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Human gaze tracks attentional focusing in memorized visual space

Abstract

Brain areas that control gaze are also recruited for covert shifts of spatial attention1,2,3,4,5,6,7,8,9. In the external space of perception, there is a natural ecological link between the control of gaze and spatial attention, as information sampled at covertly attended locations can inform where to look next2,10,11. Attention can also be directed internally to representations held within the spatial layout of visual working memory12,13,14,15,16. In such cases, the incentive for using attention to direct gaze disappears, as there are no external targets to scan. Here we investigate whether the oculomotor system of the brain also participates in attention focusing within the internal space of memory. Paradoxically, we reveal this participation through gaze behaviour itself. We demonstrate that selecting an item from visual working memory biases gaze in the direction of the memorized location of that item, despite there being nothing to look at and location memory never explicitly being probed. This retrospective ‘gaze bias’ occurs only when an item is not already in the internal focus of attention, and it predicts the performance benefit associated with the focusing of internal attention. We conclude that the oculomotor system also participates in focusing attention within memorized space, leaving traces all the way to the eyes.

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Fig. 1: Selection from working memory biases gaze towards the location of memorized visual items.
Fig. 2: Gaze bias reflects attentional focusing of currently unfocused memory items.
Fig. 3: Involuntary gaze shifts are insufficient to trigger attentional facilitation in visual working memory.
Fig. 4: Gaze bias generalizes across visual features.

Code availability

Code is available from the authors on reasonable request.

Data availability

All data are publically available through the Dryad Digital Repository at: https://doi.org/10.5061/dryad.m99r286.

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Acknowledgements

This research was funded by a Marie Skłodowska-Curie Fellowship from the European Commission (grant code: ACCESS2WM) to F.v.E., a Wellcome Trust Senior Investigator Award (grant number: 104571/Z/14/Z) and a James S. McDonnell Foundation Understanding Human Cognition Collaborative Award (grant number: 220020448) to A.C.N, and by the NIHR Oxford Health Biomedical Research Centre. The Wellcome Centre for Integrative Neuroimaging is supported by core funding from the Wellcome Trust (grant number: 203139/Z/16/Z). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. The authors also wish to thank A. Board and R. Silva Zunino for their help with the data collection of experiment 4.

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F.v.E. and A.C.N. conceived and designed the experiments. F.v.E. programmed the experiments. F.v.E. and S.R.C. acquired the data. F.v.E analysed the data. F.v.E., S.R.C. and A.C.N. interpreted the data. F.v.E. and A.C.N. drafted and revised the manuscript.

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Correspondence to Freek van Ede.

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van Ede, F., Chekroud, S.R. & Nobre, A.C. Human gaze tracks attentional focusing in memorized visual space. Nat Hum Behav 3, 462–470 (2019). https://doi.org/10.1038/s41562-019-0549-y

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