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.

Functional Use of Eye Movements for an Acting System

“…However, to our knowledge, only two studies have taken this approach. In delayed and memory-guided reaching tasks, chronic stroke patients made predictive saccades with large endpoint errors, and performed more corrective saccades, compared with healthy controls [94]. Whereas stroke patients showed similar reach latencies to controls, their endpoint errors were larger.…”

Multiple processes independently predict motor learning

“…This knowledge may help advance post-stroke rehabilitation. Notably, most stroke survivors experience chronic difficulties performing daily motor tasks like cooking, walking, and driving [ 73 – 75 ], and many exhibit deficits in performing skilled limb movements [ 76 – 80 ], visual search [ 81 – 83 ], and eye-hand coordination [ 84 , 85 ]. Our findings suggest that these deficits may independently alter the outcomes of rehabilitation interventions designed to target mechanisms of motor learning.…”

Neuromechanical Biomarkers for Robotic Neurorehabilitation

“…Following the notion that the robot-assisted neurorehabilitation demands a highly patient-tailored process, which entails the identification of the unique needs, priorities, and recovery profile of the patient, the integration of the biomarkers belonging to the different domains (sensorimotor, cognitive-behavioral, autonomic, psychological, and psychosocial) is being undertaken (Bui and Johnson, 2018 ; Zariffa, 2018 ; Picelli et al, 2020 ). The idea of developing the profile of the patient that combines the relevance of the multifactorial biomarkers is a new approach that is starting to being explored, with the design of the dedicated study protocols for defining a related profile of the biomarkers of long-term recovery after stroke (Picelli et al, 2020 ) and the exploration of the novel biomarkers related to the other aspects of the motor function rather than sensorimotor such as alterations in the body representations (Maggio et al, 2021 ), eye–hand coupling assessment (Rizzo et al, 2017 ), quantification of visuospatial neglect (VSN) (Svaerke et al, 2019 ), and somatic (or cognitive-related) biomarkers (Martinez-Pernia, 2020 ). Additionally, the combination of the neuroimaging technologies is supporting this multifactorial exploration by combining EMG, EEG, and inertial data to obtain the rehabilitation-relevant biomarkers (Gao et al, 2018 ; Zhang et al, 2019 ; Picelli et al, 2020 ).…”