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

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

  • 3,373
    views
  • 476
    downloads
  • 21
    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 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
    Cristina Gil Avila, Elisabeth S May ... Markus Ploner
    Research Article

    Chronic pain is a prevalent and debilitating condition whose neural mechanisms are incompletely understood. An imbalance of cerebral excitation and inhibition (E/I), particularly in the medial prefrontal cortex (mPFC), is believed to represent a crucial mechanism in the development and maintenance of chronic pain. Thus, identifying a non-invasive, scalable marker of E/I could provide valuable insights into the neural mechanisms of chronic pain and aid in developing clinically useful biomarkers. Recently, the aperiodic component of the electroencephalography (EEG) power spectrum has been proposed to represent a non-invasive proxy for E/I. We, therefore, assessed the aperiodic component in the mPFC of resting-state EEG recordings in 149 people with chronic pain and 115 healthy participants. We found robust evidence against differences in the aperiodic component in the mPFC between people with chronic pain and healthy participants, and no correlation between the aperiodic component and pain intensity. These findings were consistent across different subtypes of chronic pain and were similarly found in a whole-brain analysis. Their robustness was supported by preregistration and multiverse analyses across many different methodological choices. Together, our results suggest that the EEG aperiodic component does not differentiate between people with chronic pain and healthy individuals. These findings and the rigorous methodological approach can guide future studies investigating non-invasive, scalable markers of cerebral dysfunction in people with chronic pain and beyond.

    1. Neuroscience
    Ankur Sinha, Padraig Gleeson ... Robin Angus Silver
    Tools and Resources

    Data-driven models of neurons and circuits are important for understanding how the properties of membrane conductances, synapses, dendrites, and the anatomical connectivity between neurons generate the complex dynamical behaviors of brain circuits in health and disease. However, the inherent complexity of these biological processes makes the construction and reuse of biologically detailed models challenging. A wide range of tools have been developed to aid their construction and simulation, but differences in design and internal representation act as technical barriers to those who wish to use data-driven models in their research workflows. NeuroML, a model description language for computational neuroscience, was developed to address this fragmentation in modeling tools. Since its inception, NeuroML has evolved into a mature community standard that encompasses a wide range of model types and approaches in computational neuroscience. It has enabled the development of a large ecosystem of interoperable open-source software tools for the creation, visualization, validation, and simulation of data-driven models. Here, we describe how the NeuroML ecosystem can be incorporated into research workflows to simplify the construction, testing, and analysis of standardized models of neural systems, and supports the FAIR (Findability, Accessibility, Interoperability, and Reusability) principles, thus promoting open, transparent and reproducible science.