Tracking the Time-Dependent Role of the Hippocampus in Memory Recall Using DREADDs
The hippocampus is critical for the storage of new autobiographical experiences as memories. Following an initial encoding stage in the hippocampus, memories undergo a process of systems-level consolidation, which leads to greater stability through time and an increased reliance on neocortical areas...
Main Authors: | , , , , , , , |
---|---|
Other Authors: | |
Format: | Article |
Language: | en_US |
Published: |
Public Library of Science
2016
|
Online Access: | http://hdl.handle.net/1721.1/103601 https://orcid.org/0000-0002-4155-0346 https://orcid.org/0000-0001-7149-3584 |
_version_ | 1811094709942091776 |
---|---|
author | Varela, Carmen Weiss, Sarah A. Meyer, Retsina Halassa, Michael Biedenkapp, Joseph Wilson, Matthew A. Goosens, Ki Ann Bendor, Daniel |
author2 | Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences |
author_facet | Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Varela, Carmen Weiss, Sarah A. Meyer, Retsina Halassa, Michael Biedenkapp, Joseph Wilson, Matthew A. Goosens, Ki Ann Bendor, Daniel |
author_sort | Varela, Carmen |
collection | MIT |
description | The hippocampus is critical for the storage of new autobiographical experiences as memories. Following an initial encoding stage in the hippocampus, memories undergo a process of systems-level consolidation, which leads to greater stability through time and an increased reliance on neocortical areas for retrieval. The extent to which the retrieval of these consolidated memories still requires the hippocampus is unclear, as both spared and severely degraded remote memory recall have been reported following post-training hippocampal lesions. One difficulty in definitively addressing the role of the hippocampus in remote memory retrieval is the precision with which the entire volume of the hippocampal region can be inactivated. To address this issue, we used Designer Receptors Exclusively Activated by Designer Drugs (DREADDs), a chemical-genetic tool capable of highly specific neuronal manipulation over large volumes of brain tissue. We find that remote (>7 weeks after acquisition), but not recent (1–2 days after acquisition) contextual fear memories can be recalled after injection of the DREADD agonist (CNO) in animals expressing the inhibitory DREADD in the entire hippocampus. Our data demonstrate a time-dependent role of the hippocampus in memory retrieval, supporting the standard model of systems consolidation. |
first_indexed | 2024-09-23T16:03:49Z |
format | Article |
id | mit-1721.1/103601 |
institution | Massachusetts Institute of Technology |
language | en_US |
last_indexed | 2024-09-23T16:03:49Z |
publishDate | 2016 |
publisher | Public Library of Science |
record_format | dspace |
spelling | mit-1721.1/1036012022-10-02T06:04:54Z Tracking the Time-Dependent Role of the Hippocampus in Memory Recall Using DREADDs Varela, Carmen Weiss, Sarah A. Meyer, Retsina Halassa, Michael Biedenkapp, Joseph Wilson, Matthew A. Goosens, Ki Ann Bendor, Daniel Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences McGovern Institute for Brain Research at MIT Picower Institute for Learning and Memory Varela, Carmen Weiss, Sarah A. Halassa, Michael Biedenkapp, Joseph Wilson, Matthew A. Goosens, Ki Ann Bendor, Daniel Meyer, Retsina The hippocampus is critical for the storage of new autobiographical experiences as memories. Following an initial encoding stage in the hippocampus, memories undergo a process of systems-level consolidation, which leads to greater stability through time and an increased reliance on neocortical areas for retrieval. The extent to which the retrieval of these consolidated memories still requires the hippocampus is unclear, as both spared and severely degraded remote memory recall have been reported following post-training hippocampal lesions. One difficulty in definitively addressing the role of the hippocampus in remote memory retrieval is the precision with which the entire volume of the hippocampal region can be inactivated. To address this issue, we used Designer Receptors Exclusively Activated by Designer Drugs (DREADDs), a chemical-genetic tool capable of highly specific neuronal manipulation over large volumes of brain tissue. We find that remote (>7 weeks after acquisition), but not recent (1–2 days after acquisition) contextual fear memories can be recalled after injection of the DREADD agonist (CNO) in animals expressing the inhibitory DREADD in the entire hippocampus. Our data demonstrate a time-dependent role of the hippocampus in memory retrieval, supporting the standard model of systems consolidation. National Institute of Mental Health (U.S.) (NIMH (5R01MH061976)) National Institute of Mental Health (U.S.) (NIMH (R01 MH084966)) United States. Defense Advanced Research Projects Agency (Grant W911NF-10-1-0059) European Research Council (ERC) (Horizon 2020: ERC starter grant-CHIME) 2016-07-14T16:50:47Z 2016-07-14T16:50:47Z 2016-05 2015-09 Article http://purl.org/eprint/type/JournalArticle 1932-6203 http://hdl.handle.net/1721.1/103601 Varela, Carmen, Sarah Weiss, Retsina Meyer, Michael Halassa, Joseph Biedenkapp, Matthew A. Wilson, Ki Ann Goosens, and Daniel Bendor. "Tracking the Time-Dependent Role of the Hippocampus in Memory Recall Using DREADDs." PLoS ONE 11:5 (2016): e0154374. https://orcid.org/0000-0002-4155-0346 https://orcid.org/0000-0001-7149-3584 en_US http://dx.doi.org/10.1371/journal.pone.0154374 PLOS ONE Creative Commons Attribution 4.0 International License http://creativecommons.org/licenses/by/4.0/ application/pdf Public Library of Science PLOS |
spellingShingle | Varela, Carmen Weiss, Sarah A. Meyer, Retsina Halassa, Michael Biedenkapp, Joseph Wilson, Matthew A. Goosens, Ki Ann Bendor, Daniel Tracking the Time-Dependent Role of the Hippocampus in Memory Recall Using DREADDs |
title | Tracking the Time-Dependent Role of the Hippocampus in Memory Recall Using DREADDs |
title_full | Tracking the Time-Dependent Role of the Hippocampus in Memory Recall Using DREADDs |
title_fullStr | Tracking the Time-Dependent Role of the Hippocampus in Memory Recall Using DREADDs |
title_full_unstemmed | Tracking the Time-Dependent Role of the Hippocampus in Memory Recall Using DREADDs |
title_short | Tracking the Time-Dependent Role of the Hippocampus in Memory Recall Using DREADDs |
title_sort | tracking the time dependent role of the hippocampus in memory recall using dreadds |
url | http://hdl.handle.net/1721.1/103601 https://orcid.org/0000-0002-4155-0346 https://orcid.org/0000-0001-7149-3584 |
work_keys_str_mv | AT varelacarmen trackingthetimedependentroleofthehippocampusinmemoryrecallusingdreadds AT weisssaraha trackingthetimedependentroleofthehippocampusinmemoryrecallusingdreadds AT meyerretsina trackingthetimedependentroleofthehippocampusinmemoryrecallusingdreadds AT halassamichael trackingthetimedependentroleofthehippocampusinmemoryrecallusingdreadds AT biedenkappjoseph trackingthetimedependentroleofthehippocampusinmemoryrecallusingdreadds AT wilsonmatthewa trackingthetimedependentroleofthehippocampusinmemoryrecallusingdreadds AT goosenskiann trackingthetimedependentroleofthehippocampusinmemoryrecallusingdreadds AT bendordaniel trackingthetimedependentroleofthehippocampusinmemoryrecallusingdreadds |