Gaze direction as equilibrium: more evidence from spatial and temporal aspects of small-saccade triggering in the rhesus macaque monkey

Abstract

Rigorous behavioral studies made in human subjects have shown that small-eccentricity target displacements are associated with increased saccadic reaction times, but the reasons for this remain unclear. Before characterizing the neurophysiological foundations underlying this relationship between the spatial and temporal aspects of saccades, we tested the triggering of small saccades in the male rhesus macaque monkey. We also compared our results to those obtained in human subjects, both from the existing literature and through our own additional measurements. Using a variety of behavioral tasks exercising visual and nonvisual guidance of small saccades, we found that small saccades consistently require more time than larger saccades to be triggered in the nonhuman primate, even in the absence of any visual guidance and when valid advance information about the saccade landing position is available. We also found a strong asymmetry in the reaction times of small upper versus lower visual field visually guided saccades, a phenomenon that has not been described before for small saccades, even in humans. Following the suggestion that an eye movement is not initiated as long as the visuo-oculomotor system is within a state of balance, in which opposing commands counterbalance each other, we propose that the longer reaction times are a signature of enhanced times needed to create the symmetry-breaking condition that puts downstream premotor neurons into a push-pull regime necessary for rotating the eyeballs. Our results provide an important catalog of nonhuman primate oculomotor capabilities on the miniature scale, allowing concrete predictions on underlying neurophysiological mechanisms. NEW & NOTEWORTHY Leveraging a multitude of neurophysiological investigations in the rhesus macaque monkey, we generated and tested hypotheses about small-saccade latencies in this animal model. We found that small saccades always take longer, on average, than larger saccades to trigger, regardless of visual and cognitive context. Moreover, small downward saccades have the longest latencies overall. Our results provide an important documentation of oculomotor capabilities of an indispensable animal model for neuroscientific research in vision, cognition, and action.

Rapid stimulus-driven modulation of slow ocular position drifts

“…While the time bins in that study were too coarse to explore the short latency responses that we saw, these human results are, at least, consistent with our observation that image onsets can rapidly modulate ocular drifts. Other oculomotor phenomena are also very well preserved between monkeys and humans: some notable examples from our own prior work include ocular following responses ( Chen and Hafed, 2013 ) as well as saccade-related implications of SC visual field asymmetries ( Grujic et al, 2018 ; Hafed and Chen, 2016 ; Hafed and Goffart, 2020 ) and SC foveal magnification ( Chen et al, 2019 ; Hafed and Goffart, 2020 ; Willeke et al, 2019 ).…”

Rapid stimulus-driven modulation of slow ocular position drifts

“…While the time bins in that study were too coarse to explore the short latency responses that we saw, these human results are, at least, consistent with our observation that image onsets can rapidly modulate ocular drifts. Other oculomotor phenomena are also very well preserved between monkeys and humans: some notable examples from our own prior work include ocular following responses (Chen & Hafed, 2013) as well as saccade-related implications of SC visual field asymmetries (Grujic, Brehm, Gloge, Zhuo, & Hafed, 2018; Hafed & Chen, 2016; Hafed & Goffart, 2020) and SC foveal magnification (Chen et al, 2019; Hafed & Goffart, 2020; Willeke et al, 2019).…”

Closed loop motor-sensory dynamics in human vision

“…Interestingly, a different strategy appeared with size changes. When viewing small sized images, the visual system decreased the ROI sampling rate (consistent with [ 58 ]) while maintaining Sp and thus increasing Xp ( Fig 5 , Table on top ). A sequential open-loop scheme, in which the visual input affects Rs and Rs affects the drifts variables, is ruled out here; the mean values of Rs did not systematically change along with either Sp or Xp , and the pause-by-pause correlations between each Sp or Xp and its preceding instantaneous Rs (i.e., the inverse of the inter-saccadic-interval) were negligible (R 2 < 0.06).…”

“…Interestingly, a different strategy appeared with size changes. When viewing small sized images, the visual system decreased the ROI sampling rate (consistent with [58]) while maintaining Sp and thus increasing Xp (Fig 5, Table on top). A sequential open-loop scheme, in which the visual input affects Rs and Rs affects the drifts variables, is ruled out here; the mean…”

“…The dynamics of closed-loop systems are limited by the loop delay, that is, the time it takes for the effect of a signal to travel along the loop. In the drift system this delay can be estimated as < 50 ms [58]. Accordingly, drift oscillations around 10 Hz [61] may reflect fluctuating loop dynamics and may point to the characteristic limit cycle of the loop.…”