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Attention improves performance primarily by reducing interneuronal correlations

Abstract

Visual attention can improve behavioral 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 behavior. 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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Figure 1: Methods and behavior.
Figure 2: Attentional modulation of firing rate, Fano factor and noise correlation.
Figure 3: Attention has the biggest effects on the most responsive neurons.
Figure 4: Modulation of noise correlation accounts for the majority of the attentional improvement in population sensitivity.

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Acknowledgements

We thank D. Ruff for spike sorting and monkey training assistance, M. Churchland for code and advice regarding mean-matching and Fano factor analysis, and M. Histed for many helpful discussions. They, A. Ni and A. Smolyanskaya provided comments on an earlier version of the manuscript. This work was supported by US National Institutes of Health grant R01EY005911 and the Howard Hughes Medical Institute.

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M.R.C. collected the data and performed the analyses. M.R.C. and J.H.R.M. designed the study and wrote the paper.

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Correspondence to Marlene R Cohen.

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Cohen, M., Maunsell, J. Attention improves performance primarily by reducing interneuronal correlations. Nat Neurosci 12, 1594–1600 (2009). https://doi.org/10.1038/nn.2439

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