Brandon Oubre, Faye Yang, Anna C Luddy, Rohin Manohar, Nancy N Soja, Christopher D Stephen, Jeremy D Schmahmann, Divya Kulkarni, Lawrence White, Siddharth Patel, Anoopum S Gupta
{"title":"阅读段落时的眼动跟踪可支持对共济失调患者进行精确的眼球运动评估。","authors":"Brandon Oubre, Faye Yang, Anna C Luddy, Rohin Manohar, Nancy N Soja, Christopher D Stephen, Jeremy D Schmahmann, Divya Kulkarni, Lawrence White, Siddharth Patel, Anoopum S Gupta","doi":"10.1101/2025.01.13.25320487","DOIUrl":null,"url":null,"abstract":"<p><p>Abnormal eye movements occur early in the course of disease in many ataxias. However, clinical assessments of oculomotor function lack precision, limiting sensitivity for measuring progression and the ability to detect subtle early signs. Quantitative assessment of eye movements during everyday behaviors such as reading has potential to overcome these limitations and produce functionally relevant measures. In this study, we analyze eye movements in individuals with ataxia during passage reading. Binocular gaze sampled at 1000 Hz was collected from 102 individuals with ataxia diagnoses (including 36 spinocerebellar ataxias, 12 Friedreich's ataxia, and 5 multiple system atrophy among other conditions) and 70 healthy controls participating in the Neurobooth study. Longitudinal data were available for 26 participants with ataxia. Saccades were categorized as progressive (rightward) saccades, regressive saccades, or sweeps (large displacement saccades primarily generated when scanning to the beginning of the next line) based on their direction and displacement. Saccade and fixation kinematics were summarized using 28 statistical features. A linear model was trained to estimate clinician-performed ataxia rating scale scores. Model scores were reliable (ICC=0.96, p<0.001) and demonstrated convergent validity with Brief Ataxia Rating Scale total (r=0.82, p<0.001), oculomotor (r=0.52, p<0.001), and speech (r=0.73, p<0.001) scores, as well as patient surveys. The scores were also sensitive to disease progression (d=0.36, p=0.03), demonstrated strong separability between healthy controls and participants with ataxias (AUC=0.89, p<0.001), and showed evidence of the ability to detect subclinical oculomotor patterns (AUC=0.69, p=0.02). Several kinematic saccade and fixation features demonstrated strong differences across disease severity groups. Notable features included the mean angular displacement of fixations (<i>η</i> <sup>2</sup>=0.44, p<0.001), the number (<i>η</i> <sup>2</sup>=0.27, p<0.001) and frequency of saccades (<i>η</i> <sup>2</sup>=0.25, p<0.001), and the proportion of regressive saccades (<i>η</i> <sup>2</sup>=0.11, p<0.001). Quantitative assessment of eye movements during passage reading were highly informative of ataxia severity, were sensitive to disease progression, and enabled detection of subclinical signs. These properties support the inclusion of video-oculography-based measures of reading in natural history studies and clinical trials. Furthermore, this study demonstrates the feasibility of integration of oculomotor assessments in clinical workflows.</p>","PeriodicalId":94281,"journal":{"name":"medRxiv : the preprint server for health sciences","volume":" ","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2025-01-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11759587/pdf/","citationCount":"0","resultStr":"{\"title\":\"Eye Tracking during Passage Reading Supports Precise Oculomotor Assessment in Ataxias.\",\"authors\":\"Brandon Oubre, Faye Yang, Anna C Luddy, Rohin Manohar, Nancy N Soja, Christopher D Stephen, Jeremy D Schmahmann, Divya Kulkarni, Lawrence White, Siddharth Patel, Anoopum S Gupta\",\"doi\":\"10.1101/2025.01.13.25320487\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Abnormal eye movements occur early in the course of disease in many ataxias. However, clinical assessments of oculomotor function lack precision, limiting sensitivity for measuring progression and the ability to detect subtle early signs. Quantitative assessment of eye movements during everyday behaviors such as reading has potential to overcome these limitations and produce functionally relevant measures. In this study, we analyze eye movements in individuals with ataxia during passage reading. Binocular gaze sampled at 1000 Hz was collected from 102 individuals with ataxia diagnoses (including 36 spinocerebellar ataxias, 12 Friedreich's ataxia, and 5 multiple system atrophy among other conditions) and 70 healthy controls participating in the Neurobooth study. Longitudinal data were available for 26 participants with ataxia. Saccades were categorized as progressive (rightward) saccades, regressive saccades, or sweeps (large displacement saccades primarily generated when scanning to the beginning of the next line) based on their direction and displacement. Saccade and fixation kinematics were summarized using 28 statistical features. A linear model was trained to estimate clinician-performed ataxia rating scale scores. Model scores were reliable (ICC=0.96, p<0.001) and demonstrated convergent validity with Brief Ataxia Rating Scale total (r=0.82, p<0.001), oculomotor (r=0.52, p<0.001), and speech (r=0.73, p<0.001) scores, as well as patient surveys. The scores were also sensitive to disease progression (d=0.36, p=0.03), demonstrated strong separability between healthy controls and participants with ataxias (AUC=0.89, p<0.001), and showed evidence of the ability to detect subclinical oculomotor patterns (AUC=0.69, p=0.02). Several kinematic saccade and fixation features demonstrated strong differences across disease severity groups. 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Eye Tracking during Passage Reading Supports Precise Oculomotor Assessment in Ataxias.
Abnormal eye movements occur early in the course of disease in many ataxias. However, clinical assessments of oculomotor function lack precision, limiting sensitivity for measuring progression and the ability to detect subtle early signs. Quantitative assessment of eye movements during everyday behaviors such as reading has potential to overcome these limitations and produce functionally relevant measures. In this study, we analyze eye movements in individuals with ataxia during passage reading. Binocular gaze sampled at 1000 Hz was collected from 102 individuals with ataxia diagnoses (including 36 spinocerebellar ataxias, 12 Friedreich's ataxia, and 5 multiple system atrophy among other conditions) and 70 healthy controls participating in the Neurobooth study. Longitudinal data were available for 26 participants with ataxia. Saccades were categorized as progressive (rightward) saccades, regressive saccades, or sweeps (large displacement saccades primarily generated when scanning to the beginning of the next line) based on their direction and displacement. Saccade and fixation kinematics were summarized using 28 statistical features. A linear model was trained to estimate clinician-performed ataxia rating scale scores. Model scores were reliable (ICC=0.96, p<0.001) and demonstrated convergent validity with Brief Ataxia Rating Scale total (r=0.82, p<0.001), oculomotor (r=0.52, p<0.001), and speech (r=0.73, p<0.001) scores, as well as patient surveys. The scores were also sensitive to disease progression (d=0.36, p=0.03), demonstrated strong separability between healthy controls and participants with ataxias (AUC=0.89, p<0.001), and showed evidence of the ability to detect subclinical oculomotor patterns (AUC=0.69, p=0.02). Several kinematic saccade and fixation features demonstrated strong differences across disease severity groups. Notable features included the mean angular displacement of fixations (η2=0.44, p<0.001), the number (η2=0.27, p<0.001) and frequency of saccades (η2=0.25, p<0.001), and the proportion of regressive saccades (η2=0.11, p<0.001). Quantitative assessment of eye movements during passage reading were highly informative of ataxia severity, were sensitive to disease progression, and enabled detection of subclinical signs. These properties support the inclusion of video-oculography-based measures of reading in natural history studies and clinical trials. Furthermore, this study demonstrates the feasibility of integration of oculomotor assessments in clinical workflows.