Attention-related modulation of caudate neurons depends on superior colliculus activity

  1. James P Herman  Is a corresponding author
  2. Fabrice Arcizet
  3. Richard J Krauzlis
  1. National Eye Institute, United States
  2. Institut de la Vision, France

Abstract

Recent work has implicated the primate basal ganglia in visual perception and attention, in addition to their traditional role in motor control. The basal ganglia, especially the caudate nucleus 'head' (CDh) of the striatum, receive indirect anatomical connections from the superior colliculus, a midbrain structure that is known to play a crucial role in the control of visual attention. To test the possible functional relationship between these subcortical structures, we recorded CDh neuronal activity of macaque monkeys before and during unilateral superior colliculus (SC) inactivation in a spatial attention task. SC inactivation significantly altered the attention-related modulation of CDh neurons and strongly impaired the classification of task epochs based on CDh activity. Only inactivation of SC on the same side of the brain as recorded CDh neurons, not the opposite side, had these effects. These results demonstrate a novel interaction between SC activity and attention-related visual processing in the basal ganglia.

Data availability

Data for the main figures are available via Dryad (doi:10.5061/dryad.xd2547dcx).

The following data sets were generated

Article and author information

Author details

  1. James P Herman

    Laboratory of Sensorimotor Research, National Eye Institute, Bethesda, United States
    For correspondence
    james.herman@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6916-2807
  2. Fabrice Arcizet

    Visual information processing, Institut de la Vision, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Richard J Krauzlis

    Laboratory of Sensorimotor Research, National Eye Institute, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Eye Institute (1ZIAEY000511)

  • Richard J Krauzlis

European Research Council SYNERGY Grant scheme (610110)

  • Fabrice Arcizet

RHU LIGHT4DEAF (ANR-15-RHU-0001)

  • Fabrice Arcizet

LABEX LIFESENSES (ANR-10-LABX-65)

  • Fabrice Arcizet

IHU FOReSIGHT (ANR-15-RHU-0001)

  • Fabrice Arcizet

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

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Ethics

Animal experimentation: All experimental protocols (#NEI-649) were approved by the National Eye Institute Animal Care and Use Committee, and all procedures were performed in accordance with the United States Public Health Service policy on the humane care and use of laboratory animals.

Version history

  1. Received: November 27, 2019
  2. Accepted: August 26, 2020
  3. Accepted Manuscript published: September 17, 2020 (version 1)
  4. Version of Record published: October 8, 2020 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. James P Herman
  2. Fabrice Arcizet
  3. Richard J Krauzlis
(2020)
Attention-related modulation of caudate neurons depends on superior colliculus activity
eLife 9:e53998.
https://doi.org/10.7554/eLife.53998

Share this article

https://doi.org/10.7554/eLife.53998

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