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

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          Abstract

          Visual working memory provides an essential link between perception and higher cognitive functions, allowing for the active maintenance of information regarding stimuli no longer in view 1, 2. Research suggests that sustained activity in higher-order prefrontal, parietal, inferotemporal and lateral occipital areas supports visual maintenance 3- 11, and may account for working memory’s limited capacity to hold up to 3-4 items 9- 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 seconds 12. One proposal is that sensory areas serve to maintain fine-tuned feature information 13, but early visual areas show little to no sustained activity over prolonged delays 14- 16. Using fMRI decoding methods 17, 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. Activity patterns in areas V1-V4 could predict which of two oriented gratings was held in memory with mean accuracy levels upwards of 80%, even in participants exhibiting activity that 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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          Most cited references 32

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          Neurophysiological investigation of the basis of the fMRI signal.

          Functional magnetic resonance imaging (fMRI) is widely used to study the operational organization of the human brain, but the exact relationship between the measured fMRI signal and the underlying neural activity is unclear. Here we present simultaneous intracortical recordings of neural signals and fMRI responses. We compared local field potentials (LFPs), single- and multi-unit spiking activity with highly spatio-temporally resolved blood-oxygen-level-dependent (BOLD) fMRI responses from the visual cortex of monkeys. The largest magnitude changes were observed in LFPs, which at recording sites characterized by transient responses were the only signal that significantly correlated with the haemodynamic response. Linear systems analysis on a trial-by-trial basis showed that the impulse response of the neurovascular system is both animal- and site-specific, and that LFPs yield a better estimate of BOLD responses than the multi-unit responses. These findings suggest that the BOLD contrast mechanism reflects the input and intracortical processing of a given area rather than its spiking output.
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            Working memory: looking back and looking forward.

             Alan Baddeley (2003)
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              The capacity of visual working memory for features and conjunctions.

              Short-term memory storage can be divided into separate subsystems for verbal information and visual information, and recent studies have begun to delineate the neural substrates of these working-memory systems. Although the verbal storage system has been well characterized, the storage capacity of visual working memory has not yet been established for simple, suprathreshold features or for conjunctions of features. Here we demonstrate that it is possible to retain information about only four colours or orientations in visual working memory at one time. However, it is also possible to retain both the colour and the orientation of four objects, indicating that visual working memory stores integrated objects rather than individual features. Indeed, objects defined by a conjunction of four features can be retained in working memory just as well as single-feature objects, allowing sixteen individual features to be retained when distributed across four objects. Thus, the capacity of visual working memory must be understood in terms of integrated objects rather than individual features, which places significant constraints on cognitive and neurobiological models of the temporary storage of visual information.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                0028-0836
                1476-4687
                25 March 2009
                18 February 2009
                2 April 2009
                2 October 2009
                : 458
                : 7238
                : 632-635
                Affiliations
                Psychology Department and Vanderbilt Vision Research Center, Vanderbilt University, Nashville, TN, USA, 37240
                Author notes
                Correspondence and requests for materials should be addressed to frank.tong@ 123456vanderbilt.edu
                Article
                nihpa103053
                10.1038/nature07832
                2709809
                19225460
                Funding
                Funded by: National Eye Institute : NEI
                Award ID: R01 EY017082-02 ||EY
                Funded by: National Eye Institute : NEI
                Award ID: R01 EY017082-01A2 ||EY
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