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Dynamics of coherent activity between cortical areas defines a two-stage process of top-down attention

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Abstract

Analysing a visual scene requires the brain to briefly keep in memory potentially relevant items of that scene and then direct attention to their locations for detailed processing. To reveal the neuronal basis of the underlying working memory and top-down attention processes, we trained macaques to match two patterns presented with a delay between them. As the above processes are likely to require communication between brain regions, and the parietal cortex is known to be involved in spatial attention, we simultaneously recorded neuronal activities from the interconnected parietal and middle temporal areas. We found that mnemonic information about features of the first pattern was retained in coherent oscillating activity between the two areas in high-frequency bands, followed by coherent activity in lower frequency bands mediating top-down attention on the relevant spatial location. Oscillations maintaining featural information also modulated activity of the cells of the parietal cortex that mediate attention. This could potentially enable transfer of information to organize top-down signals necessary for selective attention. Our results provide evidence in support of a two-stage model of visual attention where the first stage involves creating a saliency map representing a visual scene and at the second stage attentional feedback is provided to cortical areas involved in detailed analysis of the attended parts of a scene.

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Data availability

All data that are not presented in manuscript are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank Dr. Ivan Pigarev for taking part in some of the early studies. We are grateful to Drs. Andrew Metha and Chris French for critical comments on the manuscript.

Funding

This work was supported by project grants (251600, 454676 and 628668) from the Australian National Health and Medical Research Council to T.R.V. E.L. was partly supported by ARC Centre of Excellence in Integrative Brain Function.

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Authors and Affiliations

  1. Department of Optometry and Vision Sciences, The University of Melbourne, Parkville, VIC, 3010, Australia

    E. Levichkina, M. Kermani, Y. B. Saalmann & T. R. Vidyasagar

  2. Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, 127051, Russia

    E. Levichkina

  3. ARC Centre of Excellence in Integrative Brain Function, University of Melbourne Node, Melbourne, Australia

    E. Levichkina & T. R. Vidyasagar

  4. Department of Psychology, University of Wisconsin – Madison, Madison, WI, 53706, USA

    Y. B. Saalmann

Authors
  1. E. Levichkina
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  2. M. Kermani
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  3. Y. B. Saalmann
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  4. T. R. Vidyasagar
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Contributions

YS and TRV conceptualised and performed the original experiments and collected the data. EL, TRV and MK conceptualised the present model. EL developed the analytical tools for studying the model. EL and MK did the bulk of the new analysis. EL and TRV wrote the original draft. All authors critically reviewed and edited the final manuscript. TRV acquired funding and administered the project.

Corresponding author

Correspondence to T. R. Vidyasagar.

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Conflict of interest

The authors declare no conflict of interests or competing interests.

Ethics approval

The study was conducted as per the guidelines of the National Health and Medical Research Council Australian Code of Practice for the Care and Use of Animals for Scientific Purposes and approved by the University of Melbourne Animal Experimentation Ethics Committee.

Additional information

Communicated by Melvyn A. Goodale.

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Levichkina, E., Kermani, M., Saalmann, Y.B. et al. Dynamics of coherent activity between cortical areas defines a two-stage process of top-down attention. Exp Brain Res 239, 2767–2779 (2021). https://doi.org/10.1007/s00221-021-06166-w

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