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 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 J. Ryan

    School of Biochemistry and Immunology, 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.

Reviewing Editor

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

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

Version 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.

Metrics

  • 2,946
    views
  • 444
    downloads
  • 6
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Danilo La Terra
  2. Marius Rosier
  3. Ann-Sofie Bjerre
  4. Rei Masuda
  5. Tomás J 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

Share this article

https://doi.org/10.7554/eLife.77177

Further reading

    1. Neuroscience
    Juan Jose Rodriguez Gotor, Kashif Mahfooz ... John F Wesseling
    Research Article

    Vesicles within presynaptic terminals are thought to be segregated into a variety of readily releasable and reserve pools. The nature of the pools and trafficking between them is not well understood, but pools that are slow to mobilize when synapses are active are often assumed to feed pools that are mobilized more quickly, in a series. However, electrophysiological studies of synaptic transmission have suggested instead a parallel organization where vesicles within slowly and quickly mobilized reserve pools would separately feed independent reluctant- and fast-releasing subdivisions of the readily releasable pool. Here, we use FM-dyes to confirm the existence of multiple reserve pools at hippocampal synapses and a parallel organization that prevents intermixing between the pools, even when stimulation is intense enough to drive exocytosis at the maximum rate. The experiments additionally demonstrate extensive heterogeneity among synapses in the relative sizes of the slowly and quickly mobilized reserve pools, which suggests equivalent heterogeneity in the numbers of reluctant and fast-releasing readily releasable vesicles that may be relevant for understanding information processing and storage.

    1. Evolutionary Biology
    2. Neuroscience
    Daniel Thiel, Luis Alfonso Yañez Guerra ... Gáspár Jékely
    Research Article

    Neuropeptides are ancient signaling molecules in animals but only few peptide receptors are known outside bilaterians. Cnidarians possess a large number of G protein-coupled receptors (GPCRs) – the most common receptors of bilaterian neuropeptides – but most of these remain orphan with no known ligands. We searched for neuropeptides in the sea anemone Nematostella vectensis and created a library of 64 peptides derived from 33 precursors. In a large-scale pharmacological screen with these peptides and 161 N. vectensis GPCRs, we identified 31 receptors specifically activated by 1 to 3 of 14 peptides. Mapping GPCR and neuropeptide expression to single-cell sequencing data revealed how cnidarian tissues are extensively connected by multilayer peptidergic networks. Phylogenetic analysis identified no direct orthology to bilaterian peptidergic systems and supports the independent expansion of neuropeptide signaling in cnidarians from a few ancestral peptide-receptor pairs.