LRP predicts smooth pursuit eye movement onset during the ocular tracking of self-generated movements

Abstract

Chen J, Valsecchi M, Gegenfurtner KR. LRP predicts smooth pursuit eye movement onset during the ocular tracking of selfgenerated movements. J Neurophysiol 116: 18 -29, 2016. First published March 23, 2016 doi:10.1152/jn.00184.2016.-Several studies have indicated that human observers are very efficient at tracking self-generated hand movements with their gaze, yet it is not clear whether this is simply a by-product of the predictability of selfgenerated actions or if it results from a deeper coupling of the somatomotor and oculomotor systems. In a first behavioral experiment we compared pursuit performance as observers either followed their own finger or tracked a dot whose motion was externally generated but mimicked their finger motion. We found that even when the dot motion was completely predictable in terms of both onset time and kinematics, pursuit was not identical to that produced as the observers tracked their finger, as evidenced by increased rate of catch-up saccades and by the fact that in the initial phase of the movement gaze was lagging behind the dot, whereas it was ahead of the finger. In a second experiment we recorded EEG in the attempt to find a direct link between the finger motor preparation, indexed by the lateralized readiness potential (LRP) and the latency of smooth pursuit. After taking into account finger movement onset variability, we observed larger LRP amplitudes associated with earlier smooth pursuit onset across trials. The same held across subjects, where average LRP onset correlated with average eye latency. The evidence from both experiments concurs to indicate that a strong coupling exists between the motor systems leading to eye and finger movements and that simple top-down predictive signals are unlikely to support optimal coordination. anticipatory smooth pursuit; ocular tracking of self-motion; eye-hand coordination; lateralized readiness potential

Three-Dimensional Binocular Eye-Hand Coordination in Normal Vision and with Simulated Visual Impairment

“…As such, these conditions may not faithfully represent the normal coordination between oculomotor and hand movement control systems. Nevertheless, our data and results are highly consistent with the previous findings reported by other groups [86,28,95,45,97,96,51,76,65,13]. It should be also noted that our tracking latency data did not increase with increasing visual uncertainty (e.g., blur level in either horizontal or vergence pursuit tracking).…”

“…This finding is consistent with the view that there is an exchange of information between the motor systems of the eyes and hands [76]. Furthermore, Chen et al [13] provide convincing electrophysiological evidence that the oculomotor system may receive efference copy from the hand motor system. However, it is also possible that a common command signal controls coordinated hand and smooth pursuit eye movements [8].…”

“…It should be also noted that our tracking latency data did not increase with increasing visual uncertainty (e.g., blur level in either horizontal or vergence pursuit tracking). However, this may be largely due to the predictability of the target movement, as previously suggested by Chen et al [13]. Overall, our data suggest that eye-hand coordination need not be spatially and temporally aligned, and future work is needed to characterize the spatio-temporal limits of sensorimotor coupling.…”

“…We initially selected a rough maximum estimate of movement onset, which corresponded to the first position sample in which the target had moved in the direction of motion by at least 0.5 degrees for horizontal pursuit tracking and by at least 1 degree for vergence pursuit tracking. We then searched the movement traces up to this maximum estimate for the true movement onset using the method described by Schütz et al [80,13].…”

“…Thus, it is more likely that the eye and hand systems share motor planning information that facilitates the initiation of tracking eye movements, and then hand and arm proprioception helps maintain oculomotor tracking accuracy throughout the execution of the eye movements [95,97,96,51]. For example, a recent study [13] has shown that the lateralized readiness potential, which signals hand motor preparation, is associated with anticipatory smooth pursuit eye movements to self-generated finger motion. These findings provide convincing evidence that the hand motor system shares motor planning information with the oculomotor system: shared motor planning information could take the shape of a common command signal sent to both motor systems [8].…”