Inconsistencies between human and macaque lesion data can be resolved with a stimulus-computable model of the ventral visual stream

  1. Tyler Bonnen  Is a corresponding author
  2. Mark AG Eldridge  Is a corresponding author
  1. Stanford University, United States
  2. National Institute of Mental Health, United States

Abstract

Decades of neuroscientific research has sought to understand medial temporal lobe (MTL) involvement in perception. Apparent inconsistencies in the literature have led to competing interpretations of the available evidence; critically, findings from human participants with naturally occurring MTL damage appear to be inconsistent with findings from monkeys with surgical lesions. Here we leverage a 'stimulus-computable' proxy for the primate ventral visual stream (VVS), which enables us to formally evaluate perceptual demands across stimulus sets, experiments, and species. With this approach, we analyze a series of experiments administered to monkeys with surgical, bilateral damage to perirhinal cortex (PRC), a MTL structure implicated in visual object perception. Across experiments, PRC-lesioned subjects showed no impairment on perceptual tasks; this originally led us (Eldridge et al., 2018) to conclude that PRC is not involved in perception. Here we find that a 'VVS-like' model predicts both PRC-intact and -lesioned choice behaviors, suggesting that a linear readout of the VVS should be sufficient for performance on these tasks. Evaluating these data alongside findings from human experiments, we suggest that results from Eldridge et al., 2018 alone can not be used as evidence against PRC involvement in perception. These data suggest that the experimental findings from human and non-human primate literature are consistent, and apparent discrepancies between species was due to reliance on informal accounts of perceptual processing.

Data availability

All scripts used for analysis and visualization can be accessed via github at https://github.com/tzler/eldridge_reanalysisAll stimuli and behavioral data used in these analyses can be downloaded via Dryad

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Tyler Bonnen

    Stanford University, Stanford, United States
    For correspondence
    bonnen@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8709-1651
  2. Mark AG Eldridge

    National Institute of Mental Health, Bethesda, United States
    For correspondence
    mark.eldridge@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4292-6832

Funding

National Institute of Mental Health (ZIAMH002032)

  • Tyler Bonnen

National Institute of Neurological Disorders and Stroke (F99NS125816)

  • Tyler Bonnen

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

Reviewing Editor

  1. Lila Davachi, Columbia University, United States

Ethics

Animal experimentation: All experimental procedures conformed to the Institute of Medicine Guide for the Care and Use of Laboratory Animals and were performed under an Animal Study Protocol approved by the Animal Care and Use Committee of the National Institute of Mental Health, covered by project number: MH002032.

Version history

  1. Preprint posted: September 15, 2022 (view preprint)
  2. Received: November 1, 2022
  3. Accepted: June 5, 2023
  4. Accepted Manuscript published: June 6, 2023 (version 1)
  5. Version of Record published: June 29, 2023 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Tyler Bonnen
  2. Mark AG Eldridge
(2023)
Inconsistencies between human and macaque lesion data can be resolved with a stimulus-computable model of the ventral visual stream
eLife 12:e84357.
https://doi.org/10.7554/eLife.84357

Share this article

https://doi.org/10.7554/eLife.84357

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