Atypical cognitive training-induced learning and brain plasticity and their relation to insistence on sameness in children with autism

  1. Jin Liu  Is a corresponding author
  2. Hyesang Chang
  3. Daniel Arthur Abrams
  4. Julia Boram Kang
  5. Chen Lang
  6. Miriam Rosenberg-Lee
  7. Vinod Menon  Is a corresponding author
  1. Stanford University, United States
  2. Santa Clara University, United States
  3. Rutgers, The State University of New Jersey, United States

Abstract

Children with autism spectrum disorders (ASD) often display atypical learning styles, however little is known regarding learning-related brain plasticity and its relation to clinical phenotypic features. Here, we investigate cognitive learning and neural plasticity using functional brain imaging and a novel numerical problem-solving training protocol. Children with ASD showed comparable learning relative to typically developing children but were less likely to shift from rule-based to memory-based strategy. While learning gains in typically developing children were associated with greater plasticity of neural representations in the medial temporal lobe and intraparietal sulcus, learning in children with ASD was associated with more stable neural representations. Crucially, the relation between learning and plasticity of neural representations was moderated by insistence on sameness, a core phenotypic feature of ASD. Our study uncovers atypical cognitive and neural mechanisms underlying learning in children with ASD, and informs pedagogical strategies for nurturing cognitive abilities in childhood autism.

Data availability

The training sets have been provided in Supplementary Materials. All data that support the findings of this study will be available through the NIHM Data Archive (NDA)

Article and author information

Author details

  1. Jin Liu

    Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, United States
    For correspondence
    jinliu5@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4343-2623
  2. Hyesang Chang

    Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2231-1112
  3. Daniel Arthur Abrams

    Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1255-1200
  4. Julia Boram Kang

    Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Chen Lang

    Department of Psychology, Santa Clara University, Santa Clara, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Miriam Rosenberg-Lee

    Department of Psychology, Rutgers, The State University of New Jersey, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Vinod Menon

    Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, United States
    For correspondence
    menon@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institutes of Health (HD059205)

  • Vinod Menon

National Institutes of Health (MH084164)

  • Vinod Menon

National Institutes of Health (HD094623)

  • Vinod Menon

Stanford Maternal and Child Health Research Institute

  • Jin Liu

Stanford Maternal and Child Health Research Institute

  • Hyesang Chang

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

Reviewing Editor

  1. Jason P Lerch, University of Oxford, United Kingdom

Ethics

Human subjects: The informed written consent was obtained from the legal guardian of each child and all study protocols were approved by the Stanford University Review Board (IRB-11849). All participants were volunteers and were treated in accordance with the American Psychological Association 'Ethical Principles of Psychologists and Code of Conduct'.

Version history

  1. Received: January 8, 2023
  2. Preprint posted: January 26, 2023 (view preprint)
  3. Accepted: August 2, 2023
  4. Accepted Manuscript published: August 3, 2023 (version 1)
  5. Version of Record published: October 4, 2023 (version 2)

Copyright

© 2023, Liu 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

  • 1,060
    views
  • 182
    downloads
  • 2
    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. Jin Liu
  2. Hyesang Chang
  3. Daniel Arthur Abrams
  4. Julia Boram Kang
  5. Chen Lang
  6. Miriam Rosenberg-Lee
  7. Vinod Menon
(2023)
Atypical cognitive training-induced learning and brain plasticity and their relation to insistence on sameness in children with autism
eLife 12:e86035.
https://doi.org/10.7554/eLife.86035

Share this article

https://doi.org/10.7554/eLife.86035

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.