Functional Consequences of Oculomotor Disorders in Hereditary Cerebellar Ataxias

Abstract

Saccadic eye movements are traditionally cited as an especially successful combination of accuracy and velocity, such high level of performances being believed to be crucial for optimal vision. Although the structures subtending these properties are now well recognized, very little is known about the functional consequences on visually guided behaviors of reduced saccade performances, i.e., slowness and/or inaccuracy. We therefore investigated the impact of such impairments in patients with spino-cerebellar and Friedreich ataxia, i.e., diseases known to affect both saccade parameters. Subjects performed a classical eye movement task, in order to quantify saccade inaccuracy and/or slowness, a visually search task and a reading task and completed a questionnaire designed to evaluate their perceived visual discomfort in daily activities. The first main result was that saccade impairments did have an impact on visually guided behaviors, resulting in an increased time for target detection, especially when accurate foveation was needed, and in an increased reading time. The main responsible oculomotor factor was increased variability of saccade accuracy, and the least responsible factor was reduced saccade velocity. The second main result was that saccade disorders did not induce significant subjective discomfort, since no correlations were found between the results of the questionnaire and saccade parameters. These results emphasize the functional impact of increased variable error of saccade accuracy and question the rationale of high saccade velocities. The discrepancy between objective and subjective measures underlines the largely unconscious aspect of saccade control and leads us to consider the need for an adapted therapy.

A simple saccadic reading test to assess ocular motor function in cerebellar ataxia

“…Poor eye movement control can cause eye and mental fatigue that worsens later in the day (unpublished observation) and leads to impaired activities of daily living such as reading, resulting in worse quality of life [ 6 , 29 , 46 – 50 ]. Therefore, it is not surprising that patients with cerebellar ataxia have difficulty with reading [ 31 , 36 ]. Because improved reading has been reported as the number one goal or complaint in patients with vision difficulties [ 51 – 53 ], assessment of reading should be more routinely performed in the clinical setting.…”

“…To read and survey the visual surrounding, human beings make about 250,000 eye movements per day, rapidly jumping from target to target, and each time placing gaze on the fovea, the part of the retina with the highest resolution [ 21 , 26 – 28 ]. Reflexive saccade and static fixation paradigms are traditionally used in infrared oculography studies to quantify saccade and fixation abnormalities in patients with cerebellar ataxia [ 25 , 29 – 31 ]. However, these relatively simplified tests do not simulate the pattern of eye movement during functional tasks such as reading, which requires complex coordination of multiple parts of the brain to perform rapid, alternating saccades and fixations along each line of reading followed by line-changing saccades [ 21 ].…”

“…In order to perform such an ocular motor task well, the cerebellum optimizes saccadic and fixational behavior in sequence and integrates information from each saccade to plan the next one [ 21 , 32 – 35 ]. This means patients with difficulty with eye movement control due to cerebellar ataxia may have particularly striking difficulties with reading, which is a reliable predictor for assessment of visual acuity, although this is not routinely measured in the clinical setting [ 31 , 36 ].…”

Ocular motor disorders

“…From a more functional perspective, impaired visual detection time and difficulty reading are correlated with abnormalities of saccadic function in patients with SCA1, SCA3, and Friedreich's ataxia despite relatively little by way of subjective symptoms referable to the disordered eye movements [37].…”

Top-Down but Not Bottom-Up Visual Scanning is Affected in Hereditary Pure Cerebellar Ataxia

“…Previous studies of humans and animals with cerebellar damage have found impairment in visual search and suggested that the top-down attentional processes may be disturbed while bottom-up attentional processes are not [34] – [36] . However, these studies are controversial regarding the involvement of oculomotor movement [36] , [37] . Moreover, these previous eye-tracking studies did not formally differentiate between serial and pop-out tasks.…”