The eyes are never still during maintained gaze fixation. When microsaccades are not occurring, ocular position exhibits continuous slow changes, often referred to as drifts. Unlike microsaccades, drifts remain to be viewed as largely random eye movements. Here we found that ocular position drifts can, instead, be very systematically stimulus-driven, and with very short latencies. We used highly precise eye tracking in three well trained macaque monkeys and found that even fleeting (~8 ms duration) stimulus presentations can robustly trigger transient and stimulus-specific modulations of ocular position drifts, and with only approximately 60 ms latency. Such drift responses are binocular, and they are most effectively elicited with large stimuli of low spatial frequency. Intriguingly, the drift responses exhibit some image pattern selectivity, and they are not explained by convergence responses, pupil constrictions, head movements, or starting eye positions. Ocular position drifts have very rapid access to exogenous visual information.

Visual selection in primates is intricately linked to eye movements, which are generated by a network of cortical and subcortical neural circuits. When visual selection is performed covertly, without foveating eye movements toward the selected targets, a class of fixational eye movements, called microsaccades, is still involved. Microsaccades are small saccades that occur when maintaining precise gaze fixation on a stationary point, and they exhibit robust modulations in peripheral cueing paradigms used to investigate covert visual selection mechanisms. These modulations consist of changes in both microsaccade directions and frequencies after cue onsets. Over the past two decades, the properties and functional implications of these modulations have been heavily studied, revealing a potentially important role for microsaccades in mediating covert visual selection effects. However, the neural mechanisms underlying cueing effects on microsaccades are only beginning to be investigated. Here we review the available causal manipulation evidence for these effects’ cortical and subcortical substrates. In the superior colliculus (SC), activity representing peripheral visual cues strongly influences microsaccade direction, but not frequency, modulations. In the cortical frontal eye fields (FEF), activity only compensates for early reflexive effects of cues on microsaccades. Using evidence from behavior, theoretical modeling, and preliminary lesion data from the primary visual cortex and microstimulation data from the lower brainstem, we argue that the early reflexive microsaccade effects arise subcortically, downstream of the SC. Overall, studying cueing effects on microsaccades in primates represents an important opportunity to link perception, cognition, and action through unaddressed cortical-subcortical neural interactions. These interactions are also likely relevant in other sensory and motor modalities during other active behaviors.

fixational eye movements; off responses; on responses; cueing; 58 saccadic inhibition 59 60 4New and noteworthy 61 Microsaccades are small saccades that occur during gaze fixation. Microsaccade rate 62is transiently reduced after sudden stimulus onsets, and then strongly rebounds before 63 returning to baseline. We explored the influence of stimulus polarity (black versus 64 white) on this "rate signature". We found that small black stimuli cause stronger 65 microsaccadic modulations than white ones, but primarily in the rebound phase. This 66 suggests dissociated neural mechanisms for microsaccadic inhibition and subsequent 67 rebound in the microsaccadic rate signature. 68 Ignashchenkova 2013; Laubrock et al. 2005; Peel et al. 2016; Rolfs et al. 2008; Tian 78 et al. 2018; Valsecchi et al. 2007; White and Rolfs 2016). This pattern has been 79 termed the "microsaccadic rate signature" (Engbert and Kliegl 2003; Hafed and 80 Ignashchenkova 2013; Rolfs 2009; Rolfs et al. 2008; Scholes et al. 2015), owing to 81 its highly repeatable nature across many paradigms, and it is also related to the more 82 general phenomenon of saccadic inhibition reported for larger saccades (Bompas ). 85 86 The neural mechanisms behind the microsaccadic rate signature, and saccadic 87 inhibition in general, are still being investigated. Neurophysiological perturbation 88 studies in the superior colliculus (SC), frontal eye fields (FEF), and primary visual 89 cortex (V1) have resulted in initial informative steps towards clarifying these 90 mechanisms. First, using a paradigm involving peripheral stimulus onsets, Hafed and 91 colleagues demonstrated that monkeys exhibit the same microsaccadic rate 92 signature as humans (Hafed et al. 2011). These effects persisted even after 93 thousands of trials performed by the same animals in the same tasks, confirming the 94 6 systematic nature of the effects. These authors then exploited the observation that 95 monkeys exhibit the same phenomenon as humans to perform invasive 96 neurophysiology; they reversibly inactivated portions of the SC topographic map 97 representing the locations of the appearing peripheral stimuli (Hafed et al. 2013). The 98 microsaccadic rate signature was virtually unaltered, whereas microsaccade 99 directions were significantly redistributed (Hafed et al. 2013), consistent with a 100 dissociation between the microsaccade rate signature and microsaccade direction 101 oscillations after stimulus onsets (Buonocore et al. 2017a; Hafed and 102 Ignashchenkova 2013; Tian et al. 2016). In follow up work, Peel and colleagues 103 extended these results by reversibly inactivating the FEF. They found that the early 104 inhibition was again unaltered, but, critically, the rebound phase of the microsaccadic 105 rate signature was affected (Peel et al. 2016); there were fewer post-inhibition 106 microsaccades than without FEF inactivation. In V1, lesions were found to affect 107 microsaccades in general, but the early inhibition after stimulus onset was generally 108 still present (Yo...

The primate superior colliculus (SC) contains a topographic map of space, such that the anatomical location of active neurons defines a desired eye movement vector. Complementing such a spatial code, SC neurons also exhibit saccade-related bursts that are tightly synchronized with movement onset. Current models suggest that such bursts constitute a rate code dictating movement kinematics. Here, using two complementary approaches, we demonstrate a dissociation between the SC rate code and saccade kinematics. First, we show that SC burst strength systematically varies depending on whether saccades of the same amplitude are directed towards the upper or lower visual fields, but the movements themselves have similar kinematics. Second, we show that for the same saccade vector, when saccades are significantly slowed down by the absence of a visible saccade target, SC saccade-related burst strengths can be elevated rather than diminished. Thus, SC saccade-related motor bursts do not necessarily dictate movement kinematics.