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Article(id=1208106716605026581, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1208106710208717234, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2022.04.0382, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1635868800000, receivedDateStr=2021-11-03, revisedDate=null, revisedDateStr=null, acceptedDate=1638460800000, acceptedDateStr=2021-12-03, onlineDate=1765964686776, onlineDateStr=2025-12-17, pubDate=1651075200000, pubDateStr=2022-04-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1765964686776, onlineIssueDateStr=2025-12-17, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1765964686776, creator=13701087609, updateTime=1765964686776, updator=13701087609, issue=Issue{id=1208106710208717234, tenantId=1146029695717560320, journalId=1189873630562394117, year='2022', volume='47', issue='4', pageStart='321', pageEnd='426', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1765964685250, creator=13701087609, updateTime=1765964685250, updator=13701087609, preIssue=null, nextIssue=null, ext=null, issueFiles=null}, startPage=382, endPage=389, ext={EN=ArticleExt(id=1208106716969931044, articleId=1208106716605026581, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Mechanism of multimodel visual exploration disorder in Parkinson's disease based on an infrared eye movement system, columnId=1190310109000602400, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Clinical Research, runingTitle=null, highlight=null, articleAbstract=

Objective Record and analyze the disease effects and aging effects of eye movement indicators of visual information processing system in target exploration mission through an infrared eye-movement assessment system, and explore the pathogenesis of the visual exploration disorder in patients with Parkinson's disease (PD). Methods It is a cross-sectional study. A total of 32 patients with PD and normal cognition on dopaminergic drugs were recruited (PD group) from the Dyskinesia clinic of Dalian Friendship Hospital from October 2020 to June 2021; 33 age-, gender- and education-matched healthy volunteers with normal cognition were recruited (AMC group) from the medical center of our hospital, and 33 gender- and education-matched healthy young medical intern volunteers were recruited (YC group) from medical interns in our hospital during the same period. Behavioral and eye-movement indicators of all subjects were recorded with an infrared eye movement assessment system by testing to figure-matching tasks representing the visual information processing (clock-matching task and inverted clock-matching task) and saccade tasks representing the oculomotor function. The accuracy, saccade latency, and saccade size of saccade tasks, as well as the accuracy,the reaction time, the number of saccades visiting the sample area of interest (AOI), the number of saccades visiting array AOIs, and the de-efficiency score of clock matching tasks were analyzed. The PD group's clinical characteristics (disease duration, doses of anti-Parkinsonian medication, and Hoehn-Yahr grading) and eye movement indicators with disease effect were analyzed. Results In saccade tasks, there was no significant difference in all indicators between AMC group and YC group (P>0.05). Compared with the indicators of PD group, the saccade amplitude of anti-saccade task increased in AMC group (P=0.003) and the YC group (P<0.001)with statistically significant difference. In clock-matching tasks, compared with the YC group, the reaction time of the AMC group(clock-matching task: P=0.005; reverse clock-matching task: P=0.008) and PD group (clock-matching task: P=0.002; reverse clock-matching task: P<0.001) was significantly prolonged with statistically significant difference. Compared with the PD group, the saccade numbers of visiting sample AOI (AMC group: P=0.011; YC group: P<0.001), the saccade numbers of visiting array AOIs(AMC group: P=0.023; YC group: P<0.001) and the de-efficiency score (AMC group: P=0.017; YC group: P=0.003) decreased with statistically significant differences. No statistically significant difference existed in another indicators among each groups in clock matching tasks (P>0.05). There was no obvious correlation in saccade amplitude of anti-saccade task to the numbers of saccade visiting sample AOI (r=–0.014, P=0.785), the numbers of saccade visiting array AOIs (r=–0.025, P=0.837) and de-efficiency score(r=–0.031, P=0.576) in the reverse clock-matching task. None obvious correlation of the clinical characteristics of PD group to the saccade amplitude in anti-saccade task, the numbers of saccade visiting the sample AOI, the numbers of saccade visiting array AOIs,and de-efficiency score in the inverted clock-matching task (P>0.05). Conclusion The results based on the infrared eye movement system showed that the visual exploration disorder of PD patients may be due to the combined action of visual information processing dysfunction and oculomotor dysfunction; disease effect and aging effect have different influences on the process of visual exploration.

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目的 通过红外眼动评估系统记录并分析目标探索任务中视觉信息处理系统眼动指标的疾病效应与衰老效应，探讨帕金森病患者视觉探索障碍的发生机制。方法 本研究为横断面研究。纳入2020年10月－2021年6月于大连市友谊医院运动障碍门诊临床确诊且正在使用多巴胺能药物的认知正常的帕金森病患者32例作为帕金森病组，另将本院体检中心招募的年龄、性别及受教育程度相匹配且认知正常的健康志愿者33例作为与帕金森病组年龄匹配的正常对照组(AMC组)，以及本院医护实习学生中招募的性别及受教育程度匹配的33例健康志愿者作为青年正常对照组(YC组)。所有受试者均进行代表视觉信息处理能力的图形匹配任务(时钟匹配任务与倒转时钟匹配任务)和代表动眼肌功能的扫视类任务，同时使用红外眼动评估系统记录各组受试者的行为和眼球运动指标。对扫视类任务的准确率、潜伏期和扫视幅度，以及时钟匹配类任务的准确率、反应时间、扫视样本图像感兴趣区域(AOI)次数、扫视阵列图像感兴趣区域(AOIs)次数和降效分数作为感兴趣眼动指标进行相关性分析；对帕金森病组的临床特征(疾病持续时间、抗帕金森病药物剂量和Hoehn-Yahr分级)与存在疾病效应的眼动指标进行相关性分析。结果 扫视类任务中，AMC组与YC组的各项指标比较差异均无统计学意义(P>0.05)；与帕金森病组的各项指标比较，AMC组(P=0.003)和YC组(P<0.001)在反向扫视任务中的扫视幅度均增高，差异有统计学意义。时钟匹配类任务中，与YC组比较，AMC组(时钟匹配任务：P=0.005；倒转时钟匹配任务：P=0.008)和帕金森病组(时钟匹配任务：P=0.002；倒转时钟匹配任务：P<0.001)的反应时间均明显延长，差异有统计学意义。与帕金森病组比较，AMC组及YC组在倒转时钟匹配任务中的访问样本图像AOI的扫视次数(AMC组：P=0.011；YC组：P<0.001)、访问阵列图像AOIs的扫视次数(AMC组：P=0.023；YC组：P<0.001)和降效分数(AMC组：P=0.017；YC组：P=0.003)减少，差异有统计学意义。时钟匹配类任务中其余各指标组间比较差异均无统计学意义(P>0.05)。反向扫视任务中的扫视幅度与倒转时钟匹配任务中访问样本图像AOI的扫视次数(r=–0.014，P=0.785)、访问阵列图像AOIs的扫视次数(r=–0.025，P=0.837)及降效分数(r=–0.031，P=0.576)均无明显相关性。帕金森病组的临床特征与反扫视任务的扫视幅度、倒转时钟匹配任务中访问样本图像AOI的扫视次数、访问阵列图像AOIs的扫视次数及降效分数均无相关性(P>0.05)。结论 基于红外眼动系统的结果提示，帕金森病患者的视觉探索障碍是由视觉信息处理功能失调和动眼肌功能障碍共同作用所致的，疾病效应和衰老效应对视觉探索过程存在不同性质的影响。

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杨旭，医学硕士，副主任医师，主要从事神经退行性疾病方面的研究

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杨旭，医学硕士，副主任医师，主要从事神经退行性疾病方面的研究

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杨旭，医学硕士，副主任医师，主要从事神经退行性疾病方面的研究

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Neuropsychologia, 2018, 117: 167-177., articleTitle=Subthalamic nucleus stimulation, dopaminergic treatment and impulsivity in Parkinson's disease, refAbstract=null)], funds=null, companyList=[AuthorCompany(id=1208106717762654538, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, xref=1, ext=[AuthorCompanyExt(id=1208106717766848843, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, companyId=1208106717762654538, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1Department of Neurology, Dalian Friendship Hospital, Dalian, Liaoning 116001, China), AuthorCompanyExt(id=1208106717775237452, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, companyId=1208106717762654538, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1大连市友谊医院神经内科，辽宁大连 116001)]), AuthorCompany(id=1208106717922038102, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, xref=2, ext=[AuthorCompanyExt(id=1208106717926232406, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, companyId=1208106717922038102, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2Department of Medical Imaging, Dalian Friendship Hospital, Dalian, Liaoning 116001, China), AuthorCompanyExt(id=1208106717934621015, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, companyId=1208106717922038102, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2大连市友谊医院影像科，辽宁大连 116001)])], figs=[ArticleFig(id=1208106719637508543, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, language=EN, label=Fig.1, caption=Example diagram of clock-matching task (A) and reverse clock-matching task (B) (Gray rectangles represent areas of interest)[15], figureFileSmall=9urZnA7l1qbBQEf6oVSYBQ==, figureFileBig=iFS72Y4gBtfSUUJn9SLnIQ==, tableContent=null), ArticleFig(id=1208106719704617411, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, language=CN, label=图1, caption=时钟匹配任务(A)和倒转时钟匹配任务(B)示例图(灰色矩形代表感兴趣区域)[15], figureFileSmall=9urZnA7l1qbBQEf6oVSYBQ==, figureFileBig=iFS72Y4gBtfSUUJn9SLnIQ==, tableContent=null), ArticleFig(id=1208106719893361098, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, language=EN, label=Tab.1, caption=

The demographic and clinical characteristics of each group

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项目帕金森病组(n=32)AMC组(n=33)YC组(n=33)t/χ2/FP
年龄(岁，$\bar{x}±s$)65.9±7.468.5±8.624.3±3.2333.422<0.001
性别(男/女，例)17/1516/1716/172.6820.612
教育程度(年，$\bar{x}±s$)12.7±1.513.1±1.214.3±0.92.7930.084
病程(月，$\bar{x}±s$)48.5±19.7––––
MoCA评分(分，$\bar{x}±s$)27.9±1.128.1±1.528.6±0.41.9540.167
UPDRS第Ⅲ部分评分(分，$\bar{x}±s$)21.3±5.2––––
H-Y分级(级，$\bar{x}±s$)2.3±0.7––––
LEDD(mg, $\bar{x}±s$)632.5±286.5––––
), ArticleFig(id=1208106719960469964, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, language=CN, label=表1, caption=

各组人口学及临床特征

, figureFileSmall=null, figureFileBig=null, tableContent=
项目帕金森病组(n=32)AMC组(n=33)YC组(n=33)t/χ2/FP
年龄(岁，$\bar{x}±s$)65.9±7.468.5±8.624.3±3.2333.422<0.001
性别(男/女，例)17/1516/1716/172.6820.612
教育程度(年，$\bar{x}±s$)12.7±1.513.1±1.214.3±0.92.7930.084
病程(月，$\bar{x}±s$)48.5±19.7––––
MoCA评分(分，$\bar{x}±s$)27.9±1.128.1±1.528.6±0.41.9540.167
UPDRS第Ⅲ部分评分(分，$\bar{x}±s$)21.3±5.2––––
H-Y分级(级，$\bar{x}±s$)2.3±0.7––––
LEDD(mg, $\bar{x}±s$)632.5±286.5––––
), ArticleFig(id=1208106720052744658, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, language=EN, label=Tab.2, caption=

Behavioral and eye movement measures in saccade tasks of each group

, figureFileSmall=null, figureFileBig=null, tableContent=
指标帕金森病组AMC组YC组H/FP帕金森病组vs. AMC组*AMC组vs. YC组*帕金森病组vs. YC组*
朝向扫视任务
 准确率[%, M(Q1, Q3)]91.3(75.2, 98.9)92.5(88.5, 98.7)97.5(90.3, 99.7)4.620.178–––
 潜伏期(ms, $\bar{x}±s$)158±56165±61142±502.700.524–––
 扫视幅度(°, $\bar{x}±s$)12.9±2.313.2±1.714.3±0.99.890.0270.6280.4090.065
反向扫视任务
 准确率(%, $\bar{x}±s$)48.2±19.351.0±14.662.5±17.412.250.0380.5690.1950.317
 潜伏期(ms, $\bar{x}±s$)252±110228±96206±656.620.0410.6450.1970.068
 扫视幅度(°, $\bar{x}±s$)9.4±3.513.9±1.614.5±1.918.21<0.0010.0030.359<0.001
), ArticleFig(id=1208106720145019347, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, language=CN, label=表2, caption=

各组扫视任务的行为和眼动指标

, figureFileSmall=null, figureFileBig=null, tableContent=
指标帕金森病组AMC组YC组H/FP帕金森病组vs. AMC组*AMC组vs. YC组*帕金森病组vs. YC组*
朝向扫视任务
 准确率[%, M(Q1, Q3)]91.3(75.2, 98.9)92.5(88.5, 98.7)97.5(90.3, 99.7)4.620.178–––
 潜伏期(ms, $\bar{x}±s$)158±56165±61142±502.700.524–––
 扫视幅度(°, $\bar{x}±s$)12.9±2.313.2±1.714.3±0.99.890.0270.6280.4090.065
反向扫视任务
 准确率(%, $\bar{x}±s$)48.2±19.351.0±14.662.5±17.412.250.0380.5690.1950.317
 潜伏期(ms, $\bar{x}±s$)252±110228±96206±656.620.0410.6450.1970.068
 扫视幅度(°, $\bar{x}±s$)9.4±3.513.9±1.614.5±1.918.21<0.0010.0030.359<0.001
), ArticleFig(id=1208106720224711125, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, language=EN, label=Tab.3, caption=

Behavioral and eye movement measures in clock-matching task of each group

, figureFileSmall=null, figureFileBig=null, tableContent=
指标帕金森病组AMC组YC组H/FP帕金森病组vs. AMC组*AMC组vs. YC组*帕金森病组vs. YC组*
时钟匹配任务
 准确率[%, M(Q1, Q3)]91.5(85.2, 94.9)96.7(91.8, 98.6)98.8(97.9,99.2)7.720.0410.2980.7630.205
 反应时间(ms, $\bar{x}±s$)2746±11852527±10211640±28546.44<0.0010.2470.0050.002
 扫视样本AOI次数($\bar{x}±s$)2.5±0.72.2±0.41.9±0.55.200.577–––
 扫视阵列AOIs次数($\bar{x}±s$)10.2±2.89.4±3.18.1±1.312.640.0380.0810.4530.062
 降效分数($\bar{x}±s$)1.5±0.31.4±0.21.3±0.25.320.633–––
倒转时钟匹配任务
 准确率(%, $\bar{x}±s$)76.7±12.180.2±12.485.7±8.94.210.352–––
 反应时间(ms, $\bar{x}±s$)4681±22124124±13832452±77635.96<0.0010.1090.008<0.001
 扫视样本AOI次数($\bar{x}±s$)5.4±1.23.2±0.92.9±0.710.290.0140.0110.143<0.001
 扫视阵列AOIs次数($\bar{x}±s$)18.8±3.611.5±2.49.2±2.710.610.0100.0230.547<0.001
 降效分数($\bar{x}±s$)2.1±0.41.8±0.31.5±0.412.350.0390.0170.4320.003
), ArticleFig(id=1208106720321180123, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208106716605026581, language=CN, label=表3, caption=

各组时钟匹配任务的行为和眼动指标

, figureFileSmall=null, figureFileBig=null, tableContent=
指标帕金森病组AMC组YC组H/FP帕金森病组vs. AMC组*AMC组vs. YC组*帕金森病组vs. YC组*
时钟匹配任务
 准确率[%, M(Q1, Q3)]91.5(85.2, 94.9)96.7(91.8, 98.6)98.8(97.9,99.2)7.720.0410.2980.7630.205
 反应时间(ms, $\bar{x}±s$)2746±11852527±10211640±28546.44<0.0010.2470.0050.002
 扫视样本AOI次数($\bar{x}±s$)2.5±0.72.2±0.41.9±0.55.200.577–––
 扫视阵列AOIs次数($\bar{x}±s$)10.2±2.89.4±3.18.1±1.312.640.0380.0810.4530.062
 降效分数($\bar{x}±s$)1.5±0.31.4±0.21.3±0.25.320.633–––
倒转时钟匹配任务
 准确率(%, $\bar{x}±s$)76.7±12.180.2±12.485.7±8.94.210.352–––
 反应时间(ms, $\bar{x}±s$)4681±22124124±13832452±77635.96<0.0010.1090.008<0.001
 扫视样本AOI次数($\bar{x}±s$)5.4±1.23.2±0.92.9±0.710.290.0140.0110.143<0.001
 扫视阵列AOIs次数($\bar{x}±s$)18.8±3.611.5±2.49.2±2.710.610.0100.0230.547<0.001
 降效分数($\bar{x}±s$)2.1±0.41.8±0.31.5±0.412.350.0390.0170.4320.003
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基于红外眼动系统探讨帕金森病多模式视觉探索障碍的发生机制
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杨旭 1 , 杨培红 2
解放军医学杂志 | 临床研究 2022,47(4): 382-389
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解放军医学杂志 | 临床研究 2022, 47(4): 382-389
基于红外眼动系统探讨帕金森病多模式视觉探索障碍的发生机制
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杨旭1, 杨培红2
作者信息
  • 1大连市友谊医院神经内科，辽宁大连 116001
  • 2大连市友谊医院影像科，辽宁大连 116001

    • 杨旭，医学硕士，副主任医师，主要从事神经退行性疾病方面的研究

Mechanism of multimodel visual exploration disorder in Parkinson's disease based on an infrared eye movement system
Xu Yang1, Pei-Hong Yang2
Affiliations
  • 1Department of Neurology, Dalian Friendship Hospital, Dalian, Liaoning 116001, China
  • 2Department of Medical Imaging, Dalian Friendship Hospital, Dalian, Liaoning 116001, China
出版时间: 2022-04-28 doi: 10.11855/j.issn.0577-7402.2022.04.0382
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摘要
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目的 通过红外眼动评估系统记录并分析目标探索任务中视觉信息处理系统眼动指标的疾病效应与衰老效应，探讨帕金森病患者视觉探索障碍的发生机制。方法 本研究为横断面研究。纳入2020年10月－2021年6月于大连市友谊医院运动障碍门诊临床确诊且正在使用多巴胺能药物的认知正常的帕金森病患者32例作为帕金森病组，另将本院体检中心招募的年龄、性别及受教育程度相匹配且认知正常的健康志愿者33例作为与帕金森病组年龄匹配的正常对照组(AMC组)，以及本院医护实习学生中招募的性别及受教育程度匹配的33例健康志愿者作为青年正常对照组(YC组)。所有受试者均进行代表视觉信息处理能力的图形匹配任务(时钟匹配任务与倒转时钟匹配任务)和代表动眼肌功能的扫视类任务，同时使用红外眼动评估系统记录各组受试者的行为和眼球运动指标。对扫视类任务的准确率、潜伏期和扫视幅度，以及时钟匹配类任务的准确率、反应时间、扫视样本图像感兴趣区域(AOI)次数、扫视阵列图像感兴趣区域(AOIs)次数和降效分数作为感兴趣眼动指标进行相关性分析；对帕金森病组的临床特征(疾病持续时间、抗帕金森病药物剂量和Hoehn-Yahr分级)与存在疾病效应的眼动指标进行相关性分析。结果 扫视类任务中，AMC组与YC组的各项指标比较差异均无统计学意义(P>0.05)；与帕金森病组的各项指标比较，AMC组(P=0.003)和YC组(P<0.001)在反向扫视任务中的扫视幅度均增高，差异有统计学意义。时钟匹配类任务中，与YC组比较，AMC组(时钟匹配任务：P=0.005；倒转时钟匹配任务：P=0.008)和帕金森病组(时钟匹配任务：P=0.002；倒转时钟匹配任务：P<0.001)的反应时间均明显延长，差异有统计学意义。与帕金森病组比较，AMC组及YC组在倒转时钟匹配任务中的访问样本图像AOI的扫视次数(AMC组：P=0.011；YC组：P<0.001)、访问阵列图像AOIs的扫视次数(AMC组：P=0.023；YC组：P<0.001)和降效分数(AMC组：P=0.017；YC组：P=0.003)减少，差异有统计学意义。时钟匹配类任务中其余各指标组间比较差异均无统计学意义(P>0.05)。反向扫视任务中的扫视幅度与倒转时钟匹配任务中访问样本图像AOI的扫视次数(r=–0.014，P=0.785)、访问阵列图像AOIs的扫视次数(r=–0.025，P=0.837)及降效分数(r=–0.031，P=0.576)均无明显相关性。帕金森病组的临床特征与反扫视任务的扫视幅度、倒转时钟匹配任务中访问样本图像AOI的扫视次数、访问阵列图像AOIs的扫视次数及降效分数均无相关性(P>0.05)。结论 基于红外眼动系统的结果提示，帕金森病患者的视觉探索障碍是由视觉信息处理功能失调和动眼肌功能障碍共同作用所致的，疾病效应和衰老效应对视觉探索过程存在不同性质的影响。

帕金森病  /  视觉探索  /  眼动  /  扫视  /  认知  /  衰老

Objective Record and analyze the disease effects and aging effects of eye movement indicators of visual information processing system in target exploration mission through an infrared eye-movement assessment system, and explore the pathogenesis of the visual exploration disorder in patients with Parkinson's disease (PD). Methods It is a cross-sectional study. A total of 32 patients with PD and normal cognition on dopaminergic drugs were recruited (PD group) from the Dyskinesia clinic of Dalian Friendship Hospital from October 2020 to June 2021; 33 age-, gender- and education-matched healthy volunteers with normal cognition were recruited (AMC group) from the medical center of our hospital, and 33 gender- and education-matched healthy young medical intern volunteers were recruited (YC group) from medical interns in our hospital during the same period. Behavioral and eye-movement indicators of all subjects were recorded with an infrared eye movement assessment system by testing to figure-matching tasks representing the visual information processing (clock-matching task and inverted clock-matching task) and saccade tasks representing the oculomotor function. The accuracy, saccade latency, and saccade size of saccade tasks, as well as the accuracy,the reaction time, the number of saccades visiting the sample area of interest (AOI), the number of saccades visiting array AOIs, and the de-efficiency score of clock matching tasks were analyzed. The PD group's clinical characteristics (disease duration, doses of anti-Parkinsonian medication, and Hoehn-Yahr grading) and eye movement indicators with disease effect were analyzed. Results In saccade tasks, there was no significant difference in all indicators between AMC group and YC group (P>0.05). Compared with the indicators of PD group, the saccade amplitude of anti-saccade task increased in AMC group (P=0.003) and the YC group (P<0.001)with statistically significant difference. In clock-matching tasks, compared with the YC group, the reaction time of the AMC group(clock-matching task: P=0.005; reverse clock-matching task: P=0.008) and PD group (clock-matching task: P=0.002; reverse clock-matching task: P<0.001) was significantly prolonged with statistically significant difference. Compared with the PD group, the saccade numbers of visiting sample AOI (AMC group: P=0.011; YC group: P<0.001), the saccade numbers of visiting array AOIs(AMC group: P=0.023; YC group: P<0.001) and the de-efficiency score (AMC group: P=0.017; YC group: P=0.003) decreased with statistically significant differences. No statistically significant difference existed in another indicators among each groups in clock matching tasks (P>0.05). There was no obvious correlation in saccade amplitude of anti-saccade task to the numbers of saccade visiting sample AOI (r=–0.014, P=0.785), the numbers of saccade visiting array AOIs (r=–0.025, P=0.837) and de-efficiency score(r=–0.031, P=0.576) in the reverse clock-matching task. None obvious correlation of the clinical characteristics of PD group to the saccade amplitude in anti-saccade task, the numbers of saccade visiting the sample AOI, the numbers of saccade visiting array AOIs,and de-efficiency score in the inverted clock-matching task (P>0.05). Conclusion The results based on the infrared eye movement system showed that the visual exploration disorder of PD patients may be due to the combined action of visual information processing dysfunction and oculomotor dysfunction; disease effect and aging effect have different influences on the process of visual exploration.

Parkinson's disease  /  visual exploration  /  eye movements  /  saccade  /  cognition  /  aging
杨旭, 杨培红. 基于红外眼动系统探讨帕金森病多模式视觉探索障碍的发生机制. 解放军医学杂志, 2022 , 47 (4) : 382 -389 . DOI: 10.11855/j.issn.0577-7402.2022.04.0382
Xu Yang, Pei-Hong Yang. Mechanism of multimodel visual exploration disorder in Parkinson's disease based on an infrared eye movement system[J]. Medical Journal of Chinese People’s Liberation Army, 2022 , 47 (4) : 382 -389 . DOI: 10.11855/j.issn.0577-7402.2022.04.0382
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帕金森病是常见于中老年人的进行性神经系统变性疾病，主要表现为静止性震颤、运动迟缓、肌强直和姿势平衡障碍等运动症状。近年来，包括睡眠障碍、精神症状、自主神经功能障碍和认知障碍等非运动症状以其多样性和对患者生活质量的影响而受到关注[1-2]。视觉识别能力减退[3]和人眼不能正确识别物体[4]被认为是帕金森病的重要先发症状。临床上，帕金森病患者的视觉识别能力下降曾被认为是动眼肌功能障碍所致[5]，且得到Matsumoto等[6]的研究结果支持，即帕金森病患者在视觉探索过程中的扫视幅度小于年龄匹配的对照组。然而，近期的神经心理学研究显示，帕金森病患者包括视觉工作记忆[7]和视觉空间感知准确度[8]在内的视觉信息处理能力明显降低，提示帕金森病视觉识别能力下降不仅受动眼肌功能的影响，还可能与视觉信息处理功能障碍有关，但目前尚无定论。基于计算机接口的红外眼动评估系统通过以连续方式捕获眼球运动轨迹的技术对个体在任务中的眼球运动过程进行瞳孔位置的识别与记录，现已应用于多种认知任务的探索性眼动研究中，并在认知神经科学[9]和神经科学[10]领域提出了视觉信息处理的重要概念。本研究通过红外眼动评估系统记录受试者在执行用于评估视觉信息处理能力的图形匹配类任务[10]和用于评估动眼肌功能的扫视类任务[11]时的眼动轨迹，以探讨疾病效应与衰老效应对帕金森病视觉探索障碍的影响，旨在为进一步明确帕金森病视觉探索障碍的病理机制提供依据。
1 资料与方法
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1.1 研究对象
本研究为横断面研究。纳入2020年10月－2021年6月在大连市友谊医院神经内科运动障碍门诊根据英国脑库帕金森病诊断标准[12]临床确诊且正在使用抗帕金森病药物至少2个月并从中获益的帕金森病患者32例，入组者年龄均>60岁，Hoehn-Yahr分级[13]0~3级。同期于本院体检中心招募年龄>60岁，性别及受教育程度相匹配且认知正常的健康志愿者33例作为年龄匹配正常对照(healthy age-matched controls，AMC)组，以及本院医护实习学生中招募的33例年龄<30岁且性别及受教育程度匹配的青年志愿者作为年轻正常对照(healthy young controls，YC)组。排除标准：(1)存在其他神经精神疾病或内科系统疾病且病情不稳定；(2)存在严重头部损伤病史和(或)酒精及药物滥用史；(3)存在严重视力、听力及言语功能障碍或肢体残障者；(4)年龄>80岁；(5)存在认知障碍。认知障碍定义为蒙特利尔认知评估量表[14](Montreal cognitive assessment，MoCA)评分<26分。试验期间，所有帕金森病患者均按照既往剂量使用抗帕金森病药物。本研究严格遵守2013版《赫尔辛基宣言》，已获大连市友谊医院伦理委员会批准(YY-LL-2020-0825)。所有受试者在自愿参与本研究前均签署书面知情同意书。
1.2 方法
试验在大连市友谊医院进行。使用由红外视频眼罩和OTOsuite Vestibular软件集成的ICS Impulse系统(Otometrics公司，丹麦)进行记录和分析。每位受试者需依次执行两类共四项任务：朝向扫视任务和反向扫视任务，时钟匹配任务和倒转时钟匹配任务。扫视类任务可有效评估动眼肌的控制能力，测量指标包括准确率、潜伏期和扫视幅度，试验数据由OTOsuite Vestibular软件实时计算。时钟匹配类任务是由Archibald等[10]提出的新范式，实现了对视觉探索功能的客观评价，测量指标包括准确率、反应时间、扫视样本图像感兴趣区域(area of interest，AOI)次数、扫视阵列图像AOIs次数和降效分数。扫视次数由OTOsuite Vestibular软件实时计算，准确率、反应时间与降效分数由研究人员计算。受试者距投影墙1 m处舒适坐位，保证眼部与投影墙红色准星水平对齐，使投影墙上2 cm位移大约对应1°视野。视觉刺激显示于投影墙上。试验开始前受试者需戴好红外视频眼罩并进行校准以保证十字线准确跟踪右眼瞳孔。每项试验结束后提供1 min休息时间，试验总时长约30 min。室内环境安静、舒适，光线柔和，室温23~25 ℃。试验开始前向受试者说明试验方法及步骤，并确保受试者准确理解和执行任务。
1.2.1 朝向扫视任务与反向扫视任务
进行朝向扫视任务时，刺激靶点(激光点)从视频眼罩投射于投影墙，在十字准星水平的左侧或右侧7.5°~15.0°位置随机出现，保持可见1000 ms，人眼需尽可能快速、准确地跟随并注视靶目标，整个过程中头部需保持不动。反向扫视任务的视觉演示过程与朝向扫视任务相同，但受试者需要尽可能快速、准确地注视靶目标的镜像位置。2项扫视任务的时间均为30 s，即靶目标随机出现30次。准确率定义为结果正确次数除以试验总次数；潜伏期定义为目标出现到扫视起始的时间差；扫视幅度定义为眼跳起始点与偏移点之间的距离。
1.2.2 时钟匹配任务与倒转时钟匹配任务
时钟匹配类任务参照Kaneko等[15]的试验模式。进行时钟匹配任务(图1A)时，以投影墙上十字准星为中心，1个样本时钟图像和包含不同指针方向的4个时钟图像(作为刺激阵列)同时出现，样本图像居中，4个刺激图像随机居于两侧，左右各2个，间距一致。各时钟图像直径均为15 cm，间距6 cm。刺激阵列包含1个与样本时钟图像的指针方向完全相同的目标图像和3个非目标图像，4个刺激时钟图像按照左至右的顺序从1－4编号，标识于图像正下方。受试者需从刺激阵列中尽量快速、正确地找出目标图像并提供目标图像编号。倒转时钟匹配任务(图1B)的视觉演示过程与时钟匹配任务相同，但刺激阵列的4个时钟图像为倒置出现。两项时钟匹配任务各重复6次，每次样本时钟图像指针位置随机。试验开始前需确认受试者能够正确识别时钟图像并理解任务要求。时钟图像的感兴趣区域(AOI)定义为：样本图像AOI是指以时钟图像为中心的圆外切正方形(15 cm×15 cm)区域；阵列图像AOIs是指以时钟图像为中心的圆外切正方形(15 cm×15 cm)及与正方形同宽度的数字编号区域，即4个宽15 cm×高20 cm的矩形(图1A)。对正确和错误AOI的注视分布，视觉探索过程中对不同区域的访问次数、准确率和反应时间揭示了受试者完成视觉任务的策略和效能。因此，本研究选择准确率、反应时间、访问样本图像AOI的扫视次数、访问阵列图像AOIs的扫视次数、降效分数[10]5个指标来评估视觉探索策略。其中，准确率定义为结果正确次数除以试验总次数；反应时间定义为时钟图像出现到答案出现的时间，以研究者按下计时按键的时间计算。由于不同个体按键行为的反应和执行时间可能存在较大差异，本研究由同一位研究者执行按键步骤以减少误差。根据眼球落入区域计算访问样本图像AOI扫视次数、访问各阵列图像AOIs扫视次数和访问阵列图像AOIs的总扫视次数。降效分数定义为访问3个错误AOI的总次数除以访问正确AOI的总次数。低降效分数反映了优先探索正确区域和较少访问不正确区域即可完成任务的高效策略；高降效分数则反映了重复访问不正确区域的低效策略。
1.3 指标分析
对各组受试者扫视类任务的准确率、潜伏期和扫视幅度，以及时钟匹配类任务的准确率、反应时间、扫视样本图像AOI次数、扫视阵列图像AOIs次数和降效分数作为感兴趣指标进行分析；AMC组与帕金森病组的眼动指标比较以评估视觉探索过程中的疾病效应；AMC组与YC组的眼动指标比较以评估衰老效应[16]。对帕金森病组的临床特征(疾病持续时间、抗帕金森病药物剂量和Hoehn-Yahr分级)与存在疾病效应的眼动指标进行相关性分析。
1.4 统计学处理
采用SPSS 22.0软件进行统计分析。数据分布采用Shapiro-Wilk法进行正态性检验，正态分布的计量资料以$\bar{x}±s$表示，方差齐时多组间比较采用单因素方差分析，进一步两两比较采用Bonferroni检验；非正态分布则采用M(Q1，Q3)表示，组间比较采用Kruskal-Wallis非参数检验；计数资料以例(%)表示，组间比较采用χ2检验。对存在疾病效应的眼动指标采用Pearson相关系数进行相关性分析。P<0.05为差异有统计学意义。
2 结果
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2.1 人口学资料及临床特征
帕金森病组患者的年龄为(65.9±7.4)岁，帕金森病病程为(48.5±19.7)个月；对帕金森病组患者采用帕金森病综合评分量表(unified Parkinson's disease rating scale，UPDRS)[13]第Ⅲ部分评测运动功能；使用标准方法[17]计算抗帕金森病药物的左旋多巴当量日剂量(daily dosage of L-dopa-equivalents，LEDD)。AMC组年龄为(68.5±8.6)岁，YC组年龄为(24.3±3.2)岁。帕金森病组、AMC组受试者的年龄均明显高于YC组(P<0.001)，但帕金森病组与AMC组间差异无统计学意义(P=0.749)。三组受试者的MoCA评分均匹配(P=0.167)，且性别(P=0.612)及受教育程度(P=0.084)差异无统计学意义，具有可比性。各组人口学资料及临床特征详见表1。
2.2 扫视任务的眼动数据比较
在朝向扫视任务和反向扫视任务中，AMC组与YC组的各项指标比较差异均无统计学意义(P>0.05)。与帕金森病组比较，AMC组(P=0.003)和YC组(P<0.001)在反向扫视任务中的扫视幅度均增高，差异有统计学意义，其余各指标组间比较差异无统计学意义(P>0.05)(表2)。
2.3 时钟匹配任务的眼动数据比较
在时钟匹配类任务中，与YC组比较，AMC组(时钟匹配任务：P=0.005；倒转时钟匹配任务：P=0.008)和帕金森病组(时钟匹配任务：P=0.002；倒转时钟匹配任务：P<0.001)的反应时间均明显延长，差异有统计学意义；而AMC组与帕金森病组比较差异无统计学意义。与帕金森病组比较，AMC组和YC组在倒转时钟匹配任务中的访问样本图像AOI扫视次数(AMC组：P=0.011；YC组：P<0.001)、访问阵列图像AOIs扫视次数(AMC组：P=0.023；YC组：P<0.001)和降效分数(AMC组：P=0.017；YC组：P=0.003)均明显减少，差异有统计学意义。其余各指标组间比较差异均无统计学意义(P>0.05)(表3)。
2.4 动眼肌眼动指标与视觉眼动指标的相关性
对存在疾病效应的眼动指标(反向扫视任务的扫视幅度与倒转时钟匹配任务的扫视次数及降效分数)进行相关性分析，结果显示，反向扫视任务中的扫视幅度与倒转时钟匹配任务中访问样本图像AOI扫视次数(r=–0.014，P=0.785)、访问阵列图像AOIs扫视次数(r=–0.025，P=0.837)及降效分数(r=–0.031，P=0.576)均无相关性。
2.5 临床特征与眼动指标的相关性
帕金森病组的临床特征(包括疾病持续时间、抗帕金森病药物剂量和Hoehn-Yahr分级)与存在疾病效应的眼动指标均无相关性。其中，疾病持续时间与反向扫视任务的扫视幅度(r=–0.093，P=0.345)及倒转时钟匹配任务中的访问样本图像AOI扫视次数(r=0.087，P=0.554)、访问阵列图像AOIs扫视次数(r=0.075，P=0.632)、降效分数(r=0.124，P=0.235)均无相关性；药物剂量与反向扫视任务的扫视幅度(r=0.105，P=0.674)及倒转时钟匹配任务中的访问样本图像AOI扫视次数(r=–0.133，P=0.219)、访问阵列图像AOIs扫视次数(r=–0.098，P=0.512)、降效分数(r=–0.079，P=0.651)均无相关性；Hoehn-Yahr分级与反向扫视任务的扫视幅度(r=–0.096，P=0.313)及倒转时钟匹配任务中的访问样本图像AOI扫视次数(r=0.071，P=0.683)、访问阵列图像AOIs扫视次数(r=0.094，P=0.356)、降效分数(r=0.057，P=0.802)也均无相关性。
3 讨论
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本研究通过分析视觉探索过程中感兴趣眼动指标的疾病效应与衰老效应，探讨了帕金森病视觉探索障碍的发生机制。
3.1 衰老效应的影响
无论在朝向还是反向扫视任务中，本研究均未观察到衰老效应，提示扫视能力不会随着年龄增长而改变，这与Bialystok等[18]的研究结果一致，但Fernandez-Ruiz等[19]则认为在朝向扫视和反向扫视任务中均存在衰老效应。这种差异可能与研究中使用了不同的任务范式、认知异质性及参与者的纳入和排除标准不同有关。而时钟匹配任务和倒转时钟匹配任务中仅反应时间存在衰老效应，则可能与正常的老龄化过程中神经-肌肉活动减慢有关。
3.2 疾病效应的影响
疾病效应对扫视任务的影响仅与反向扫视任务的扫视幅度有关，表现为帕金森病患者扫视幅度降低，但朝向扫视任务中未发现疾病效应的证据。这种差异可能是由于任务复杂程度或任务所需的功能域不同所致，即反向扫视任务作为记忆介导的扫视活动比朝向扫视任务需要更复杂的认知资源。帕金森病早期的病理改变主要累及黑质和纹状体区，由于反向扫视引发的自发性扫视活动发生于额叶-基底节-上丘通路，因此可出现部分性自发扫视能力受损；而朝向扫视任务引发的反射性扫视活动是经顶叶皮质直接投射至上丘中间区域的扫视相关脑区，在疾病早期尚未受累，故朝向扫视任务时动眼肌能力得以保留。
本研究发现，倒转时钟匹配任务中，访问样本AOI扫视次数和访问阵列AOIs扫视次数及降效分数均存在疾病效应，表现为帕金森病组扫视样本图像AOI次数和扫视阵列图像AOIs次数及降效分数均高于AMC组和YC组；而时钟匹配任务的各项眼动指标均未发现疾病效应证据。鉴于倒转时钟匹配任务需要受试者将刺激目标转换为旋转180°的心理图像，相当于引入了额外的空间成分，故在2个结构相似但认知复杂程度不同的任务中，这种差异可能和与帕金森病病理机制有关的认知功能改变存在潜在的关系，即认知正常的帕金森病患者的扫视行为异常可能是预测其认知损害的指标，可对已经存在的细微但无法通过认知筛查发现的视觉认知、执行功能或注意力受损进行早期识别，但尚需进一步验证。
本研究还发现，反向扫视任务的扫视幅度与倒转时钟匹配任务中存在疾病效应的3个指标(访问样本图像AOI扫视次数、访问阵列图像AOIs扫视次数及降效分数)均无相关性，提示倒转时钟匹配任务中表现出的疾病效应并不能用动眼肌功能障碍来解释。在倒转时钟匹配任务中，帕金森病组访问样本AOI的扫视次数、访问阵列AOIs的扫视次数及降效分数均明显高于AMC组和YC组，说明帕金森病患者在高认知负荷条件下采取了效率较低的探索策略，即多次重复访问不正确区域，故而需要进行更多的探索性眼球运动才能够做出决策以完成任务。在要求对多个对象进行识别的任务中，将刺激阵列的新信息与作为模板的样本信息进行比较，需要在工作记忆中恰当地保存模板信息，因此工作记忆系统需要被激活。当受试者不能有效保存和维持样本信息和刺激信息的视觉图像时，将导致完成任务的效率降低，即访问样本图像AOI和阵列图像AOIs的扫视次数增加及重复地访问不正确信息。因此，倒转时钟匹配任务中表现的疾病效应提示帕金森病患者完成任务的低效性与工作记忆和信息处理能力障碍有关，这也支持了Grogan等[20]提出的帕金森病患者视觉工作记忆功能受损的观点。而在时钟匹配任务中未发现疾病效应的原因则可能是由于其对工作记忆的需求较少。
尽管存在实验设备、试验范式及检测指标的不同，但本研究结果与Nagai等[16]的研究结果基本一致，即帕金森病患者的动眼肌功能和视觉信息处理功能均受损，而差异仅在于数据分布的不同。Nagai等[16]发现，朝向扫视任务与时钟匹配任务的各项指标均呈偏态分布，而本研究中仅朝向扫视任务与时钟匹配任务的准确率呈负偏态分布，其余指标均呈正态分布。这既可能是更多数量的受试者(不论组别)在低认知需求下可以更准确完成任务的直观证据，也可能是由于样本量相对较少所致。因此，本研究认为，眼动行为具有客观性、稳定性和可重复性，不易受到其他因素的干扰。
3.3 帕金森病患者的视觉探索障碍
本研究中，时钟匹配类任务的眼动指标存在疾病效应和衰老效应的双重证据，而扫视类任务的眼动指标仅存在疾病效应证据，但两类任务中存在疾病效应的指标间无相关性，说明帕金森病视觉探索障碍是视觉信息处理功能失调和动眼肌功能障碍共同作用所致，疾病效应和衰老效应可能对视觉探索过程产生不同性质的影响。尽管在两类任务中存在扫视幅度、扫视次数及探索策略的疾病效应，但准确率的差异未发现疾病效应，表明认知正常的帕金森病患者尽管可能已经存在不完全性执行功能、记忆、视觉空间或视觉感知缺陷[21]，但尚可通过对任务过度学习的代偿机制以保证准确率。但随着病情进展，则可能表现出记忆、注意和执行能力等方面的差异，在视觉空间和视觉感知任务上的错误率也更高[10]。这种随病程延长而显示出的差异可能与帕金森病Braak病理分期[22]有关，由于多巴胺能神经元进行性缺失使黑质网状部γ-氨基丁酸能神经纤维对上丘的抑制作用减弱，皮质及皮质下眼动控制网络损伤导致个体在执行自主扫视意图时，需要在每个位置花费更长时间注视目标来提取足够的视觉信息，间接引起了扫视时间减少和扫视幅度下降，表现为多个短暂低振幅扫视集合，即本研究中扫视次数增多和扫视幅度下降的结果。而由于病程处于Braak病理第3或4期，新皮质功能尚未受累，故可通过更多次数的反复扫视行为纠正在视觉任务中的错误倾向。而病情进展至Braak病理第5或第6期时，新皮质进行性广泛受累，认知受损，精神行为异常等症状将逐渐出现并进行性加重。
人眼通过扫视活动以目标导向的方式将靶目标反射的光线投射至视网膜中央凹，以便迅速和准确地理解视觉环境。精确的空间扫视行为受到额叶眼域、辅助眼域、顶叶眼域，以及前额叶和后顶叶皮质区域的影响，可将视觉信息传递至进行视觉感知和视觉空间处理的高级视觉中心，再通过上丘、丘脑和基底神经节投射到与眼球扫视运动有关的脑干下部区域[23]。当帕金森病病理改变累及这些区域时，患者将逐渐出现视觉空间、视觉感知、执行功能，以及注意和记忆领域的损伤。由于视觉探索过程中扫视行为和视觉空间输入与运动输出的整合是在相邻皮质区域进行的，有效视觉探索策略中断可能导致运动并发症，如视觉诱导的步态冻结、转向困难和跌倒。有研究证实，转向不但涉及眼球运动和头部运动的复杂整合，还包括躯干旋转和步态的共同协作[24]，老年人跌倒的风险与水平扫视起始和抬脚行为之间的延迟有关[25]。步态冻结通常也是由于转向困难所致，进而引起侧倾摔倒[26]。早期帕金森病患者已经存在扫视行为起始及控制障碍，因而在静态条件下，扫视活动可作为即时转向行为的预测指标[27]。在更复杂的自然条件下，如在认知受到干扰时的行走和转向，帕金森病患者在转向前进行早期“有效预备”的扫视次数将明显减少，这种差异与认知能力下降呈正相关[28]。本研究中帕金森病组扫视幅度、扫视次数和探索效率的变化与上述结果一致，因此可能对早期预测帕金森病的运动并发症风险具有重要意义。未来可考虑采用包括在行走过程中使用便携式眼球跟踪设备等“动态”方式对视觉探索的“静态”参数进行评估以验证这一假设。
3.4 局限性
本研究存在以下局限性：(1)样本量相对较少，未来可扩大样本量进一步验证结果。(2)帕金森病组患者均正在接受抗帕金森药物治疗，这些药物可能通过兴奋多巴胺能系统或抑制胆碱能系统影响个体的运动和认知功能[29]。尽管研究中左旋多巴当量日剂量与眼动指标间不存在相关性，但并不能完全排除抗帕金森药物的影响，如服药与试验之间的间隔时间不同对眼球运动的潜在影响。下一步应考虑设置未服用药物的帕金森病组进行对照。(3)鉴于客观条件限制，本研究仅设置了帕金森病组(年龄>60岁)、AMC组及YC组，如能增加青中年帕金森病组，通过析因设计分析疾病效应、衰老效应以及二者间的交互作用，将能更好地保证试验结果的全面性与均衡性。(4)未对帕金森病认知功能与眼动特征的连续变化进行纵向观察。未来可进行前瞻性队列研究，纵向监测视觉探索参数及扫视参数，这也可能是评估新型抗帕金森病药物反应的新方法。
综上所述，本研究以视觉、认知和动眼肌功能的共定位效应为基础，对视觉探索任务中动眼肌功能和视觉信息处理过程进行分析后发现，帕金森病病理改变不但可以影响动眼肌功能，还可导致利用心理图像进行视觉信息加工的过程受损；帕金森病患者的视觉探索障碍是由视觉信息处理功能失调和动眼肌功能障碍共同作用引起的，疾病效应和衰老效应对视觉探索过程存在不同性质的影响。本研究还为使用非语言方式即通过对神经或精神疾病患者联合应用时钟匹配类任务和扫视类任务比较视觉探索策略和眼动肌参数以探讨中枢神经系统疾病的病理生理学机制提供了新思路。
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2022年第47卷第4期
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doi: 10.11855/j.issn.0577-7402.2022.04.0382
  • 接收时间：2021-11-03
  • 首发时间：2025-12-17
  • 出版时间：2022-04-28
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  • 收稿日期：2021-11-03
  • 录用日期：2021-12-03
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    1大连市友谊医院神经内科，辽宁大连 116001
    2大连市友谊医院影像科，辽宁大连 116001
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