Microsaccades are directed toward the midpoint between targets in a variably cued attention task

Abstract

Reliable, noninvasive biomarkers that reveal the internal state of a subject are an invaluable tool for neurological diagnoses. Small fixational eye movements, called microsaccades, are a candidate biomarker thought to reflect a subject's focus of attention [Z. M. Hafed, J. J. Clark, VisionRes. 42 , 2533–2545 (2002); R. Engbert, R. Kliegl, VisionRes. 43 , 1035–1045 (2003)]. The linkage between the direction of microsaccades and attention has mainly been demonstrated using explicit and unambiguous attentional cues. However, the natural world is seldom predictable and rarely provides unambiguous information. Thus, a useful biomarker must be robust to such changes in environmental statistics. To determine how well microsaccades reveal visual-spatial attention across behavioral contexts, we analyzed these fixational eye movements in monkeys performing a conventional change detection task. The task included two stimulus locations and variable cue validities across blocks of trials. Subjects were adept at the task, showing precise and graded modulations of visual attention for subtle target changes and performing better and faster when the cue was more reliable [J. P. Mayo, J. H. R. Maunsell, J. Neurosci. 36 , 5353 (2016)]. However, over tens of thousands of microsaccades, we found no difference in microsaccade direction between cued locations when cue variability was high nor between hit and miss trials. Instead, microsaccades were made toward the midpoint of the two target locations, not toward individual targets. Our results suggest that the direction of microsaccades should be interpreted with caution and may not be a reliable measure of covert spatial attention in more complex viewing conditions.

Dissociation of attentional state and behavioral outcome using local field potentials

“…Saccade preparation is another factor which can modulate the low-frequency oscillations in V4 (Steinmetz and Moore, 2014) that might contribute to better behavioral discriminability. However, a recent study which used the same experimental data found no difference in the microsaccade direction – a potential indicator of saccade preparation (Hafed and Krauzlis, 2012) - between hits and miss trials (Willett and Mayo, 2023).…”

Attention and microsaccades: do attention shifts trigger new microsaccades or only bias ongoing microsaccades?

“…A recent study (Willett & Mayo, 2023) found little to no evidence for a directional biasing of microsaccades to an attended visual stimulus, despite clear behavioural and neural benefits of attention. A critical difference with our study is that the authors did not consider shifts of attention following a cue, but rather sustaining attention to either of two targets that remained fixed throughout a block of trials.…”

“…One particular example of this contribution comes from the study of microsaccades, a class of fixational eye-movements that occur even during attempted fixation (e.g., (Engbert, 2006;Hafed et al, 2015;Martinez-Conde et al, 2004;Rolfs, 2009;Rucci & Poletti, 2015)). In particular, it has been demonstrated how the direction of fixational microsaccades can be modulated by the deployment of spatial attention to peripherally attended locations, in the absence of large eye-movements to these locations ( (Corneil & Munoz, 2014;Engbert, 2012;Engbert & Kliegl, 2003;Fernández et al, 2023;Hafed et al, 2011;Hafed & Clark, 2002;Laubrock et al, 2005;Lowet et al, 2018;Pastukhov & Braun, 2010;Xue et al, 2020); but see also (Horowitz et al, 2007;Tse et al, 2002;Willett & Mayo, 2023) to which we return in our discussion). Building on this earlier work, we recently uncovered similar microsaccade biases when directing attention to memorised visual contents held within the spatial lay-out of working memory (e.g., (de Vries & van Ede, 2023;Liu et al, 2022;van Ede et al, 2019van Ede et al, , 2020van Ede et al, , 2021).…”

Microsaccades reflect attention shifts: a mini review of 20 years of microsaccade research

“…Attention shifts induced by emotional stimuli modulated microsaccadic activity ( Kashihara et al, 2014 ). In more ecologically valid environments, some studies replicated the link between attention and microsaccade direction (e.g., Barnhart et al, 2019 ; Xue et al, 2020 ), while others found that this relationship disappears with increasing environmental complexity ( Willett and Mayo, 2023 ).…”