Behavioral evidence for memory replay of video episodes in the macaque

  1. Shuzhen Zuo
  2. Lei Wang
  3. Jung Han Shin
  4. Yudian Cai
  5. Sang Wan Lee
  6. Kofi Appiah
  7. Yong-di Zhou
  8. Sze Chai Kwok  Is a corresponding author
  1. East China Normal University, China
  2. Korea Advanced Institute of Science and Technology, Republic of Korea
  3. University of York, United Kingdom
  4. Shenzhen University, China

Abstract

Humans recall the past by replaying fragments of events temporally. Here, we demonstrate a similar effect in macaques. We trained six rhesus monkeys with a temporal-order judgement (TOJ) task and collected 5000 TOJ trials. In each trial, they watched a naturalistic video of about 10 s comprising two across-context clips, and after a 2-s delay, performed TOJ between two frames from the video. The data is suggestive of a non-linear, time-compressed forward memory replay mechanism in the macaque. In contrast with humans, such compression of replay is however not sophisticated enough to allow them to skip over irrelevant information by compressing the encoded video globally. We also reveal that the monkeys detect event contextual boundaries and such detection facilitates recall by an increased rate of information accumulation. Demonstration of a time-compressed, forward replay-like pattern in the macaque provides insights into the evolution of episodic memory in our lineage.

Data availability

All data is available at Dryad (doi: 10.5061/dryad.3r2280gcc).

The following data sets were generated

Article and author information

Author details

  1. Shuzhen Zuo

    School of Psychology and Cognitive Science, East China Normal University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8917-8352
  2. Lei Wang

    School of Psychology and Cognitive Science, East China Normal University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6224-6474
  3. Jung Han Shin

    Program of Brain and Cognitive Engineering, Korea Advanced Institute of Science and Technology, Daejeon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
  4. Yudian Cai

    School of Psychology and Cognitive Science, East China Normal University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Sang Wan Lee

    Department of Bio and Brain Engineering & KAIST Institute for Health Science and Technology, Korea Advanced Institute of Science and Technology, Daejeon, Republic of Korea
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6266-9613
  6. Kofi Appiah

    Computer Science, University of York, York, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Yong-di Zhou

    School of Psychology, Shenzhen University, Shenzhen, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Sze Chai Kwok

    School of Psychology and Cognitive Science, East China Normal University, Shanghai, China
    For correspondence
    sze-chai.kwok@st-hughs.oxon.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7439-1193

Funding

National Key Fundamental Research Program of China Grant (2013CB329501)

  • Yong-di Zhou

Ministry of Education of PRC Humanities and Social Sciences Research Grant (16YJC190006)

  • Sze Chai Kwok

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

Ethics

Animal experimentation: The experimental protocol was approved by the Institutional Animal Care and Use Committee (permission code: M020150902 & M020150902-2018) at East China Normal University. All experimental protocols and animal welfare adhered with the "NIH Guidelines for the Care and Use of Laboratory Animals".

Human subjects: The experimental protocol was approved by the the University Committee on Human Research Protection (permission code: HR 023-2017) at East China Normal University. . The participants provided informed consent.

Reviewing Editor

  1. Morgan Barense, University of Toronto, Canada

Version history

  1. Received: December 17, 2019
  2. Accepted: April 20, 2020
  3. Accepted Manuscript published: April 20, 2020 (version 1)
  4. Version of Record published: May 18, 2020 (version 2)

Copyright

© 2020, Zuo 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

  • 2,968
    Page views
  • 340
    Downloads
  • 6
    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. Shuzhen Zuo
  2. Lei Wang
  3. Jung Han Shin
  4. Yudian Cai
  5. Sang Wan Lee
  6. Kofi Appiah
  7. Yong-di Zhou
  8. Sze Chai Kwok
(2020)
Behavioral evidence for memory replay of video episodes in the macaque
eLife 9:e54519.
https://doi.org/10.7554/eLife.54519

Further reading

    1. Neuroscience
    Connon I Thomas, Melissa A Ryan ... Benjamin Scholl
    Research Article

    Postsynaptic mitochondria are critical for the development, plasticity, and maintenance of synaptic inputs. However, their relationship to synaptic structure and functional activity is unknown. We examined a correlative dataset from ferret visual cortex with in vivo two-photon calcium imaging of dendritic spines during visual stimulation and electron microscopy reconstructions of spine ultrastructure, investigating mitochondrial abundance near functionally and structurally characterized spines. Surprisingly, we found no correlation to structural measures of synaptic strength. Instead, we found that mitochondria are positioned near spines with orientation preferences that are dissimilar to the somatic preference. Additionally, we found that mitochondria are positioned near groups of spines with heterogeneous orientation preferences. For a subset of spines with a mitochondrion in the head or neck, synapses were larger and exhibited greater selectivity to visual stimuli than those without a mitochondrion. Our data suggest mitochondria are not necessarily positioned to support the energy needs of strong spines, but rather support the structurally and functionally diverse inputs innervating the basal dendrites of cortical neurons.

    1. Neuroscience
    Weiwei Qui, Chelsea R Hutch ... Darleen Sandoval
    Research Article

    Several discrete groups of feeding-regulated neurons in the nucleus of the solitary tract (nucleus tractus solitarius; NTS) suppress food intake, including avoidance-promoting neurons that express Cck (NTSCck cells) and distinct Lepr- and Calcr-expressing neurons (NTSLepr and NTSCalcr cells, respectively) that suppress food intake without promoting avoidance. To test potential synergies among these cell groups we manipulated multiple NTS cell populations simultaneously. We found that activating multiple sets of NTS neurons (e.g., NTSLepr plus NTSCalcr (NTSLC), or NTSLC plus NTSCck (NTSLCK)) suppressed feeding more robustly than activating single populations. While activating groups of cells that include NTSCck neurons promoted conditioned taste avoidance (CTA), NTSLC activation produced no CTA despite abrogating feeding. Thus, the ability to promote CTA formation represents a dominant effect but activating multiple non-aversive populations augments the suppression of food intake without provoking avoidance. Furthermore, silencing multiple NTS neuron groups augmented food intake and body weight to a greater extent than silencing single populations, consistent with the notion that each of these NTS neuron populations plays crucial and cumulative roles in the control of energy balance. We found that silencing NTSLCK neurons failed to blunt the weight-loss response to vertical sleeve gastrectomy (VSG) and that feeding activated many non-NTSLCK neurons, however, suggesting that as-yet undefined NTS cell types must make additional contributions to the restraint of feeding.