Distinct functional properties of the vertical and horizontal saccadic network in Health and Parkinson's disease: An eye-tracking and fMRI study

Lemos, Joâo; Pereira, Daniela; Almendra, Luciano; Rebelo, Diliana; Patrício, Miguel; Castelhano, João; Cunha, Gil; Januário, Cristina; Cunha, Luı́s; Freire, Antônio Fernando Menezes

doi:10.1016/j.brainres.2016.07.037

Cited by 26 publications

(28 citation statements)

References 71 publications

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“…This processing is supposed to largely bypass the BG circuit and it is considered the reason why reflexive saccades are mostly preserved in PD, particularly at early stages of the disease, while voluntary saccades are more severely affected ( 15 , 17 ). According to this picture, a recent fMRI study, while failing to find differences in saccadic metrics between PD patients and controls, found that PD showed left frontal underactivation during horizontal prosaccades and right parietal overactivation during horizontal and vertical prosaccades and horizontal antisaccades ( 18 ).…”

Section: Introductionmentioning

confidence: 99%

Eye Movements in Parkinson’s Disease and Inherited Parkinsonian Syndromes

Pretegiani

Optican

2017

Front. Neurol.

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Despite extensive research, the functions of the basal ganglia (BG) in movement control have not been fully understood. Eye movements, particularly saccades, are convenient indicators of BG function. Here, we review the main oculomotor findings reported in Parkinson’s disease (PD) and genetic parkinsonian syndromes. PD is a progressive, neurodegenerative disorder caused by dopaminergic cell loss within the substantia nigra pars compacta, resulting in depletion of striatal dopamine and subsequent increased inhibitory BG output from the internal globus pallidus and the substantia nigra pars reticulata. Eye movement abnormalities are common in PD: anomalies are more evident in voluntary than reflexive saccades in the initial stages, but visually guided saccades may also be involved at later stages. Saccadic hypometria (including abnormally fragmented saccades), reduced accuracy, and increased latency are among the most prominent deficits. PD patients show also unusually frequent and large square wave jerks and impaired inhibition of reflexive saccades when voluntary mirror saccades are required. Poor convergence ability and altered pursuit are common. Inherited parkinsonisms are a heterogeneous group of rare syndromes due to gene mutations causing symptoms resembling those of PD. Eye movement characteristics of some parkinsonisms have been studied. While sharing some PD features, each syndrome has a distinctive profile that could contribute to better define the clinical phenotype of parkinsonian disorders. Moreover, because the pathogenesis and the underlying neural circuit failure of inherited parkinsonisms are often well defined, they might offer a better prospect than idiopathic PD to understand the BG function.

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Section: Introductionmentioning

confidence: 99%

Eye Movements in Parkinson’s Disease and Inherited Parkinsonian Syndromes

Pretegiani

Optican

2017

Front. Neurol.

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“…Execution of eye movement involves the frontal eye fields, supplemental eye field and the parietal eye fields. Functional MRIs (magnetic resonance imaging) in PD patients have demonstrated underactivity in the frontal eye fields and the supplemental eye fields and a relative hyperactivity in the parietal fields [ 43 , 44 ].…”

Section: Discussionmentioning

confidence: 99%

Slower saccadic reading in Parkinson’s disease

Jehangir

Song

et al. 2018

PLoS ONE

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Idiopathic Parkinson’s Disease (PD) is characterized by degeneration of dopaminergic and other neurons, leading to motor and non-motor deficits. Abnormal eye movements in PD, including fixations, saccades, and convergence, are well described. However, saccadic reading, which requires serial and alternating saccades and fixations, is not well studied, despite its obvious impact on the quality of life. In this study, we assessed saccadic reading using variations of the King-Devick (KD) test, a rapid single digit number naming test, as a way to assess the ability to make serial left-to-right ocular motor movements necessary for reading. We recruited 42 treated PD patients and 80 age-matched controls and compared their reading times with a variety of measures, including age, duration of disease, Unified Parkinson’s Disease Rating Scale (UPDRS), the National Eye Institute 25-Item Visual Functioning Questionnaire 25 (VFQ-25), and Montreal Cognitive assessment (MoCA) test. The subjects performed 4 trials of reading 120 single digit numbers aloud as fast as possible without making errors. In each trial, they read 3 pages (KD1, KD2, and KD3), and each page contained 40 numbers per page in 8 lines with 5 numbers/line. We found that PD patients read about 20% slower than controls on all tests (KD1, 2, and 3 tests) (p < 0.02), and both groups read irregularly spaced numbers slower than regularly spaced numbers. Having lines between numbers to guide reading (KD1 tests) did not impact reading time in both PD and controls, but increased visual crowding as a result of decreased spacing between numbers (KD3 tests) was associated with significantly slower reading times in both PD and control groups. Our study revealed that saccadic reading is slower in PD, but controls and PD patients are both impacted by visuospatial planning challenges posed by increased visual crowding and irregularity of number spacing. Reading time did not correlate with UPDRS or MoCA scores in PD patients but significantly correlated with age, duration of disease, and VFQ-25 scores. The presence of convergence insufficiency did not significantly correlate with reading time in PD patients, although on average there was slower reading time in those with convergence insufficiency by 8 s (p = 0.2613). We propose that a simple reading task using 120 single-digit numbers can be used as a screening tool in the clinical setting to assess functional ocular motor difficulties in Parkinson’s disease that can have a profound impact on quality of life.

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“…The “classic” “task-evoked” fMRI concept, i.e., simultaneous eye movement recordings and visual stimulus presentation in the MRI scanner, have limitations including the restriction of MRI-dedicated eye movement recording devices and the “noisy” and uncomfortable environment. Some concepts have emerged that to overcome these limitations of eye movement recordings in the scanner by running the fMRI scan afterward or before performing extensive eye movement assessment in a dedicated oculomotor lab ( 50 , 51 ). The observed activation patterns in these studies revealed regions that are on the one hand part of the well-known oculomotor network and on the other hand regions that are known to be functionally disrupted in PD ( 50 , 52 ).…”

Section: Brain Mapping Of Oculomotor Phenotypes In Neurodegenerative mentioning

confidence: 99%

“…Some concepts have emerged that to overcome these limitations of eye movement recordings in the scanner by running the fMRI scan afterward or before performing extensive eye movement assessment in a dedicated oculomotor lab ( 50 , 51 ). The observed activation patterns in these studies revealed regions that are on the one hand part of the well-known oculomotor network and on the other hand regions that are known to be functionally disrupted in PD ( 50 , 52 ). The activation patterns in association with saccades impairment in PSP demonstrated that not only in the brainstem, but also cortical neuronal networks contributed to impaired saccadic eye movements in PSP ( 51 ).…”

Section: Brain Mapping Of Oculomotor Phenotypes In Neurodegenerative mentioning

confidence: 99%

Structural and Functional Brain Mapping Correlates of Impaired Eye Movement Control in Parkinsonian Syndromes: A Systems-Based Concept

Gorges¹,

Müller²,

Kassubek³

2018

Front. Neurol.

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The investigation of the human oculomotor system by eye movement recordings provides an approach to behavior and its alterations in disease. The neurodegenerative process underlying parkinsonian syndromes, including Parkinson’s disease (PD), progressive supranuclear palsy (PSP), and multisystem atrophy (MSA) changes structural and functional brain organization, and thus affects eye movement control in a characteristic manner. Video-oculography has been established as a non-invasive recording device for eye movements, and systematic investigations of eye movement control in a clinical framework have emerged as a functional diagnostic tool in neurodegenerative parkinsonism. Disease-specific brain atrophy in parkinsonian syndromes has been reported for decades, these findings were refined by studies utilizing diffusion tensor imaging (DTI) and task-based/task-free functional MRI—both MRI techniques revealed disease-specific patterns of altered structural and functional brain organization. Here, characteristic disturbances of eye movement control in parkinsonian syndromes and their correlations with the structural and functional brain network alterations are reviewed. On this basis, we discuss the growing field of graph-based network analysis of the structural and functional connectome as a promising candidate for explaining abnormal phenotypes of eye movement control at the network level, both in health and in disease.

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Distinct functional properties of the vertical and horizontal saccadic network in Health and Parkinson's disease: An eye-tracking and fMRI study

Cited by 26 publications

References 71 publications

Eye Movements in Parkinson’s Disease and Inherited Parkinsonian Syndromes

Eye Movements in Parkinson’s Disease and Inherited Parkinsonian Syndromes

Slower saccadic reading in Parkinson’s disease

Structural and Functional Brain Mapping Correlates of Impaired Eye Movement Control in Parkinsonian Syndromes: A Systems-Based Concept

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