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Research Articles, Behavioral/Cognitive

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

Jolande Fooken, Pooja Patel, Christina B. Jones, Martin J. McKeown and Miriam Spering
Journal of Neuroscience 19 January 2022, 42 (3) 487-499; DOI: https://doi.org/10.1523/JNEUROSCI.1690-21.2021
Jolande Fooken
1Centre for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada K7L 3N6
2Ophthalmology & Visual Sciences, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z3
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Pooja Patel
2Ophthalmology & Visual Sciences, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z3
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Christina B. Jones
5Medicine, Division of Neurology, University of British Columbia, Vancouver, British Columbia, Canada V6T 2B5
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Martin J. McKeown
3Graduate Program in Neuroscience, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z3
4Djavad Mowafaghian Center for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z3
5Medicine, Division of Neurology, University of British Columbia, Vancouver, British Columbia, Canada V6T 2B5
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Miriam Spering
2Ophthalmology & Visual Sciences, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z3
3Graduate Program in Neuroscience, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z3
4Djavad Mowafaghian Center for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z3
6Institute for Computing, Information and Cognitive Systems, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4
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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.

SIGNIFICANCE STATEMENT Eye movements are a promising clinical tool to aid in the diagnosis of movement disorders and to monitor disease progression. Although Parkinson's disease (PD) patients show some oculomotor abnormalities, it is not clear whether previously described eye movement impairments are task-specific. We assessed eye movements in PD under different visual (stationary vs moving targets) and movement (reactive vs deliberate) conditions. We demonstrate that PD patients are able to accurately track moving objects but make inaccurate eye movements toward stationary targets. The preservation of eye movements toward dynamic stimuli might enable patients to accurately act on the predicted motion path of the moving target. These results can inform the development of tools for the rehabilitation or maintenance of functional performance.

  • eye movements
  • Parkinson's disease
  • prediction
  • preservation of function
  • saccades
  • smooth pursuit

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The Journal of Neuroscience: 42 (3)
Journal of Neuroscience
Vol. 42, Issue 3
19 Jan 2022
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Preservation of Eye Movements in Parkinson's Disease Is Stimulus- and Task-Specific
Jolande Fooken, Pooja Patel, Christina B. Jones, Martin J. McKeown, Miriam Spering
Journal of Neuroscience 19 January 2022, 42 (3) 487-499; DOI: 10.1523/JNEUROSCI.1690-21.2021

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Preservation of Eye Movements in Parkinson's Disease Is Stimulus- and Task-Specific
Jolande Fooken, Pooja Patel, Christina B. Jones, Martin J. McKeown, Miriam Spering
Journal of Neuroscience 19 January 2022, 42 (3) 487-499; DOI: 10.1523/JNEUROSCI.1690-21.2021
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Keywords

  • eye movements
  • Parkinson's disease
  • prediction
  • preservation of function
  • saccades
  • smooth pursuit

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