Abstract
Under natural behavioral conditions, visually guided eye movements are linked to direction-specific modulations of cortico-spinal system (CSS) excitability in upper-limb muscles, even in absence of a manual response. These excitability changes have been shown to be compatible with a covert motor program encoding a manual movement toward the same target of the eyes. The aim of this study is to investigate whether this implicit oculo-manual coupling is enforced following every saccade execution or it depends on the behavioral context. Twenty-two healthy young adults participated in the study. Single-pulse transcranial magnetic stimulation was applied to the motor cortex at nine different time epochs during a double-choice eye task, in which the decision to execute a prosaccade or an antisaccade was made on the color of a peripheral visual cue. By analyzing the amplitude of the motor evoked potentials (MEP) in three distal muscles of the resting upper-limb, a facilitation peak of CSS excitability was found in two of them at 120 ms before the eyes begin to move. Furthermore, a long-lasting, generalized reduced corticomotor excitability develops following the eye response. Finally, a quite large modulation of MEP amplitude, depending on the direction of the saccade, is observed only in the first dorsal interosseous muscle, in a narrow time window at about 150 ms before the eye movement, irrespective of the type of the ocular response (pro-/anti-saccade). This change in CSS excitability is not tied up to the timing of the occurrence of the visual cue but, instead, appears to be tightly time-related to the saccade onset. Observed excitability changes differ in many respects from those previously reported with different behavioral paradigms. A main finding of our study is that the implicit coupling between eye and hand motor systems is contingent upon the particular motor set determined by the cognitive aspects of the performed oculomotor task. In particular, the direction-specific modulation in CSS excitability described in this study appears to be related to perceptual and decision-making processes rather than representing an implicit upper-limb motor program, coupled to the saccade execution.
Highlights
In everyday life, we move the eyes in order to bring the image of a salient visual object on the fovea
Subjects were told to make an eye movement toward the peripheral visual stimulus or toward its mirror spatial position according to the stimulus color code and to maintain their gaze on the attained location until the turning off of the imperative stimulus, which marked the beginning of a new trial
By conducting a mixed-effect regression analysis on single motor evoked potentials (MEP) amplitudes for each transcranial magnetic stimulation (TMS) delay, on a model in which only ‘gaze direction’ was taken as both fixed and random effect at the participant level, we found that its fixed-effect regression coefficient was significant only at the TMS delay of 360 ms [type II Wald χ2(1) = 9.005; p = 0.003]
Summary
We move the eyes in order to bring the image of a salient visual object on the fovea. Fast eye movements typically fall into two broad classes. One class stems from the bottomup target selection triggered by a novel visual stimulus Such ‘exogenously’ cued ocular responses can be assimilated to a visual grasp reflex (Hess et al, 1946) which involves little or even no cognitive control. Saccades can voluntarily direct gaze toward a specific area of interest. The generation of such ‘endogenously’ cued saccades reflects additional processing requirements that involve, among others, goal-driven visual selection and top–down control of the oculomotor system
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