A naturalistic environment to study visual cognition in unrestrained monkeys

  1. Georgin Jacob
  2. Harish Katti
  3. Thomas Cherian
  4. Jhilik Das
  5. KA Zhivago
  6. SP Arun  Is a corresponding author
  1. Indian Institute of Science Bangalore, India

Abstract

Macaque monkeys are widely used to study vision. In the traditional approach, monkeys are brought into a lab to perform visual tasks while they are restrained to obtain stable eye tracking and neural recordings. Here, we describe a novel environment to study visual cognition in a more natural setting as well as other natural and social behaviors. We designed a naturalistic environment with an integrated touchscreen workstation that enables high-quality eye tracking in unrestrained monkeys. We used this environment to train monkeys on a challenging same-different task. We also show that this environment can reveal interesting novel social behaviors. As proof of concept, we show that two naïve monkeys were able to learn this complex task through a combination of socially observing trained monkeys and through solo trial-and-error. We propose that such naturalistic environments can be used to rigorously study visual cognition as well as other natural and social behaviors in freely moving monkeys.

Data availability

All data required to reproduce the results in the study are available at https://osf.io/5764q/

Article and author information

Author details

  1. Georgin Jacob

    Centre for Neuroscience, Indian Institute of Science Bangalore, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8262-0155
  2. Harish Katti

    Centre for Neuroscience, Indian Institute of Science Bangalore, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  3. Thomas Cherian

    Centre for Neuroscience, Indian Institute of Science Bangalore, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  4. Jhilik Das

    Centre for Neuroscience, Indian Institute of Science Bangalore, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  5. KA Zhivago

    Centre for Neuroscience, Indian Institute of Science Bangalore, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  6. SP Arun

    Centre for Neuroscience, Indian Institute of Science Bangalore, Bangalore, India
    For correspondence
    sparun@iisc.ac.in
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9602-5066

Funding

DBT-Wellcome Trust India Alliance (IA/S/17/1/503081)

  • SP Arun

ICMR Senior Research Fellowship

  • Thomas Cherian

UGC Senior Research Fellowship

  • Jhilik Das

DST Cognitive Science Research Initiative

  • Harish Katti

MHRD Senior Research Fellowship

  • Georgin Jacob

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 procedures were in accordance to experimental protocols approved by the Institutional Animal Ethics Committee of the Indian Institute of Science (CAF/Ethics/399/2014 & CAF/Ethics/750/2020) and by the Committee for the Purpose of Control and Supervision of Experiments on Animals, Government of India (25/61/2015-CPCSEA & V-11011(3)/15/2020-CPCSEA-DADF).

Copyright

© 2021, Jacob 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

  • 3,462
    views
  • 358
    downloads
  • 6
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

Share this article

https://doi.org/10.7554/eLife.63816

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
    Zhujun Shao, Mengya Zhang, Qing Yu
    Research Article

    When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.