Unsupervised changes in core object recognition behavior are predicted by neural plasticity in inferior temporal cortex

  1. Xiaoxuan Jia  Is a corresponding author
  2. Ha Hong
  3. James J DiCarlo
  1. Massachusetts Institute of Technology, United States

Abstract

Temporal continuity of object identity is a feature of natural visual input, and is potentially exploited -- in an unsupervised manner -- by the ventral visual stream to build the neural representation in inferior temporal (IT) cortex. Here we investigated whether plasticity of individual IT neurons underlies human core-object-recognition behavioral changes induced with unsupervised visual experience. We built a single-neuron plasticity model combined with a previously established IT population-to-recognition-behavior linking model to predict human learning effects. We found that our model, after constrained by neurophysiological data, largely predicted the mean direction, magnitude and time course of human performance changes. We also found a previously unreported dependency of the observed human performance change on the initial task difficulty. This result adds support to the hypothesis that tolerant core object recognition in human and non-human primates is instructed -- at least in part -- by naturally occurring unsupervised temporal contiguity experience.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files, in the most useful format (https://github.com/jiaxx/temporal_learning_paper). Datasets from previous studies (IT population dataset (Majaj et al., 2015) and IT plasticity data (Li & DiCarlo, 2010)) are also compiled in the most useful format and saved in the same github location. Original datasets for previous studies can be obtained by directly contacting the corresponding authors of those studies ((Majaj et al., 2015) and (Li & DiCarlo, 2010)). Source data files for figure 2,4,5 and 6 are provided in the github repo as well.

Article and author information

Author details

  1. Xiaoxuan Jia

    Dept. of Brain and Cognitive Sciences and McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    jxiaoxuan@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5484-9331
  2. Ha Hong

    Dept. of Brain and Cognitive Sciences and McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. James J DiCarlo

    McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institutes of Health (2-RO1-EY014970-06)

  • James J DiCarlo

Simons Foundation (SCGB [325500])

  • James J DiCarlo

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

Reviewing Editor

  1. Thomas Serre, Brown University, United States

Ethics

Human subjects: All human experiments were done in accordance with the MIT Committee on the Use of Humans as Experimental Subjects (COUHES; the protocol number is 0812003043). We used Amazon Mechanical Turk (MTurk), an online platform where subjects can participate in non-profit psychophysical experiments for payment based on the duration of the task. In the description of each task, it is clearly stated that participation is voluntary and subjects may quit at any time. Subjects can preview each task before agreeing to participate. Subjects will also be informed that anonymity is assured and the researchers will not receive any personal information. MTurk requires subjects to read task descriptions before agreeing to participate. If subjects successfully complete the task, they anonymously receive payment through the MTurk interface.

Version history

  1. Received: July 8, 2020
  2. Accepted: June 10, 2021
  3. Accepted Manuscript published: June 11, 2021 (version 1)
  4. Accepted Manuscript updated: June 17, 2021 (version 2)
  5. Version of Record published: July 30, 2021 (version 3)

Copyright

© 2021, Jia 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

  • 1,651
    Page views
  • 263
    Downloads
  • 7
    Citations

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

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. Xiaoxuan Jia
  2. Ha Hong
  3. James J DiCarlo
(2021)
Unsupervised changes in core object recognition behavior are predicted by neural plasticity in inferior temporal cortex
eLife 10:e60830.
https://doi.org/10.7554/eLife.60830

Share this article

https://doi.org/10.7554/eLife.60830

Further reading

    1. Developmental Biology
    2. Neuroscience
    Tariq Zaman, Daniel Vogt ... Michael R Williams
    Research Article

    The cell-type-specific expression of ligand/receptor and cell-adhesion molecules is a fundamental mechanism through which neurons regulate connectivity. Here, we determine a functional relevance of the long-established mutually exclusive expression of the receptor tyrosine kinase Kit and the trans-membrane protein Kit Ligand by discrete populations of neurons in the mammalian brain. Kit is enriched in molecular layer interneurons (MLIs) of the cerebellar cortex (i.e., stellate and basket cells), while cerebellar Kit Ligand is selectively expressed by a target of their inhibition, Purkinje cells (PCs). By in vivo genetic manipulation spanning embryonic development through adulthood, we demonstrate that PC Kit Ligand and MLI Kit are required for, and capable of driving changes in, the inhibition of PCs. Collectively, these works in mice demonstrate that the Kit Ligand/Kit receptor dyad sustains mammalian central synapse function and suggest a rationale for the affiliation of Kit mutation with neurodevelopmental disorders.

    1. Neuroscience
    Hideo Hagihara, Hirotaka Shoji ... Tsuyoshi Miyakawa
    Research Article

    Increased levels of lactate, an end-product of glycolysis, have been proposed as a potential surrogate marker for metabolic changes during neuronal excitation. These changes in lactate levels can result in decreased brain pH, which has been implicated in patients with various neuropsychiatric disorders. We previously demonstrated that such alterations are commonly observed in five mouse models of schizophrenia, bipolar disorder, and autism, suggesting a shared endophenotype among these disorders rather than mere artifacts due to medications or agonal state. However, there is still limited research on this phenomenon in animal models, leaving its generality across other disease animal models uncertain. Moreover, the association between changes in brain lactate levels and specific behavioral abnormalities remains unclear. To address these gaps, the International Brain pH Project Consortium investigated brain pH and lactate levels in 109 strains/conditions of 2294 animals with genetic and other experimental manipulations relevant to neuropsychiatric disorders. Systematic analysis revealed that decreased brain pH and increased lactate levels were common features observed in multiple models of depression, epilepsy, Alzheimer’s disease, and some additional schizophrenia models. While certain autism models also exhibited decreased pH and increased lactate levels, others showed the opposite pattern, potentially reflecting subpopulations within the autism spectrum. Furthermore, utilizing large-scale behavioral test battery, a multivariate cross-validated prediction analysis demonstrated that poor working memory performance was predominantly associated with increased brain lactate levels. Importantly, this association was confirmed in an independent cohort of animal models. Collectively, these findings suggest that altered brain pH and lactate levels, which could be attributed to dysregulated excitation/inhibition balance, may serve as transdiagnostic endophenotypes of debilitating neuropsychiatric disorders characterized by cognitive impairment, irrespective of their beneficial or detrimental nature.