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.

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

  • 3,526
    views
  • 488
    downloads
  • 25
    citations

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

Download links

Share this article

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

Further reading

    1. Evolutionary Biology
    2. Neuroscience
    Jenny Chen, Phoebe R Richardson ... Hopi E Hoekstra
    Research Article

    Genetic variation is known to contribute to the variation of animal social behavior, but the molecular mechanisms that lead to behavioral differences are still not fully understood. Here, we investigate the cellular evolution of the hypothalamic preoptic area (POA), a brain region that plays a critical role in social behavior, across two sister species of deer mice (Peromyscus maniculatus and P. polionotus) with divergent social systems. These two species exhibit large differences in mating and parental care behavior across species and sex. Using single-nucleus RNA-sequencing, we build a cellular atlas of the POA for males and females of both Peromyscus species. We identify four cell types that are differentially abundant across species, two of which may account for species differences in parental care behavior based on known functions of these cell types. Our data further implicate two sex-biased cell types to be important for the evolution of sex-specific behavior. Finally, we show a remarkable reduction of sex-biased gene expression in P. polionotus, a monogamous species that also exhibits reduced sexual dimorphism in parental care behavior. Our POA atlas is a powerful resource to investigate how molecular neuronal traits may be evolving to give rise to innate differences in social behavior across animal species.

    1. Neuroscience
    Yisi Liu, Pu Wang ... Hongwei Zhou
    Short Report

    The increasing use of tissue clearing techniques underscores the urgent need for cost-effective and simplified deep imaging methods. While traditional inverted confocal microscopes excel in high-resolution imaging of tissue sections and cultured cells, they face limitations in deep imaging of cleared tissues due to refractive index mismatches between the immersion media of objectives and sample container. To overcome these challenges, the RIM-Deep was developed to significantly improve deep imaging capabilities without compromising the normal function of the confocal microscope. This system facilitates deep immunofluorescence imaging of the prefrontal cortex in cleared macaque tissue, extending imaging depth from 2 mm to 5 mm. Applied to an intact and cleared Thy1-EGFP mouse brain, the system allowed for clear axonal visualization at high imaging depth. Moreover, this advancement enables large-scale, deep 3D imaging of intact tissues. In principle, this concept can be extended to any imaging modality, including existing inverted wide-field, confocal, and two-photon microscopy. This would significantly upgrade traditional laboratory configurations and facilitate the study of connectomes in the brain and other tissues.