Microsaccades Track Location-Based Object Rehearsal in Visual Working Memory

Abstract

Besides controlling eye movements, the brain's oculomotor system has been implicated in the control of covert spatial attention and the rehearsal of spatial information in working memory. We investigated whether the oculomotor system also contributes to rehearsing visual objects in working memory when object location is never asked about. To address this, we tracked the incidental use of locations for mnemonic rehearsal via directional biases in microsaccades while participants maintained two visual objects (coloured oriented gratings) in working memory. By varying the stimulus configuration (horizontal, diagonal, and vertical) at encoding, we could quantify whether microsaccades were more aligned with the configurational axis of the memory contents, as opposed to the orthogonal axis. Experiment 1 revealed that microsaccades continued to be biased along the axis of the memory content several seconds into the working-memory delay. In Experiment 2, we confirmed that this directional microsaccade bias was specific to memory demands, ruling out lingering effects from passive and attentive encoding of the same visual objects in the same configurations. Thus, by studying microsaccade directions, we uncover oculomotor-driven rehearsal of visual objects in working memory through their associated locations.Significance StatementHow humans rehearse information in working memory is a foundational question in psychology and neuroscience. To provide insight into the cognitive and neural bases of working-memory rehearsal, we turned to microsaccades – small eye-movements produced by the brain's oculomotor system. We reveal how microsaccades track memorised objects’ locations during memory rehearsal, even when object location is never asked about. This brings three advances. From a psychology standpoint, it demonstrates how rehearsal engages object locations. From a neuroscience standpoint, it demonstrates how such location-based rehearsal recruits brain circuitry that also controls our eyes. From a practical standpoint, it demonstrates how microsaccades are a relevant variable in cognitive-neuroscience studies, and can themselves be utilised to track working-memory rehearsal across space and time.

Jointly looking to the past and the future in visual working memory

“…However, in this case, one may have expected to exclusively find a future-directed gaze bias, unlike what we observed. Moreover, using a complementary analysis of saccade directions along the axis of the future rule ( de Vries and van Ede, 2024 ), we found no direct evidence for remapping in the period between encoding and cue ( Figure 2—figure supplement 1 ). Second, when dealing with multiple memory contents, contents could be stored at the past location at first and the future location could be considered only after relevant memory content has been selected (in which case the past bias should have preceded the future bias).…”

“…Our finding of joint utilisation of past and future memory attributes emerged from at least two alternative scenarios of how the brain may deal with dynamic everyday working memory demands in which memory content is encoded at one location but needed at another. First, memory contents could have directly been remapped ( Brincat et al, 2021 ; de Vries and van Ede, 2024 ; Hayhoe and Ballard, 2005 ; Pelz and Canosa, 2001 ) to their future-relevant location. However, in this case, one may have expected to exclusively find a future-directed gaze bias, unlike what we observed.…”

Linking Cognitive Integrity to Working Memory Dynamics in the Aging Human Brain

“…Participants were instructed to keep their gaze fixated on the cross in the center of the screen during task performance. Even so, fixational eye movements are difficult to suppress (especially for individuals not used to psychophysical testing), and previous work has lined fixational eye movements to working memory performance ( Van Ede et al, 2019 ; Willeke et al, 2019 ; Linde-Domingo and Spitzer, 2023 ; De Vries and Van Ede, 2024 ). Furthermore, even small fixational eye movements may affect E/MEG data ( Yuval-Greenberg et al, 2008 ; Liu et al, 2022 ).…”

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

“…The mechanisms by which microsaccades reflect shifts in internal attention are at the forefront of contemporary cognitive research, with significant advancements noted in recent literature ( Griffin and Nobre, 2003 ; Souza and Oberauer, 2016 ; van Ede and Nobre, 2023 ). This reflection is potentially attributable to the involuntary encoding of location information with memory representations (e.g., Treisman and Zhang, 2006 ; Gu et al, 2020 ), coupled with an active rehearsal of memory representations based on their relative positions in the focus of attention ( de Vries and van Ede, 2024 ). One intriguing aspect for future examination is the dependency of microsaccade directionality on the spatial arrangement of information at the time of memory encoding, the relative positions among memory representation, as well as the interaction between the two factors.…”