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Title: Dopaminergic inputs in the dentate gyrus direct the choice of memory encoding

Abstract

Rewarding experiences are often well remembered, and such memory formation is known to be dependent on dopamine modulation of the neural substrates engaged in learning and memory; however, it is unknown how and where in the brain dopamine signals bias episodic memory toward preceding rather than subsequent events. Here we found that photostimulation of channelrhodopsin-2–expressing dopaminergic fibers in the dentate gyrus induced a long-term depression of cortical inputs, diminished theta oscillations, and impaired subsequent contextual learning. Computational modeling based on this dopamine modulation indicated an asymmetric association of events occurring before and after reward in memory tasks. In subsequent behavioral experiments, preexposure to a natural reward suppressed hippocampus-dependent memory formation, with an effective time window consistent with the duration of dopamine-induced changes of dentate activity. Altogether, our results suggest a mechanism by which dopamine enables the hippocampus to encode memory with reduced interference from subsequent experience.

Authors:
 [1];  [2];  [3];  [1];  [2];  [2];  [4];  [2];  [1];  [4];  [2];  [1]
  1. Huazhong Univ. of Science and Technology, Wuhan (China)
  2. Salk Institute for Biological Studies, La Jolla, CA (United States)
  3. Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
  4. Chinese Academy of Sciences, Shenzhen (China)
Publication Date:
Research Org.:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1328121
Report Number(s):
SAND-2016-7558J
Journal ID: ISSN 0027-8424; 646387; TRN: US1700156
Grant/Contract Number:
AC04-94AL85000
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 113; Journal Issue: 37; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; dopamine; channelrhodopsin-2; theta oscillation; temporal difference learning

Citation Formats

Du, Huiyun, Deng, Wei, Aimone, James B., Ge, Minyan, Parylak, Sarah, Walch, Keenan, Zhang, Wei, Cook, Jonathan, Song, Huina, Wang, Liping, Gage, Fred H., and Mu, Yangling. Dopaminergic inputs in the dentate gyrus direct the choice of memory encoding. United States: N. p., 2016. Web. doi:10.1073/pnas.1606951113.
Du, Huiyun, Deng, Wei, Aimone, James B., Ge, Minyan, Parylak, Sarah, Walch, Keenan, Zhang, Wei, Cook, Jonathan, Song, Huina, Wang, Liping, Gage, Fred H., & Mu, Yangling. Dopaminergic inputs in the dentate gyrus direct the choice of memory encoding. United States. doi:10.1073/pnas.1606951113.
Du, Huiyun, Deng, Wei, Aimone, James B., Ge, Minyan, Parylak, Sarah, Walch, Keenan, Zhang, Wei, Cook, Jonathan, Song, Huina, Wang, Liping, Gage, Fred H., and Mu, Yangling. 2016. "Dopaminergic inputs in the dentate gyrus direct the choice of memory encoding". United States. doi:10.1073/pnas.1606951113. https://www.osti.gov/servlets/purl/1328121.
@article{osti_1328121,
title = {Dopaminergic inputs in the dentate gyrus direct the choice of memory encoding},
author = {Du, Huiyun and Deng, Wei and Aimone, James B. and Ge, Minyan and Parylak, Sarah and Walch, Keenan and Zhang, Wei and Cook, Jonathan and Song, Huina and Wang, Liping and Gage, Fred H. and Mu, Yangling},
abstractNote = {Rewarding experiences are often well remembered, and such memory formation is known to be dependent on dopamine modulation of the neural substrates engaged in learning and memory; however, it is unknown how and where in the brain dopamine signals bias episodic memory toward preceding rather than subsequent events. Here we found that photostimulation of channelrhodopsin-2–expressing dopaminergic fibers in the dentate gyrus induced a long-term depression of cortical inputs, diminished theta oscillations, and impaired subsequent contextual learning. Computational modeling based on this dopamine modulation indicated an asymmetric association of events occurring before and after reward in memory tasks. In subsequent behavioral experiments, preexposure to a natural reward suppressed hippocampus-dependent memory formation, with an effective time window consistent with the duration of dopamine-induced changes of dentate activity. Altogether, our results suggest a mechanism by which dopamine enables the hippocampus to encode memory with reduced interference from subsequent experience.},
doi = {10.1073/pnas.1606951113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 37,
volume = 113,
place = {United States},
year = 2016,
month = 9
}

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