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      Attention can increase or decrease spike count correlations between pairs of neurons depending on their role in a task

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      Nature neuroscience

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          Abstract

          Visual attention enhances the responses of visual neurons that encode the attended location. Several recent studies showed that attention also decreases correlations between fluctuations in the responses of pairs of neurons (termed spike count correlation or r SC). The previous results are consistent with two hypotheses. Attention–related changes in rate and r SC might be linked (perhaps through a common mechanism), so that attention always decreases r SC. Alternately, attention might either increase or decrease r SC, possibly depending on the role the neurons play in the behavioral task. We recorded simultaneously from dozens of neurons in area V4 while monkeys performed a discrimination task. We found strong evidence in favor of the second hypothesis, showing that attention can flexibly increase or decrease correlations, depending on whether the neurons provide evidence for the same or opposite perceptual decisions. These results place important constraints on models of the neuronal mechanisms underlying cognitive factors.

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          Most cited references30

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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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            Attention improves performance primarily by reducing interneuronal correlations

            Visual attention can dramatically improve behavioural performance by allowing observers to focus on the important information in a complex scene. Attention also typically increases the firing rates of cortical sensory neurons. Rate increases improve the signal-to-noise ratio of individual neurons, and this improvement has been assumed to underlie attention-related improvements in behaviour. We recorded dozens of neurons simultaneously in visual area V4 and found that changes in single neurons accounted for only a small fraction of the improvement in the sensitivity of the population. Instead, over 80% of the attentional improvement in the population signal was caused by decreases in the correlations between the trial-to-trial fluctuations in the responses of pairs of neurons. These results suggest that the representation of sensory information in populations of neurons and the way attention affects the sensitivity of the population may only be understood by considering the interactions between neurons.
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              Correlated neuronal discharge rate and its implications for psychophysical performance.

              Single neurons can signal subtle changes in the sensory environment with surprising fidelity, often matching the perceptual sensitivity of trained psychophysical observers. This similarity poses an intriguing puzzle: why is psychophysical sensitivity not greater than that of single neurons? Pooling responses across neurons should average out noise in the activity of single cells, leading to substantially improved psychophysical performance. If, however, noise is correlated among these neurons, the beneficial effects of pooling would be diminished. To assess correlation within a pool, the responses of pairs of neurons were recorded simultaneously during repeated stimulus presentations. We report here that the observed covariation in spike count was relatively weak, the correlation coefficient averaging 0.12. A theoretical analysis revealed, however, that weak correlation can limit substantially the signalling capacity of the pool. In addition, theory suggests a relationship between neuronal responses and psychophysical decisions which may prove useful for identifying cell populations underlying specific perceptual capacities.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                19 May 2015
                12 October 2014
                November 2014
                27 May 2015
                : 17
                : 11
                : 1591-1597
                Affiliations
                Department of Neuroscience and Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, PA
                Author notes
                [* ]Correspondence: Marlene Cohen, 4400 Fifth Ave., MI Room 115, Pittsburgh, PA 15213, Tel: 412-268-4486, cohenm@ 123456pitt.edu
                Article
                NIHMS628381
                10.1038/nn.3835
                4446056
                25306550
                271b7c21-444d-43d5-b71a-d49948c7d050
                History
                Categories
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                Neurosciences
                Neurosciences

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