The role of higher order thalamus during learning and correct performance in goal-directed behavior

  1. Danilo La Terra
  2. Marius Rosier
  3. Ann-Sofie Bjerre
  4. Rei Masuda
  5. Tomás J Ryan
  6. Lucy Maree Palmer  Is a corresponding author
  1. University of Melbourne, Australia
  2. Trinity College Dublin, Ireland

Abstract

The thalamus is a gateway to the cortex. Cortical encoding of complex behavior can therefore only be understood by considering the thalamic processing of sensory and internally-generated information. Here, we use two-photon Ca2+ imaging and optogenetics to investigate the role of axonal projections from the posteromedial nucleus of the thalamus (POm) to the forepaw area of the mouse primary somatosensory cortex (forepaw S1). By recording the activity of POm axonal projections within forepaw S1 during expert and chance performance in two tactile goal-directed tasks, we demonstrate that POm axons increase activity in the response and, to a lesser extent, reward epochs specifically during correct HIT performance. When performing at chance level during learning of a new behavior, POm axonal activity was decreased to naïve rates and did not correlate with task performance. However, once evoked, the Ca2+ transients were larger than during expert performance, suggesting POm input to S1 differentially encodes chance and expert performance. Furthermore, the POm influences goal-directed behavior, as photo-inactivation of archaerhodopsin-expressing neurons in the POm decreased the learning rate and overall success in the behavioral task. Taken together, these findings expand the known roles of the higher-thalamic nuclei, illustrating the POm encodes and influences correct action during learning and performance in a sensory-based goal-directed behavior.

Data availability

The source code for the behavioral system can be found online at https://github.com/palmerlab/behaviour_box, as well as additional documentation at https://palmerlab.github.io. Calcium imaging data is available on Dryad doi:10.5061/dryad.1rn8pk0wb.

The following data sets were generated

Article and author information

Author details

  1. Danilo La Terra

    Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  2. Marius Rosier

    Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Ann-Sofie Bjerre

    Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  4. Rei Masuda

    Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  5. Tomás J Ryan

    Trinity College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  6. Lucy Maree Palmer

    Florey Institute of Neuroscience and Mental Health, University of Melbourne, Melbourne, Australia
    For correspondence
    lucy.palmer@florey.edu.au
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3676-657X

Funding

National Health and Medical Research Council (APP1086082)

  • Lucy Maree Palmer

National Health and Medical Research Council (APP1063533)

  • Lucy Maree Palmer

National Health and Medical Research Council (APP1085708)

  • Lucy Maree Palmer

Australian Respiratory Council (DP160103047)

  • Lucy Maree Palmer

Sylvia and Charles Viertel Charitable Foundation

  • Lucy Maree Palmer

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

Ethics

Animal experimentation: All procedures were approved by the Florey Institute of Neuroscience and Mental Health Animal Care and Ethics Committee and followed the guidelines of the Australian Code of Practice for the Care and Use of Animals for Scientific Purpose

Reviewing Editor

  1. Ishmail Abdus-Saboor, Columbia University, United States

Publication history

  1. Preprint posted: July 6, 2020 (view preprint)
  2. Received: January 18, 2022
  3. Accepted: March 2, 2022
  4. Accepted Manuscript published: March 8, 2022 (version 1)
  5. Accepted Manuscript updated: March 9, 2022 (version 2)
  6. Version of Record published: March 21, 2022 (version 3)

Copyright

© 2022, La Terra et al.

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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  1. Danilo La Terra
  2. Marius Rosier
  3. Ann-Sofie Bjerre
  4. Rei Masuda
  5. Tomás J Ryan
  6. Lucy Maree Palmer
(2022)
The role of higher order thalamus during learning and correct performance in goal-directed behavior
eLife 11:e77177.
https://doi.org/10.7554/eLife.77177

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