Alterations of Eye Movement Control in Neurodegenerative Movement Disorders

Abstract

The evolution of the fovea centralis, the most central part of the retina and the area of the highest visual accuracy, requires humans to shift their gaze rapidly (saccades) to bring some object of interest within the visual field onto the fovea. In addition, humans are equipped with the ability to rotate the eye ball continuously in a highly predicting manner (smooth pursuit) to hold a moving target steadily upon the retina. The functional deficits in neurodegenerative movement disorders (e.g., Parkinsonian syndromes) involve the basal ganglia that are critical in all aspects of movement control. Moreover, neocortical structures, the cerebellum, and the midbrain may become affected by the pathological process. A broad spectrum of eye movement alterations may result, comprising smooth pursuit disturbance (e.g., interrupting saccades), saccadic dysfunction (e.g., hypometric saccades), and abnormal attempted fixation (e.g., pathological nystagmus and square wave jerks). On clinical grounds, videooculography is a sensitive noninvasive in vivo technique to classify oculomotion function alterations. Eye movements are a valuable window into the integrity of central nervous system structures and their changes in defined neurodegenerative conditions, that is, the oculomotor nuclei in the brainstem together with their directly activating supranuclear centers and the basal ganglia as well as cortical areas of higher cognitive control of attention.

Patterns of Eye Movement Impairment Correlate with Regional Brain Atrophy in Neurodegenerative Parkinsonism

“…The observed oculomotor disturbances in PD ( n = 39), PSP ( n = 32), and MSA ( n = 18) patients were consistent with the findings reported in previous studies [2,5]. ANOVA indicated severely disturbed eye movements in PD, MSA, and PSP patients compared to controls ( p < 0.0001); the statistics of all of the investigated oculomotor parameters are listed in Table 2.…”

“…Both PSP and MSA patients showed a characteristic pattern of “saccadized” smooth pursuit [5] comprising “catch-up” saccades that compensated for a substantial gain lag by almost periodical saccadic eye movements bringing the fovea back onto the smoothly moving target. We did not detect any significant correlation in patients with PSP between pursuit gain and the investigated brain structures, indicating that the occurrence of smooth pursuit abnormalities may not be explained by regional volumetric loss and demands future multimodal studies using brain connectivity measures to readdress this critical issue.…”

“…Alterations in oculomotor performance are ubiquitously present in parkinsonian syndromes including Parkinson's disease (PD), progressive supranuclear palsy (PSP) with the parkinsonian (PSP-P) and Richardson subtypes (PSP-RS), and multisystem atrophy (MSA) with the parkinsonian (MSA-P) and cerebellar subtypes (MSA-C) [3]. From a diagnostic perspective, according to the current Movement Disorder Society clinical diagnostic criteria for PD [4], oculomotor features in PD are purely exclusionary, i.e., oculomotor investigation is used to rule out “red flags” in order to distinguish it from other parkinsonian syndromes such as PSP and MSA [5]; however, there are no oculomotor features that are sufficiently specific to be used as supportive diagnostic information for PD [2]. Although measures of oculomotor performance in PD are not yet diagnostically specific, they provide an excellent research tool in patients [6].…”

Visual Contrast Sensitivity in Early-Stage Parkinson's Disease

“…Whereas eye movement deficits are highly characteristic of PD and other Parkinsonian disorders 17,19,[21][22][23][24][25][26][27][28] and neurodegenerative disorders in general, 18,20 we observed impairments in fixational stability only, and these were limited to the rate of small microsaccades. We did not observe a significant increase in the proportion of saccades classified as SWJ.…”

“…[17][18][19][20] Smooth pursuit and saccades have longer latencies and lower velocity in PD patients versus healthy age-matched controls. [17][18][19][20][21][22][23] Generally, lower pursuit eye velocity gain produces higher retinal image motion (motion blur), impairing perception of moving images. Fixational eye movements are characteristically unstable in PD, with more frequent small saccadic intrusions and tremor than in healthy controls.…”