An oculomotor continuum from exploration to fixation

Abstract

During visual exploration, saccadic eye movements scan the scene for objects of interest. During attempted fixation, the eyes are relatively still but often produce microsaccades. Saccadic rates during exploration are higher than those of microsaccades during fixation, reinforcing the classic view that exploration and fixation are two distinct oculomotor behaviors. An alternative model is that fixation and exploration are not dichotomous, but are instead two extremes of a functional continuum. Here, we measured the eye movements of human observers as they either fixed their gaze on a small spot or scanned natural scenes of varying sizes. As scene size diminished, so did saccade rates, until they were continuous with microsaccadic rates during fixation. Other saccadic properties varied as function of image size as well, forming a continuum with microsaccadic parameters during fixation. This saccadic continuum extended to nonrestrictive, ecological viewing conditions that allowed all types of saccades and fixation positions. Eye movement simulations moreover showed that a single model of oculomotor behavior can explain the saccadic continuum from exploration to fixation, for images of all sizes. These findings challenge the view that exploration and fixation are dichotomous, suggesting instead that visual fixation is functionally equivalent to visual exploration on a spatially focused scale.free-viewing | fixational eye movements | miniature eye movements | fixational saccades | natural images C lassic and current vision studies distinguish between visual exploration, characterized by the alternation of saccades and brief fixation periods, and attempted visual fixation, where subjects maintain relative gaze stability despite continuous but minute fixational eye movements (i.e., microsaccades, slow drift, and oculomotor tremor) (1-7). The theoretical separation between exploratory gaze shifts and attempted fixation dates back to the discovery of fixational eye movements in the early 1900s (2-4), and remains central to contemporary discourse in visual, cognitive, and oculomotor research (8). However, mounting evidence in support of a common generator for both exploratory saccades and fixational microsaccades (refs. 9-12 but see ref. 13) brings into question whether such a dichotomy is justified. Instead, it may be that saccades and microsaccades form an oculomotor continuum along the entire spectrum of exploratory scales, with classical exploratory saccades at one end and classical fixational microsaccades at the other end. In that case, it might be baseless to distinguish between fixational and exploratory behaviors. Recent studies have identified abnormal dynamics of saccades and microsaccades as potential diagnostic markers of neurological disease (14-16); thus, the frame of reference proposed here may have important clinical implications concerning the role of the affected brain centers in the patients' oculomotor behavior.To establish such a framework, one must first reconcile any known discrepancy between the ...

Oculomotor inhibition covaries with conscious detection

“…Even when an observer fixates on a single point, spontaneous microsaccades correct gaze position, prevent and counteract visual fading, and explore tiny image details McCamy et al 2014;Otero-Millan et al 2013;Rolfs 2009;Rucci and Victor 2015). The onset of an irrelevant stimulus inhibits these movements within 100 ms, followed by a rebound in the microsaccade rate (Engbert and Kliegl 2003;Hafed and Ignashchenkova 2013).…”

Abnormal fixational eye movements in strabismus

“…Disconjugate saccades have also been reported in monkeys with strabismus 16. Saccades and microsaccades follow an oculomotor continuum,17 and both types of movements are generated by common neural circuits 18–21. Besides saccades, strabismus is known to produce asymmetric, variable and subnormal convergence response 22.…”

Micro and regular saccades across the lifespan during a visual search of “Where’s Waldo” puzzles

“…In early studies, “microsaccade” referred to extremely small (less than 10–12 arc min, 0.16–0.20°) binocular eye movements and debate concentrated on whether these served any unique purpose for vision (Collewijn & Kowler, 2008; Hafed, 2011). However, the accepted definitional size of a microsaccade has increased (Martinez-Conde et al, 2009, 2013), such that microsaccades are now generally viewed as sitting at the small amplitude end of a microsaccade-saccade continuum (Ko et al, 2010; Martinez-Conde et al, 2013; Otero-Millan, Macknik, et al, 2013; Otero-Millan, Schneider, et al, 2013). For an alternative opinion see Collewijn and Kowler (2008).…”

“…At the neuroanatomical level, microsaccade generation appears almost identical to regular saccade generation (Hafed, Goffart, & Krauzlis, 2009; Hafed, Lovejoy, & Krauzlis, 2011). Rather than constituting a separate class of eye movements, they are believed to serve similar functions as larger saccades but within a narrow region around a point of fixation (Ko et al, 2010; McCamy et al, 2012; Otero-Millan, Macknik, et al, 2013; Otero-Millan, Schneider, et al, 2013). …”