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Attention can either increase or decrease spike count correlations in visual cortex

Abstract

Visual attention enhances the responses of visual neurons that encode the attended location. Several recent studies have shown that attention also decreases correlations between fluctuations in the responses of pairs of neurons (termed spike count correlation or rSC). These results are consistent with two hypotheses. First, attention-related changes in rate and rSC might be linked (perhaps through a common mechanism), with attention always decreasing rSC. Second, attention might either increase or decrease rSC, possibly depending on the role of the neurons 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 choices. These results place important constraints on models of the neuronal mechanisms underlying cognitive factors.

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Figure 1: Task and stimuli.
Figure 2: TTS calculation.
Figure 3: Hypotheses for how spike count correlations depend on TTS.
Figure 4: Attention can either increase or decrease spike count correlations.
Figure 5: Summary of results across 17 recording sessions.
Figure 6: The observed pattern of attention-related changes in rSC is not caused by differences in rate or baseline correlations.

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Acknowledgements

We thank R. Chang for assistance with animal training and recordings, K. McCracken for technical assistance, and J. Maunsell and B. Doiron for comments on an earlier version of this manuscript. The authors are supported by US National Institutes of Health grants 4R00EY020844-03 and R01 EY022930 (M.R.C.), a training grant slot on US National Institutes of Health grant 5T32NS7391-14 (D.A.R.), a Whitehall Foundation grant (M.R.C.), a Klingenstein Fellowship (M.R.C.) and a Sloan Research Fellowship (M.R.C.).

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D.A.R. and M.R.C. designed the experiments, analyzed the data and wrote the manuscript. D.A.R. conducted the experiments. M.R.C. supervised the project.

Corresponding author

Correspondence to Marlene R Cohen.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Example recordings from chronically implanted microarrays

(a) An example recording session from Monkey F. Each panel shows overlaid waveforms from several seconds of threshold crossings from one electrode. The panels are arranged in the same spatial layout for the arrays implanted in the left hemisphere (8 rows by 6 columns on the left side of the figure) and right hemisphere (right side of the figure). (b) and (c) depict close up views of the waveforms from the electrodes highlighted in panel (a) in red and yellow, respectively. The trace in (b) contains a single-unit in addition to multi-unit activity. The trace in (c) contains multi-unit activity. (d) and (e) depict example PSTHs from a representative single unit and a representative multiunit cluster, respectively. The stimuli came on at time 0 and remained on the screen past the 300 ms mark where these plots end. Note the different Y–axis scale between (d) and (e) as well as the different baseline firing rates. The thin gray lines on either side of the black trace are s.e.m.

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Ruff, D., Cohen, M. Attention can either increase or decrease spike count correlations in visual cortex. Nat Neurosci 17, 1591–1597 (2014). https://doi.org/10.1038/nn.3835

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