Gaze patterns and brain activations in humans and marmosets in the Frith-Happé theory-of-mind animation task

Abstract

Theory of Mind (ToM) refers to the cognitive ability to attribute mental states to other individuals. This ability extends even to the attribution of mental states to animations featuring simple geometric shapes, such as the Frith-Happé animations in which two triangles move either purposelessly (Random condition), exhibit purely physical movement (Goal-directed condition), or move as if one triangle is reacting to the other triangle's mental states (ToM condition). While this capacity in humans has been thoroughly established, research on nonhuman primates has yielded inconsistent results. This study explored how marmosets (Callithrix jacchus), a highly social primate species, process Frith-Happé animations by examining gaze patterns and brain activations of marmosets and humans as they observed these animations. We revealed that both marmosets and humans exhibited longer fixations on one of the triangles in ToM animations, compared to other conditions. However, we did not observe the same pattern of longer overall fixation duration on the ToM animations in marmosets as identified in humans. Furthermore, our findings reveal that both species activated extensive and comparable brain networks when viewing ToM versus Random animations, suggesting that marmosets differentiate between these scenarios similarly to humans. While marmosets did not mimic human overall fixation patterns, their gaze behavior and neural activations indicate a distinction between ToM and non-ToM scenarios. This study expands our understanding of nonhuman primate cognitive abilities, shedding light on potential similarities and differences in ToM processing between marmosets and humans.

Data availability

All fMRI and eye tracking data generated and analysed as well as the scripts used have been deposited in Github and the link has been provided in the manuscript. Here the link: https://github.com/audreydureux/Theory-of-mind_Human_Marmosets_Paper

Article and author information

Author details

  1. Audrey Dureux

    Centre for Functional and Metabolic Mapping, University of Western Ontario, London, Canada
    For correspondence
    audrey.dureux@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1687-8347
  2. Alessandro Zanini

    Centre for Functional and Metabolic Mapping, University of Western Ontario, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Janahan Selvanayagam

    Centre for Functional and Metabolic Mapping, University of Western Ontario, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3708-8742
  4. Ravi S Menon

    Centre for Functional and Metabolic Mapping, University of Western Ontario, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Stefan Everling

    Centre for Functional and Metabolic Mapping, University of Western Ontario, London, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9714-9757

Funding

Canadian Institutes of Health Research (FRN 148365)

  • Stefan Everling

Canada First Research Excellence Fund

  • Stefan Everling

Natural Sciences and Engineering Research Council of Canada (Discovery grant)

  • Stefan Everling

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

Ethics

Animal experimentation: All experimental methods described were performed in accordance with the guidelines of the Canadian Council of Animal Care policy and a protocol approved by the Animal Care Committee of the University of Western Ontario Council on Animal Care (#2021-111). Animals were monitoring during the acquisition sessions by a veterinary technician.

Human subjects: This study was approved by the Ethics Committee of the University of Western Ontario and subjects were informed about the experimental procedures and provided informed written consent.

Copyright

© 2023, Dureux 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

  • 1,026
    views
  • 147
    downloads
  • 8
    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. Audrey Dureux
  2. Alessandro Zanini
  3. Janahan Selvanayagam
  4. Ravi S Menon
  5. Stefan Everling
(2023)
Gaze patterns and brain activations in humans and marmosets in the Frith-Happé theory-of-mind animation task
eLife 12:e86327.
https://doi.org/10.7554/eLife.86327

Share this article

https://doi.org/10.7554/eLife.86327

Further reading

    1. Neuroscience
    Franziska Auer, Katherine Nardone ... David Schoppik
    Research Article

    Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.

    1. Neuroscience
    Gáspár Oláh, Rajmund Lákovics ... Gábor Tamás
    Research Article

    Human-specific cognitive abilities depend on information processing in the cerebral cortex, where the neurons are significantly larger and their processes longer and sparser compared to rodents. We found that, in synaptically connected layer 2/3 pyramidal cells (L2/3 PCs), the delay in signal propagation from soma to soma is similar in humans and rodents. To compensate for the longer processes of neurons, membrane potential changes in human axons and/or dendrites must propagate faster. Axonal and dendritic recordings show that the propagation speed of action potentials (APs) is similar in human and rat axons, but the forward propagation of excitatory postsynaptic potentials (EPSPs) and the backward propagation of APs are 26 and 47% faster in human dendrites, respectively. Experimentally-based detailed biophysical models have shown that the key factor responsible for the accelerated EPSP propagation in human cortical dendrites is the large conductance load imposed at the soma by the large basal dendritic tree. Additionally, larger dendritic diameters and differences in cable and ion channel properties in humans contribute to enhanced signal propagation. Our integrative experimental and modeling study provides new insights into the scaling rules that help maintain information processing speed albeit the large and sparse neurons in the human cortex.