Fixational saccades reflect volitional action preparation

Abstract

Human volitional actions are preceded by preparatory processes, a critical mental process of cognitive control for future behavior. Volitional action preparation is regulated by large-scale neural circuits including the cerebral cortex and the basal ganglia. Because volitional action preparation is a covert process, the network dynamics of such neural circuits have been examined by neuroimaging and recording event-related potentials. Here, we examined whether such covert processes can be measured by the overt responses of fixational saccades (including microsaccades), the largest miniature eye movements that occur during eye fixation. We analyzed fixational saccades while adult humans maintained fixation on a central visual stimulus as they prepared to generate a volitional saccade in response to peripheral stimulus appearance. We used the antisaccade paradigm, in which subjects generate a saccade toward the opposite direction of a peripheral stimulus. Appropriate antisaccade performance requires the following two aspects of volitional control: 1) facilitation of saccades away from the stimulus and 2) suppression of inappropriate saccades toward the stimulus. We found that fixational saccades that occurred before stimulus appearance reflected the dual preparatory states of saccade facilitation and suppression and correlated with behavioral outcome (i.e., whether subjects succeeded or failed to cancel inappropriate saccades toward the stimulus). Moreover, fixational saccades explained a large proportion of individual differences in behavioral performance (poor/excellent) across subjects. These results suggest that fixational saccades predict the outcome of future volitional actions and may be used as a potential biomarker to detect people with difficulties in volitional action preparation.

Enhanced sensory sampling precedes self-initiated locomotion in an electric fish

“…As the preparatory sensory acquisition before movement offers substantial evolutionary advantages, it may be a general feature of the vertebrate brain. Recent studies in humans found a link between preparatory visual sampling and voluntary eye movements, by measuring fixational saccades occurring before the stimulus appearance that signalled voluntary gaze (Watanabe et al, 2013). A sustained period of heightened sensory sampling during movement preparation could improve the detectability of weak or infrequent sensory signals in a noisy background that might be biologically important (Ratnam and Nelson, 2000;Gussin et al, 2007).…”

Ocular drift reflects volitional action preparation

“…Neural activity for saccade preparation builds up over time (Dorris, Pare, & Munoz, ; Everling & Munoz, ; Watanabe & Munoz, ), which could be readout by fixational eye movements (Jainta et al., ; Wang et al., ; Watanabe et al., ). We therefore included the following two conditions that manipulated fixation durations to modulate saccade preparation experimentally; random and constant conditions.…”

“…Volitional action preparation can be defined operationally as neural processes controlling the preparatory activity across the neural axis (Haggard, ). We hypothesized that such processes could possibly be readout by fixational eye movements because modulations in the frequency of fixational saccades and pupil dilation are in accordance with neural signals controlling volitional saccades during the antisaccade paradigm (Wang et al., ; Watanabe et al., ).…”

“…The hypothesis of mental fatigue focuses on changes in arousal states over several hours (Di Stasi et al., ). In contrast, our hypothesis of volitional action preparation focuses on a short period of time (hundreds of milliseconds) within a current trial (Watanabe et al., ). Accordingly, cognitive effects on ocular drift, not identified in the previous study, could be revealed possibly by analyses designed appropriately with respect to specific task events that guide cognitive behavior.…”

“…However, it has been shown recently that volitional action preparation can be readout by looking at eye movement behavior (Corneil & Munoz, ). We have shown previously that the frequency of fixational saccades, the largest miniature eye movements including microsaccades, is modulated during fixation maintenance as subjects prepare to generate a volitional saccade (Watanabe, Matsuo, Zha, Munoz, & Kobayashi, ). Similar results have also been reported for pupil dilation (Jainta, Vernet, Yang, & Kapoula, ; Wang, Brien, & Munoz, ).…”