Preservation of Eye Movements in Parkinson's Disease Is Stimulus- and Task-Specific

Abstract

Parkinson's disease (PD) is a neurodegenerative disease that includes motor impairments, such as tremor, bradykinesia, and postural instability. Although eye movement deficits are commonly found in saccade and pursuit tasks, preservation of oculomotor function has also been reported. Here we investigate specific task and stimulus conditions under which oculomotor function in PD is preserved. Sixteen PD patients and 18 healthy, age-matched controls completed a battery of movement tasks that included stationary or moving targets eliciting reactive or deliberate eye movements: pro-saccades, anti-saccades, visually guided pursuit, and rapid go/no-go manual interception. Compared with controls, patients demonstrated systematic impairments in tasks with stationary targets: pro-saccades were hypometric and anti-saccades were incorrectly initiated toward the cued target in ;35% of trials compared with 14% errors in controls. In patients, task errors were linked to short latency saccades, indicating abnormalities in inhibitory control. However, patients' eye movements in response to dynamic targets were relatively preserved. PD patients were able to track and predict a disappearing moving target and make quick go/no-go decisions as accurately as controls. Patients' interceptive hand movements were slower on average but initiated earlier, indicating adaptive processes to compensate for motor slowing. We conclude that PD patients demonstrate stimulus and task dependency of oculomotor impairments, and we propose that preservation of eye and hand movement function in PD is linked to a separate functional pathway through the superior colliculus-brainstem loop that bypasses the fronto-basal ganglia network. Our results demonstrate that studying oculomotor and hand movement function in PD can support disease diagnosis and further our understanding of disease progression and dynamics.

Exploration of sensory-motor tradeoff behavior in Parkinson’s disease

“…Although terminating a catching movement is very different from aborting an ongoing movement at a random cue, as in stop signal reaction time tasks, or controlling prepotent response tendencies, as in conflict tasks, we consider this the most likely explanation. Another consideration is that patients, while showing good performance when moving to a physically present target under a time constraint (e.g., Majsak et al, 1998 ; Fooken et al, 2022 ), are poorer when the target location is not given but is estimated, as in the combined task. Thus motor execution might differ depending on whether the target is physically present or not.…”

“…Hence optimal control analyses provide a means to evaluate the change as compensatory in nature or pathological. Recent data showing faster movement initiation but slower movement speed in PD patients compared to controls ( Fooken et al, 2022 ), led the authors to ask the very same question: is it compensation or impulsivity?…”

“…First, previous studies have shown that patients initiate their movements earlier and move significantly faster to catch a moving ball compared to when reaching to a static ball ( Majsak et al, 1998 , 2008 ; Bieńkiewicz et al, 2013 , 2014 ). Second, the ball catching task has an embedded implicit time constraint, adding urgency for action and thus facilitating movement in PD patients ( Ballanger et al, 2006 , 2008 ; Majsak et al, 2008 ; Fooken et al, 2022 ). However, the facilitation by the perception of movement and by urgency, might in fact be a manifestation of reduced inhibition.…”

From anticipation to impulsivity in Parkinson’s disease

“…Eye movements are impacted by iPD 56 – 59 and oculomotor anticipation is reduced 60 – 62 . The increase in latency of visually-guided saccades is usually explained by an overactive inhibition of the superior colliculus (SC) by the substantia nigra pars reticulata (SNr) resulting in oculomotor bradykinesia/akinesia 63 , 64 .…”

Machine Learning and Eye Movements Give Insights into Neurodegenerative Disease Mechanisms

“…Fooken et al [26] studied different tasks and conditions in which the oculomotor function in Parkinson's patients is preserved. 16 patients with Parkinson's disease and 18 healthy, age-matched controls performed a set of tasks of saccades (RS), anti-saccades (AS), pursuits, and rapid 'go / no-go' manual interventions.…”