Active information maintenance in working memory by a sensory cortex
- CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, China
- Zhejiang University School of Medicine, China
- Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Spain
Abstract
Working memory is a critical brain function for maintaining and manipulating information over delay periods of seconds. It is debated whether delay-period neural activity in sensory regions is important for the active maintenance of information during the delay period. Here, we tackle this question by examining the anterior piriform cortex (APC), an olfactory sensory cortex, in head-fixed mice performing several olfactory working memory tasks. Active information maintenance is necessary in these tasks, especially in a dual-task paradigm in which mice are required to perform another distracting task while actively maintaining information during the delay period. Optogenetic suppression of neuronal activity in APC during the delay period impaired performance in all the tasks. Furthermore, electrophysiological recordings revealed that APC neuronal populations encoded odor information in the delay period even with an intervening distracting task. Thus, delay activity in APC is important for active information maintenance in olfactory working memory.
Data availability
All data generated or analyzed during this study are available on Dryad under doi:10.5061/dryad.dt5h4m1. Source data files have been provided for Figures 1-4.
-
Data from: Active information maintenance in working memory by a sensory cortexDryad Digital Repository, doi:10.5061/dryad.dt5h4m1.
Article and author information
Author details
Funding
National Natural Science Foundation of China (Distinguished Young Scholars of China (31525010))
- Chengyu T Li
Chinese Academy of Agricultural Sciences (Key Research Program of Frontier Sciences QYZDB-SSW-SMC009)
- Chengyu T Li
Chinese Academy of Agricultural Sciences (Instrument Developing Project YZ201540)
- Chengyu T Li
Shanghai Science and Technology Commission (No.15JC1400102)
- Chengyu T Li
Spanish Ministry of Science
- Albert Compte
Innovation and Universities and the European Regional Development Fund (BFU2015-65318-R)
- Albert Compte
CERCA Programme/Generalitat de Catalunya
- Albert Compte
Shanghai Municipal Science and Technology Major Project (2018SHZDZX05)
- Chengyu T Li
National Natural Science Foundation of China (General Program 31471049)
- Chengyu T Li
Shanghei Science and Technology Commission (16JC1400101)
- Chengyu T Li
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 experiments were performed in compliance with the animal care standards set by the U.S. National Institutes of Health and have been approved by the Institutional Animal Care and Use Committee of the Institute of Neuroscience, Chinese Academy of Sciences (ION-2018010).
Copyright
© 2019, Zhang 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
-
- 5,367
- views
-
- 833
- downloads
-
- 47
- 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)
Active information maintenance in working memory by a sensory cortex
eLife 8:e43191.
https://doi.org/10.7554/eLife.43191
Further reading
-
- Neuroscience
Detecting causal relations structures our perception of events in the world. Here, we determined for visual interactions whether generalized (i.e. feature-invariant) or specialized (i.e. feature-selective) visual routines underlie the perception of causality. To this end, we applied a visual adaptation protocol to assess the adaptability of specific features in classical launching events of simple geometric shapes. We asked observers to report whether they observed a launch or a pass in ambiguous test events (i.e. the overlap between two discs varied from trial to trial). After prolonged exposure to causal launch events (the adaptor) defined by a particular set of features (i.e. a particular motion direction, motion speed, or feature conjunction), observers were less likely to see causal launches in subsequent ambiguous test events than before adaptation. Crucially, adaptation was contingent on the causal impression in launches as demonstrated by a lack of adaptation in non-causal control events. We assessed whether this negative aftereffect transfers to test events with a new set of feature values that were not presented during adaptation. Processing in specialized (as opposed to generalized) visual routines predicts that the transfer of visual adaptation depends on the feature similarity of the adaptor and the test event. We show that the negative aftereffects do not transfer to unadapted launch directions but do transfer to launch events of different speeds. Finally, we used colored discs to assign distinct feature-based identities to the launching and the launched stimulus. We found that the adaptation transferred across colors if the test event had the same motion direction as the adaptor. In summary, visual adaptation allowed us to carve out a visual feature space underlying the perception of causality and revealed specialized visual routines that are tuned to a launch’s motion direction.
-
- Neuroscience
Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.
