig. 3  FC values of the left amygdala and left and right anterior cingulate/left orbital part of the superior frontal gyrus in the RDE group were positively correlated with RRS scale scores. RDE: recurrent depressive episodes; FC: functional connectivity; RRS: Rumination Response Scale.

3 讨论

       本研究发现RDE与FDE在杏仁核与边缘神经环路、奖赏环路、体感运动区及DMN的FC存在差异,且RDE患者在这些部分脑区存在更为广泛的FC,我们推测这可能是RDE神经病理机制更为复杂的原因。据我们所知,这是第一项采用基于静息态fMRI的FC方法,以杏仁核为感兴趣区观察RDE和FDE患者的脑功能活动差异的研究。

3.1 RDE杏仁核-边缘系统、奖赏环路FC异常

       本研究发现,与FDE组比较,RDE组左侧杏仁核与左、右前扣带回及左侧眶部额上回的FC增强,且右侧杏仁核与右侧中扣带回的FC也增强。扣带回位于胼胝体与大脑半球内侧扣带沟之间,是边缘神经环路重要组成部分。扣带回主要包括前扣带回、中扣带回以及后扣带回[14]。前扣带回参与调节人体情绪、运动、感觉和认知行为,与MDD发病密切相关[15]。研究表明[16],前扣带回与杏仁核具有高度连通性,形成杏仁核-扣带回环路。Workman等[17]发现,前扣带回与杏仁核的FC异常改变能够有效区别MDD和HCs。另一项研究表明[18],RDE患者杏仁核与内侧前额叶及膝下扣带回的FC较HC组增强,这支持了本研究结果。因此,本研究结果提示RDE患者在杏仁核和前扣带回的FC存在代偿性激活,这可能是RDE发病的重要的神经病理机制。

       左侧眶部额上回位于内侧额叶眶区,该区域与快感缺失和奖赏动机有关,是奖赏网络的重要组成部分[19, 20]。既往研究发现[21, 22],MDD组较HC组在杏仁核与内侧眶额皮质的FC增强,这提示MDD组存在杏仁核和奖赏环路的代偿性激活。另一项研究发现[23],与HC组比较,缓解性MDD组存在杏仁核与奖赏网络的FC增强,这可能与缓解性MDD组负性情绪和奖赏功能障碍相互作用有关。冗思症状是个体反复关注自身消极情绪的思维方式,是MDD核心症状之一[24]。冗思水平越高,提示陷入抑郁情绪时间越长。本研究相关性分析显示,RDE组左侧杏仁核与左、右前扣带回/左侧眶部额上回的FC值和RRS量表评分呈正相关,而在FDE患者中未发现此现象,则提示RDE患者的发病与情感、认知及奖赏环路的代偿性激活有关。

3.2 RDE杏仁核-体感运动区FC异常

       本研究中,与FDE组比较,RDE组右侧杏仁核与右侧中央前回及右侧补充运动区的FC增强。中央前回及补充运动区均属于大脑皮质运动区,参与人体的位置感觉和运动的神经冲动,是额顶网络的重要组成部分,与执行控制和情绪管理功能密切相关[25, 26]。既往研究发现[9],与FDE组比较,RDE患者在中央前回存在异常的功能激活。也有研究发现[27],与HC组比较,有自杀意念的MDD患者杏仁核与体感运动区的FC降低。根据本研究结果,我们推测这可能与RDE患者病程较长和前期服用抗抑郁药物有关。

3.3 RDE杏仁核-默认网络FC异常

       本研究还发现RDE组右侧杏仁核与右侧楔前叶的FC较FDE组增强。楔前叶参与着人体情感加工、视觉意象、情景记忆等功能,是后DMN重要的中心节点[28]。Sun等[7]研究发现,与FDE组比较,RDE组的后DMN的低频振幅增高。既往研究表明[29],抑郁程度越严重,楔前叶与颞顶叶交界处的FC越弱,与背内侧前额叶皮质的FC越强。Zhang等[30]研究发现,与HC组相比,FDE患者在右侧杏仁核与楔前叶的FC减低,这提示FDE患者存在杏仁核与DMN之间的FC损伤。Albert等[31]研究发现,有MDD病史的抑郁患者在杏仁核和DMN表现出更高的FC。因此,本研究结果提示,RDE患者右侧杏仁核与右侧楔前叶的FC较FDE患者更为异常,这表明杏仁核与楔前叶的FC异常是FDE和RDE重要的神经病理机制差异。

3.4 本研究的不足

       本研究还存在一定不足之处:(1)本研究样本量偏少,年龄跨度大,未来将进一步进行扩大样本量、按年龄层次划分进行研究,从而为挖掘RDE和FDE的早期鉴别诊断或可能临床用药提供依据;(2)RDE患者纳入虽有一段时间药物脱洗期,但也可能存在前期抗抑郁药物的潜在影响,且不同患者的发作次数和病程也是潜在的混淆因素;(3)本研究阈值体素水平设置P<0.005,统计效力较弱,阈值体素水平设置P<0.001更为合理。

       综上所述,本研究采用FC分析方法,以双侧杏仁核为种子点进行研究,结果发现RDE患者较FDE患者存在更为广泛的FC,主要在边缘神经环路、奖赏环路、体感运动区及默认网络等部分脑区存在差异,这可能是RDE神经病理机制更为复杂的原因。这项研究有利于为RDE患者临床诊断提供一定依据。在未来的研究中我们将进一步扩大样本量,采用更为严格的统计效力以提高本研究的科学价值。

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