Thalamocortical contribution to cognitive task activity

  1. Kai Hwang  Is a corresponding author
  2. James M Shine
  3. Michael W Cole
  4. Evan Sorenson
  1. University of Iowa, United States
  2. University of Sydney, Australia
  3. Rutgers, The State University of New Jersey, United States

Abstract

Thalamocortical interaction is a ubiquitous functional motif in the mammalian brain. Previously (Hwang et al., 2021), we reported that lesions to network hubs in the human thalamus are associated with multi-domain behavioral impairments in language, memory, and executive functions. Here we show how task-evoked thalamic activity are organized to support these broad cognitive abilities. We analyzed functional MRI data from human subjects that performed 127 tasks encompassing a broad range of cognitive representations. We first investigated the spatial organization of task-evoked activity and found a basis set of activity patterns evoked to support processing needs of each task. Specifically, the anterior, medial, and posterior-medial thalamus exhibit hub-like activity profiles that are suggestive of broad functional participation. These thalamic task hubs overlapped with network hubs interlinking cortical systems. To further determine the cognitive relevance of thalamic activity and thalamocortical functional connectivity, we built a data-driven thalamocortical model to test whether thalamic activity can be used to predict cortical task activity. The thalamocortical model predicted task-specific cortical activity patterns, and outperformed comparison models built on cortical, hippocampal, and striatal regions. Simulated lesions to low-dimensional, multi-task thalamic hub regions impaired task activity prediction. This simulation result was further supported by profiles of neuropsychological impairments in human patients with focal thalamic lesions. In summary, our results suggest a general organizational principle of how the human thalamocortical system supports cognitive task activity.

Data availability

Raw data are available at OpenNeuro.org (https://openneuro.org/datasets/ds002105/ and https://openneuro.org/datasets/ds002306/). Code and data are available at (https://github.com/HwangLabNeuroCogDynamics/ThalamicTaskHubs)

The following previously published data sets were used

Article and author information

Author details

  1. Kai Hwang

    Department of Psychological and Brain Sciences, University of Iowa, Iowa City, United States
    For correspondence
    kai-hwang@uiowa.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1064-7815
  2. James M Shine

    Brain and Mind Center, University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1762-5499
  3. Michael W Cole

    Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4329-438X
  4. Evan Sorenson

    Department of Psychological and Brain Sciences, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institutes of Health (R01MH122613)

  • Kai Hwang

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

Reviewing Editor

  1. Jörn Diedrichsen, Western University, Canada

Ethics

Human subjects: All participants gave written informed consent, and the study was approved by the University of Iowa Institutional Review Board (IRB protocol #200105018).

Version history

  1. Received: June 28, 2022
  2. Preprint posted: July 1, 2022 (view preprint)
  3. Accepted: December 19, 2022
  4. Accepted Manuscript published: December 20, 2022 (version 1)
  5. Version of Record published: December 29, 2022 (version 2)

Copyright

© 2022, Hwang 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. Kai Hwang
  2. James M Shine
  3. Michael W Cole
  4. Evan Sorenson
(2022)
Thalamocortical contribution to cognitive task activity
eLife 11:e81282.
https://doi.org/10.7554/eLife.81282

Share this article

https://doi.org/10.7554/eLife.81282

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