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Eye Control Deficits Coupled to Hand Control Deficits: Eye-Hand Incoordination in Chronic Cerebral Injury.

ABSTRACT: It is widely accepted that cerebral pathology can impair ocular motor and manual motor control. This is true in indolent and chronic processes, such as neurodegeneration and in acute processes such as stroke or those secondary to neurotrauma. More recently, it has been suggested that disruptions in these control systems are useful markers for prognostication and longitudinal monitoring. The utility of examining the relationship or the coupling between these systems has yet to be determined. We measured eye and hand-movement control in chronic, middle cerebral artery stroke, relative to healthy controls, in saccade-to-reach paradigms to assess eye-hand coordination. Primary saccades were initiated significantly earlier by stroke participants relative to control participants. However, despite these extremely early initial saccades to the target, reaches were nevertheless initiated at approximately the same time as those of control participants. Control participants minimized the time period between primary saccade onset and reach initiation, demonstrating temporal coupling between eye and hand. In about 90% of all trials, control participants produced no secondary, or corrective, saccades, instead maintaining fixation in the terminal position of the primary saccade until the end of the reach. In contrast, participants with stroke increased the time period between primary saccade onset and reach initiation. During this temporal decoupling, multiple saccades were produced in about 50% of the trials with stroke participants making between one and five additional saccades. Reaches made by participants with stroke were both longer in duration and less accurate. In addition to these increases in spatial reach errors, there were significant increases in saccade endpoint errors. Overall, the magnitude of the endpoint errors for reaches and saccades were correlated across participants. These findings suggest that in individuals with otherwise intact visual function, the spatial and temporal relationships between the eye and hand are disrupted poststroke, and may need to be specifically targeted during neurorehabilitation. Eye-hand coupling may be a useful biomarker in individuals with cerebral pathology in the setting of neurovascular, neurotraumatic, and neurodegenerative pathology.

SUBMITTER: Rizzo JR

PROVIDER: S-EPMC5512342 | biostudies-other | 2017

REPOSITORIES: biostudies-other

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Project description:A barrier in the diagnosis of mild traumatic brain injury (mTBI) stems from the lack of measures that are adequately sensitive in detecting mild head injuries. MRI and CT are typically negative in mTBI patients with persistent symptoms of post-concussive syndrome (PCS), and characteristic difficulties in sustaining attention often go undetected on neuropsychological testing, which can be insensitive to momentary lapses in concentration. Conversely, visual tracking strongly depends on sustained attention over time and is impaired in chronic mTBI patients, especially when tracking an occluded target. This finding suggests deficient internal anticipatory control in mTBI, the neural underpinnings of which are poorly understood. The present study investigated the neuronal bases for deficient anticipatory control during visual tracking in 25 chronic mTBI patients with persistent PCS symptoms and 25 healthy control subjects. The task was performed while undergoing magnetoencephalography (MEG), which allowed us to examine whether neural dysfunction associated with anticipatory control deficits was due to altered alpha, beta, and/or gamma activity. Neuropsychological examinations characterized cognition in both groups. During MEG recordings, subjects tracked a predictably moving target that was either continuously visible or randomly occluded (gap condition). MEG source-imaging analyses tested for group differences in alpha, beta, and gamma frequency bands. The results showed executive functioning, information processing speed, and verbal memory deficits in the mTBI group. Visual tracking was impaired in the mTBI group only in the gap condition. Patients showed greater error than controls before and during target occlusion, and were slower to resynchronize with the target when it reappeared. Impaired tracking concurred with abnormal beta activity, which was suppressed in the parietal cortex, especially the right hemisphere, and enhanced in left caudate and frontal-temporal areas. Regional beta-amplitude demonstrated high classification accuracy (92%) compared to eye-tracking (65%) and neuropsychological variables (80%). These findings show that deficient internal anticipatory control in mTBI is associated with altered beta activity, which is remarkably sensitive given the heterogeneity of injuries.

Project description:Imbalance is common following mild Traumatic Brain Injury (mTBI) and can persist months after the initial injury. To determine if mTBI subjects with chronic imbalance differed from healthy age- and sex-matched controls (HCs) we used both the Central SensoriMotor Integration (CSMI) test, which evaluates sensory integration, time delay, and motor activation properties and the standard Sensory Organization Test (SOT). Four CSMI conditions evoked center-of-mass sway in response to: surface tilts with eyes closed (SS/EC), surface tilts with eyes open viewing a fixed visual surround (SS/EO), visual surround tilts with eyes open standing on a fixed surface (VS/EO), and combined surface and visual tilts with eyes open (SS+VS/EO). The mTBI participants relied significantly more on visual cues during the VS/EO condition compared to HCs but had similar reliance on combinations of vestibular, visual, and proprioceptive cues for balance during SS/EC, SS/EO, and SS+VS/EO conditions. The mTBI participants had significantly longer time delays across all conditions and significantly decreased motor activation relative to HCs across conditions that included surface-tilt stimuli with a sizeable subgroup having a prominent increase in time delay coupled with reduced motor activation while demonstrating no vestibular sensory weighting deficits. Decreased motor activation compensates for increased time delay to maintain stability of the balance system but has the adverse consequence that sensitivity to both internal (e.g., sensory noise) and external disturbances is increased. Consistent with this increased sensitivity, SOT results for mTBI subjects showed increased sway across all SOT conditions relative to HCs with about 45% of mTBI subjects classified as having an "Aphysiologic" pattern based on published criteria. Thus, CSMI results provided a plausible physiological explanation for the aphysiologic SOT pattern. Overall results suggest that rehabilitation that focuses solely on sensory systems may be incomplete and may benefit from therapy aimed at enhancing rapid and vigorous responses to balance perturbations.

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Eye Control Deficits Coupled to Hand Control Deficits: Eye-Hand Incoordination in Chronic Cerebral Injury.

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