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

  • 3,361
    views
  • 354
    downloads
  • 5
    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. Georgin Jacob
  2. Harish Katti
  3. Thomas Cherian
  4. Jhilik Das
  5. KA Zhivago
  6. SP Arun
(2021)
A naturalistic environment to study visual cognition in unrestrained monkeys
eLife 10:e63816.
https://doi.org/10.7554/eLife.63816

Share this article

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

Further reading

    1. Neuroscience
    Eleni Hackwell, Sharon R Ladyman ... David R Grattan
    Research Article

    The specific role that prolactin plays in lactational infertility, as distinct from other suckling or metabolic cues, remains unresolved. Here, deletion of the prolactin receptor (Prlr) from forebrain neurons or arcuate kisspeptin neurons resulted in failure to maintain normal lactation-induced suppression of estrous cycles. Kisspeptin immunoreactivity and pulsatile LH secretion were increased in these mice, even in the presence of ongoing suckling stimulation and lactation. GCaMP fibre photometry of arcuate kisspeptin neurons revealed that the normal episodic activity of these neurons is rapidly suppressed in pregnancy and this was maintained throughout early lactation. Deletion of Prlr from arcuate kisspeptin neurons resulted in early reactivation of episodic activity of kisspeptin neurons prior to a premature return of reproductive cycles in early lactation. These observations show dynamic variation in arcuate kisspeptin neuronal activity associated with the hormonal changes of pregnancy and lactation, and provide direct evidence that prolactin action on arcuate kisspeptin neurons is necessary for suppressing fertility during lactation in mice.

    1. Neuroscience
    Nico A Flierman, Sue Ann Koay ... Chris I De Zeeuw
    Research Article

    The role of cerebellum in controlling eye movements is well established, but its contribution to more complex forms of visual behavior has remained elusive. To study cerebellar activity during visual attention we recorded extracellular activity of dentate nucleus (DN) neurons in two non-human primates (NHPs). NHPs were trained to read the direction indicated by a peripheral visual stimulus while maintaining fixation at the center, and report the direction of the cue by performing a saccadic eye movement into the same direction following a delay. We found that single-unit DN neurons modulated spiking activity over the entire time course of the task, and that their activity often bridged temporally separated intra-trial events, yet in a heterogeneous manner. To better understand the heterogeneous relationship between task structure, behavioral performance, and neural dynamics, we constructed a behavioral, an encoding, and a decoding model. Both NHPs showed different behavioral strategies, which influenced the performance. Activity of the DN neurons reflected the unique strategies, with the direction of the visual stimulus frequently being encoded long before an upcoming saccade. Moreover, the latency of the ramping activity of DN neurons following presentation of the visual stimulus was shorter in the better performing NHP. Labeling with the retrograde tracer Cholera Toxin B in the recording location in the DN indicated that these neurons predominantly receive inputs from Purkinje cells in the D1 and D2 zones of the lateral cerebellum as well as neurons of the principal olive and medial pons, all regions known to connect with neurons in the prefrontal cortex contributing to planning of saccades. Together, our results highlight that DN neurons can dynamically modulate their activity during a visual attention task, comprising not only sensorimotor but also cognitive attentional components.