1. Neuroscience
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How biological attention mechanisms improve task performance in a large-scale visual system model

  1. Grace W Lindsay  Is a corresponding author
  2. Kenneth D Miller
  1. Columbia University, United States
Research Article
  • Cited 13
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Cite this article as: eLife 2018;7:e38105 doi: 10.7554/eLife.38105


How does attentional modulation of neural activity enhance performance? Here we use a deep convolutional neural network as a large-scale model of the visual system to address this question. We model the feature similarity gain model of attention, in which attentional modulation is applied according to neural stimulus tuning. Using a variety of visual tasks, we show that neural modulations of the kind and magnitude observed experimentally lead to performance changes of the kind and magnitude observed experimentally. We find that, at earlier layers, attention applied according to tuning does not successfully propagate through the network, and has a weaker impact on performance than attention applied according to values computed for optimally modulating higher areas. This raises the question of whether biological attention might be applied at least in part to optimize function rather than strictly according to tuning. We suggest a simple experiment to distinguish these alternatives.

Data availability

The weights for the model used are linked to in the study. The data resulting from simulations have been packaged and are available on Dryad (doi:10.5061/dryad.jc14081). The analysis code are available on GitHub (https://github.com/gwl2108/CNN_attention)

The following data sets were generated

Article and author information

Author details

  1. Grace W Lindsay

    Center for Theoretical Neuroscience, Columbia University, New York, United States
    For correspondence
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9904-7471
  2. Kenneth D Miller

    Center for Theoretical Neuroscience, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1433-0647


National Science Foundation (DBI-1707398)

  • Kenneth D Miller

National Institutes of Health (T32 NS064929)

  • Kenneth D Miller

Gatsby Charitable Foundation

  • Kenneth D Miller


  • Grace W Lindsay

National Science Foundation (IIS-1704938)

  • Kenneth D Miller

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Marcel van Gerven, Radboud Universiteit, Netherlands

Publication history

  1. Received: May 5, 2018
  2. Accepted: September 28, 2018
  3. Accepted Manuscript published: October 1, 2018 (version 1)
  4. Version of Record published: October 30, 2018 (version 2)


© 2018, Lindsay & Miller

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.


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Further reading

    1. Neuroscience
    Gordon H Petty et al.
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    Neocortical sensory areas have associated primary and secondary thalamic nuclei. While primary nuclei transmit sensory information to cortex, secondary nuclei remain poorly understood. We recorded juxtasomally from secondary somatosensory (POm) and visual (LP) nuclei of awake mice while tracking whisking and pupil size. POm activity correlated with whisking, but not precise whisker kinematics. This coarse movement modulation persisted after facial paralysis and thus was not due to sensory reafference. This phenomenon also continued during optogenetic silencing of somatosensory and motor cortex and after lesion of superior colliculus, ruling out a motor efference copy mechanism. Whisking and pupil dilation were strongly correlated, possibly reflecting arousal. Indeed LP, which is not part of the whisker system, tracked whisking equally well, further indicating that POm activity does not encode whisker movement per se. The semblance of movement-related activity is likely instead a global effect of arousal on both nuclei. We conclude that secondary thalamus monitors behavioral state, rather than movement, and may exist to alter cortical activity accordingly.

    1. Neuroscience
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    Neurophysiological studies depend on a reliable quantification of whether and when a neuron responds to stimulation. Simple methods to determine responsiveness require arbitrary parameter choices, such as binning size, while more advanced model-based methods require fitting and hyperparameter tuning. These parameter choices can change the results, which invites bad statistical practice and reduces the replicability. New recording techniques that yield increasingly large numbers of cells would benefit from a test for cell-inclusion that requires no manual curation. Here, we present the parameter-free ZETA-test, which outperforms t-tests, ANOVAs, and renewal-process-based methods by including more cells at a similar false-positive rate. We show that our procedure works across brain regions and recording techniques, including calcium imaging and Neuropixels data. Furthermore, in illustration of the method, we show in mouse visual cortex that (1) visuomotor-mismatch and spatial location are encoded by different neuronal subpopulations and (2) optogenetic stimulation of VIP cells leads to early inhibition and subsequent disinhibition.