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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 23

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          Neural correlations, population coding and computation.

          How the brain encodes information in population activity, and how it combines and manipulates that activity as it carries out computations, are questions that lie at the heart of systems neuroscience. During the past decade, with the advent of multi-electrode recording and improved theoretical models, these questions have begun to yield answers. However, a complete understanding of neuronal variability, and, in particular, how it affects population codes, is missing. This is because variability in the brain is typically correlated, and although the exact effects of these correlations are not known, it is known that they can be large. Here, we review studies that address the interaction between neuronal noise and population codes, and discuss their implications for population coding in general.
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            Persistent activity in the prefrontal cortex during working memory.

            The dorsolateral prefrontal cortex (DLPFC) plays a crucial role in working memory. Notably, persistent activity in the DLPFC is often observed during the retention interval of delayed response tasks. The code carried by the persistent activity remains unclear, however. We critically evaluate how well recent findings from functional magnetic resonance imaging studies are compatible with current models of the role of the DLFPC in working memory. These new findings suggest that the DLPFC aids in the maintenance of information by directing attention to internal representations of sensory stimuli and motor plans that are stored in more posterior regions.
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              Neural activity predicts individual differences in visual working memory capacity.

              Contrary to our rich phenomenological visual experience, our visual short-term memory system can maintain representations of only three to four objects at any given moment. For over a century, the capacity of visual memory has been shown to vary substantially across individuals, ranging from 1.5 to about 5 objects. Although numerous studies have recently begun to characterize the neural substrates of visual memory processes, a neurophysiological index of storage capacity limitations has not yet been established. Here, we provide electrophysiological evidence for lateralized activity in humans that reflects the encoding and maintenance of items in visual memory. The amplitude of this activity is strongly modulated by the number of objects being held in the memory at the time, but approaches a limit asymptotically for arrays that meet or exceed storage capacity. Indeed, the precise limit is determined by each individual's memory capacity, such that the activity from low-capacity individuals reaches this plateau much sooner than that from high-capacity individuals. Consequently, this measure provides a strong neurophysiological predictor of an individual's capacity, allowing the demonstration of a direct relationship between neural activity and memory capacity.
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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
                d78e8a8f-0375-45c4-9044-4c8232dd35e4
                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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