Behavioral evidence for memory replay of video episodes in the macaque
- East China Normal University, China
- Korea Advanced Institute of Science and Technology, Republic of Korea
- University of York, United Kingdom
- 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).
-
Behavioral evidence for memory replay of video episodes in macaque monkeysDryad, doi: 10.5061/dryad.3r2280gcc.
Article and author information
Author details
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.
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
-
- 3,257
- views
-
- 366
- downloads
-
- 11
- 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)
Behavioral evidence for memory replay of video episodes in the macaque
eLife 9:e54519.
https://doi.org/10.7554/eLife.54519
Further reading
-
- Neuroscience
Insulin plays a key role in metabolic homeostasis. Drosophila insulin-producing cells (IPCs) are functional analogues of mammalian pancreatic beta cells and release insulin directly into circulation. To investigate the in vivo dynamics of IPC activity, we quantified the effects of nutritional and internal state changes on IPCs using electrophysiological recordings. We found that the nutritional state strongly modulates IPC activity. IPC activity decreased with increasing periods of starvation. Refeeding flies with glucose or fructose, two nutritive sugars, significantly increased IPC activity, whereas non-nutritive sugars had no effect. In contrast to feeding, glucose perfusion did not affect IPC activity. This was reminiscent of the mammalian incretin effect, where glucose ingestion drives higher insulin release than intravenous application. Contrary to IPCs, Diuretic hormone 44-expressing neurons in the pars intercerebralis (DH44PINs) responded to glucose perfusion. Functional connectivity experiments demonstrated that these DH44PINs do not affect IPC activity, while other DH44Ns inhibit them. Hence, populations of autonomously and systemically sugar-sensing neurons work in parallel to maintain metabolic homeostasis. Accordingly, activating IPCs had a small, satiety-like effect on food-searching behavior and reduced starvation-induced hyperactivity, whereas activating DH44Ns strongly increased hyperactivity. Taken together, we demonstrate that IPCs and DH44Ns are an integral part of a modulatory network that orchestrates glucose homeostasis and adaptive behavior in response to shifts in the metabolic state.
-
- Neuroscience
The mushroom body (MB) is the center for associative learning in insects. In Drosophila, intersectional split-GAL4 drivers and electron microscopy (EM) connectomes have laid the foundation for precise interrogation of the MB neural circuits. However, investigation of many cell types upstream and downstream of the MB has been hindered due to lack of specific driver lines. Here we describe a new collection of over 800 split-GAL4 and split-LexA drivers that cover approximately 300 cell types, including sugar sensory neurons, putative nociceptive ascending neurons, olfactory and thermo-/hygro-sensory projection neurons, interneurons connected with the MB-extrinsic neurons, and various other cell types. We characterized activation phenotypes for a subset of these lines and identified a sugar sensory neuron line most suitable for reward substitution. Leveraging the thousands of confocal microscopy images associated with the collection, we analyzed neuronal morphological stereotypy and discovered that one set of mushroom body output neurons, MBON08/MBON09, exhibits striking individuality and asymmetry across animals. In conjunction with the EM connectome maps, the driver lines reported here offer a powerful resource for functional dissection of neural circuits for associative learning in adult Drosophila.
