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

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.

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

  • 4,112
    views
  • 428
    downloads
  • 51
    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. Ma Feilong
  2. J Swaroop Guntupalli
  3. James V Haxby
(2021)
The neural basis of intelligence in fine-grained cortical topographies
eLife 10:e64058.
https://doi.org/10.7554/eLife.64058

Share this article

https://doi.org/10.7554/eLife.64058

Further reading

    1. Neuroscience
    Yiting Li, Wenqu Yin ... Baoming Li
    Research Article

    Time estimation is an essential prerequisite underlying various cognitive functions. Previous studies identified ‘sequential firing’ and ‘activity ramps’ as the primary neuron activity patterns in the medial frontal cortex (mPFC) that could convey information regarding time. However, the relationship between these patterns and the timing behavior has not been fully understood. In this study, we utilized in vivo calcium imaging of mPFC in rats performing a timing task. We observed cells that showed selective activation at trial start, end, or during the timing interval. By aligning long-term time-lapse datasets, we discovered that sequential patterns of time coding were stable over weeks, while cells coding for trial start or end showed constant dynamism. Furthermore, with a novel behavior design that allowed the animal to determine individual trial interval, we were able to demonstrate that real-time adjustment in the sequence procession speed closely tracked the trial-to-trial interval variations. And errors in the rats’ timing behavior can be primarily attributed to the premature ending of the time sequence. Together, our data suggest that sequential activity maybe a stable neural substrate that represents time under physiological conditions. Furthermore, our results imply the existence of a unique cell type in the mPFC that participates in the time-related sequences. Future characterization of this cell type could provide important insights in the neural mechanism of timing and related cognitive functions.

    1. Neuroscience
    Bhanu Shrestha, Jiun Sang ... Youngseok Lee
    Research Article

    Sour taste, which is elicited by low pH, may serve to help animals distinguish appetitive from potentially harmful food sources. In all species studied to date, the attractiveness of oral acids is contingent on concentration. Many carboxylic acids are attractive at ecologically relevant concentrations but become aversive beyond some maximal concentration. Recent work found that Drosophila ionotropic receptors IR25a and IR76b expressed by sweet-responsive gustatory receptor neurons (GRNs) in the labellum, a peripheral gustatory organ, mediate appetitive feeding behaviors toward dilute carboxylic acids. Here, we disclose the existence of pharyngeal sensors in Drosophila melanogaster that detect ingested carboxylic acids and are also involved in the appetitive responses to carboxylic acids. These pharyngeal sensors rely on IR51b, IR94a, and IR94h, together with IR25a and IR76b, to drive responses to carboxylic acids. We then demonstrate that optogenetic activation of either Ir94a+ or Ir94h+ GRNs promotes an appetitive feeding response, confirming their contributions to appetitive feeding behavior. Our discovery of internal pharyngeal sour taste receptors opens up new avenues for investigating the internal sensation of tastants in insects.