1. Neuroscience
Download icon

The neural basis of intelligence in fine-grained cortical topographies

  1. Ma Feilong
  2. J Swaroop Guntupalli
  3. James V Haxby  Is a corresponding author
  1. Dartmouth College, United States
Research Article
  • Cited 1
  • Views 2,827
  • Annotations
Cite this article as: eLife 2021;10:e64058 doi: 10.7554/eLife.64058

Abstract

Intelligent thought is the product of efficient neural information processing, which is embedded in fine-grained, topographically-organized population responses and supported by fine-grained patterns of connectivity among cortical fields. Previous work on the neural basis of intelligence, however, has focused on coarse-grained features of brain anatomy and function, because cortical topographies are highly idiosyncratic at a finer scale, obscuring individual differences in fine-grained connectivity patterns. We used a computational algorithm, hyperalignment, to resolve these topographic idiosyncrasies, and found that predictions of general intelligence based on fine-grained (vertex-by-vertex) connectivity patterns were markedly stronger than predictions based on coarse-grained (region-by-region) patterns. Intelligence was best predicted by fine-grained connectivity in the default and frontoparietal cortical systems, both of which are associated with self-generated thought. Previous work overlooked fine-grained architecture because existing methods couldn't resolve idiosyncratic topographies, preventing investigation where the keys to the neural basis of intelligence are more likely to be found.

Data availability

Data used in the preparation of this work were obtained from the MGH-USC Human Connectome Project (HCP) database (https://ida.loni.usc.edu/login.jsp). The HCP project (Principal Investigators : Bruce Rosen, M.D., Ph.D., Martinos Center at Massachusetts General Hospital; Arthur W. Toga, Ph.D., University of Southern California, Van J. Weeden, MD, Martinos Center at Massachusetts General Hospital) is supported by the National Institute of Dental and Craniofacial Research (NIDCR), the National Institute of Mental Health (NIMH) and the National Institute of Neurological Disorders and Stroke (NINDS). Collectively, the HCP is the result of efforts of co-investigators from the University of Southern California, Martinos Center for Biomedical Imaging at Massachusetts General Hospital (MGH), Washington University, and the University of Minnesota.

The following previously published data sets were used

Article and author information

Author details

  1. Ma Feilong

    Psychological and Brain Sciences, Dartmouth College, Hanover, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6838-3971
  2. J Swaroop Guntupalli

    Psychological and Brain Sciences, Dartmouth College, Hanover, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0677-5590
  3. James V Haxby

    Psychological and Brain Sciences, Dartmouth College, Hanover, United States
    For correspondence
    james.v.haxby@dartmouth.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6558-3118

Funding

National Science Foundation (1607845)

  • James V Haxby

National Science Foundation (1835200)

  • James V Haxby

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

Ethics

Human subjects: Human research participants in the Human Connectome Project gave written informed consent for their participation in accordance with guidelines at participating institutions.

Reviewing Editor

  1. Thomas Yeo, National University of Singapore, Singapore

Publication history

  1. Received: October 15, 2020
  2. Accepted: March 5, 2021
  3. Accepted Manuscript published: March 8, 2021 (version 1)
  4. Version of Record published: March 25, 2021 (version 2)

Copyright

© 2021, Feilong 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

  • 2,827
    Page views
  • 262
    Downloads
  • 1
    Citations

Article citation count generated by polling the highest count across the following sources: PubMed Central, Crossref, Scopus.

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)

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

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

Further reading

    1. Neuroscience
    Gordon H Petty et al.
    Research Article

    Neocortical sensory areas have associated primary and secondary thalamic nuclei. While primary nuclei transmit sensory information to cortex, secondary nuclei remain poorly understood. We recorded juxtasomally from secondary somatosensory (POm) and visual (LP) nuclei of awake mice while tracking whisking and pupil size. POm activity correlated with whisking, but not precise whisker kinematics. This coarse movement modulation persisted after facial paralysis and thus was not due to sensory reafference. This phenomenon also continued during optogenetic silencing of somatosensory and motor cortex and after lesion of superior colliculus, ruling out a motor efference copy mechanism. Whisking and pupil dilation were strongly correlated, possibly reflecting arousal. Indeed LP, which is not part of the whisker system, tracked whisking equally well, further indicating that POm activity does not encode whisker movement per se. The semblance of movement-related activity is likely instead a global effect of arousal on both nuclei. We conclude that secondary thalamus monitors behavioral state, rather than movement, and may exist to alter cortical activity accordingly.

    1. Neuroscience
    Jorrit S Montijn et al.
    Tools and Resources Updated

    Neurophysiological studies depend on a reliable quantification of whether and when a neuron responds to stimulation. Simple methods to determine responsiveness require arbitrary parameter choices, such as binning size, while more advanced model-based methods require fitting and hyperparameter tuning. These parameter choices can change the results, which invites bad statistical practice and reduces the replicability. New recording techniques that yield increasingly large numbers of cells would benefit from a test for cell-inclusion that requires no manual curation. Here, we present the parameter-free ZETA-test, which outperforms t-tests, ANOVAs, and renewal-process-based methods by including more cells at a similar false-positive rate. We show that our procedure works across brain regions and recording techniques, including calcium imaging and Neuropixels data. Furthermore, in illustration of the method, we show in mouse visual cortex that (1) visuomotor-mismatch and spatial location are encoded by different neuronal subpopulations and (2) optogenetic stimulation of VIP cells leads to early inhibition and subsequent disinhibition.