Microsaccade direction reflects the economic value of potential saccade goals and predicts saccade choice

Abstract

Microsaccades are small-amplitude (typically <1°), ballistic eye movements that occur when attempting to fixate gaze. Initially thought to be generated randomly, it has recently been established that microsaccades are influenced by sensory stimuli, attentional processes, and certain cognitive states. Whether decision processes influence microsaccades, however, is unknown. Here, we adapted two classic economic tasks to examine whether microsaccades reflect evolving saccade decisions. Volitional saccade choices of monkey and human subjects provided a measure of the subjective value of targets. Importantly, analyses occurred during a period of complete darkness to minimize the known influence of sensory and attentional processes on microsaccades. As the time of saccadic choice approached, microsaccade direction became the following: 1) biased toward targets as a function of their subjective value and 2) predictive of upcoming, voluntary choice. Our results indicate that microsaccade direction is influenced by and is a reliable tell of evolving saccade decisions. Our results are consistent with dynamic decision processes within the midbrain superior colliculus; that is, microsaccade direction is influenced by the transition of activity toward caudal saccade regions associated with high saccade value and/or future saccade choice.

Dynamics of fixational eye position and microsaccades during spatial cueing: the case of express microsaccades

“…Moreover, time since the last microsaccade (Nachmias 1959) can be used, in conjunction with eye position measurements, to predict in real time whether microsaccades are expected to occur in response to visual stimuli. Because microsaccades are associated with substantial visual performance changes (Bellet et al 2017;Chen et al 2015;Chen and Hafed 2017;Hafed 2013;Hafed and Krauzlis 2010;Tian et al 2016;Watanabe et al 2013Watanabe et al , 2014Yu et al 2016Yu et al , 2017, such predictions could be used to control behavioral performance and neural activity in a variety of paradigms requiring gaze fixation.…”

Pupil dilation but not microsaccade rate robustly reveals decision formation

“…6B). Moreover, microsaccade rate has been shown to respond to odd stimuli in oddball tasks and can thus be considered as useful when investigating decision-making with rare targets 22,23 or with visuospatial cues 44 . A sudden change in brightness, as well as a key press did not alter microsaccade rate for the stimulus-locked data (Fig.…”

The necessity to choose causes the effects of reward on saccade preparation

“…Most of these studies however have compared rewarded to unrewarded behavior and did not include different levels of reward. When rewards of different magnitudes can be obtained, saccade endpoints are closer to high than to low reward targets 36 and maximize gain 33 , the microsaccade rate scales with value 37 and saccade vigor decreases with advanced discounting of rewards 16 , 38 . Here, looking at saccade latencies without interleaved choices (Experiment 1 & 3), we found no significant evidence for a direct influence of value in two out of three conditions.…”

“…The here reported inter-trial dependency might also have affected oculomotor and neural findings in monkeys 18 , 39 . A recent study tested whether microsaccade behavior also varies as a function of EV 37 . The authors reanalyzed their previously collected monkey data mixing choice and single responses 18 and recorded new human data for single-trials only.…”