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Decoding reveals the contents of visual working memory in early visual areas

Abstract

Visual working memory provides an essential link between perception and higher cognitive functions, allowing for the active maintenance of information about stimuli no longer in view1,2. Research suggests that sustained activity in higher-order prefrontal, parietal, inferotemporal and lateral occipital areas supports visual maintenance3,4,5,6,7,8,9,10,11, and may account for the limited capacity of working memory to hold up to 3–4 items9,10,11. Because higher-order areas lack the visual selectivity of early sensory areas, it has remained unclear how observers can remember specific visual features, such as the precise orientation of a grating, with minimal decay in performance over delays of many seconds12. One proposal is that sensory areas serve to maintain fine-tuned feature information13, but early visual areas show little to no sustained activity over prolonged delays14,15,16. Here we show that orientations held in working memory can be decoded from activity patterns in the human visual cortex, even when overall levels of activity are low. Using functional magnetic resonance imaging and pattern classification methods, we found that activity patterns in visual areas V1–V4 could predict which of two oriented gratings was held in memory with mean accuracy levels upwards of 80%, even in participants whose activity fell to baseline levels after a prolonged delay. These orientation-selective activity patterns were sustained throughout the delay period, evident in individual visual areas, and similar to the responses evoked by unattended, task-irrelevant gratings. Our results demonstrate that early visual areas can retain specific information about visual features held in working memory, over periods of many seconds when no physical stimulus is present.

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Figure 1: Design of working memory experiment and resulting time course of fMRI activity.
Figure 2: Orientation decoding results for areas V1–V4.
Figure 3: Time-resolved decoding of individual fMRI time points.

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Acknowledgements

We thank D. Brady and B. Wolfe for technical support, and J. Gore and the Vanderbilt University Institute of Imaging Science for MRI support. This work was supported by a grant from the National Eye Institute, National Institutes of Health to F.T. and a postgraduate fellowship from the Natural Sciences and Engineering Research Council of Canada to S.A.H.

Author Contributions F.T. devised and designed the experiments, S.A.H. and F.T. programmed the experiments, S.A.H. conducted the experiments and carried out the analyses with assistance from F.T., F.T. and S.A.H. wrote the paper together.

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Correspondence to Frank Tong.

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Harrison, S., Tong, F. Decoding reveals the contents of visual working memory in early visual areas. Nature 458, 632–635 (2009). https://doi.org/10.1038/nature07832

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