False Opposing Fear Memories Are Produced as a Function of the Hippocampal Sector Where Glucocorticoid Receptors Are Activated
Injection of corticosterone (CORT) in the dorsal hippocampus (DH) can mimic post-traumatic stress disorder (PTSD)—related memory in mice: both maladaptive hypermnesia for a salient but irrelevant simple cue and amnesia for the traumatic context. However, accumulated evidence indicates a functional d...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-08-01
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| Series: | Frontiers in Behavioral Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fnbeh.2020.00144/full |
| _version_ | 1818610080289914880 |
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| author | Nadia Kaouane Nadia Kaouane Eva-Gunnel Ducourneau Eva-Gunnel Ducourneau Aline Marighetto Aline Marighetto Menahem Segal Aline Desmedt Aline Desmedt |
| author_facet | Nadia Kaouane Nadia Kaouane Eva-Gunnel Ducourneau Eva-Gunnel Ducourneau Aline Marighetto Aline Marighetto Menahem Segal Aline Desmedt Aline Desmedt |
| author_sort | Nadia Kaouane |
| collection | DOAJ |
| description | Injection of corticosterone (CORT) in the dorsal hippocampus (DH) can mimic post-traumatic stress disorder (PTSD)—related memory in mice: both maladaptive hypermnesia for a salient but irrelevant simple cue and amnesia for the traumatic context. However, accumulated evidence indicates a functional dissociation within the hippocampus such that contextual learning is primarily associated with the DH whereas emotional processes are more linked to the ventral hippocampus (VH). This suggests that CORT might have different effects on fear memories as a function of the hippocampal sector preferentially targeted and the type of fear learning (contextual vs. cued) considered. We tested this hypothesis in mice using CORT infusion into the DH or VH after fear conditioning, during which a tone was either paired (predicting-tone) or unpaired (predicting-context) with the shock. We first replicate our previous results showing that intra-DH CORT infusion impairs contextual fear conditioning while inducing fear responses to the not predictive tone. Second, we show that, in contrast, intra-VH CORT infusion has opposite effects on fear memories: in the predicting-tone situation, it blocks tone fear conditioning while enhancing the fear responses to the context. In both situations, a false fear memory is formed based on an erroneous selection of the predictor of the threat. Third, these opposite effects of CORT on fear memory are both mediated by glucocorticoid receptor (GR) activation, and reproduced by post-conditioning stress or systemic CORT injection. These findings demonstrate that false opposing fear memories can be produced depending on the hippocampal sector in which the GRs are activated. |
| first_indexed | 2024-12-16T15:08:45Z |
| format | Article |
| id | doaj.art-4953231816a44e969808627e1e65cfa7 |
| institution | Directory Open Access Journal |
| issn | 1662-5153 |
| language | English |
| last_indexed | 2024-12-16T15:08:45Z |
| publishDate | 2020-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Behavioral Neuroscience |
| spelling | doaj.art-4953231816a44e969808627e1e65cfa72022-12-21T22:27:02ZengFrontiers Media S.A.Frontiers in Behavioral Neuroscience1662-51532020-08-011410.3389/fnbeh.2020.00144566815False Opposing Fear Memories Are Produced as a Function of the Hippocampal Sector Where Glucocorticoid Receptors Are ActivatedNadia Kaouane0Nadia Kaouane1Eva-Gunnel Ducourneau2Eva-Gunnel Ducourneau3Aline Marighetto4Aline Marighetto5Menahem Segal6Aline Desmedt7Aline Desmedt8INSERM, Neurocentre Magendie, Physiopathologie de la Plasticité Neuronale, Bordeaux, FranceUniversity of Bordeaux, Bordeaux, FranceINSERM, Neurocentre Magendie, Physiopathologie de la Plasticité Neuronale, Bordeaux, FranceUniversity of Bordeaux, Bordeaux, FranceINSERM, Neurocentre Magendie, Physiopathologie de la Plasticité Neuronale, Bordeaux, FranceUniversity of Bordeaux, Bordeaux, FranceDepartment of Neurobiology, The Weizmann Institute, Rehovot, IsraelINSERM, Neurocentre Magendie, Physiopathologie de la Plasticité Neuronale, Bordeaux, FranceUniversity of Bordeaux, Bordeaux, FranceInjection of corticosterone (CORT) in the dorsal hippocampus (DH) can mimic post-traumatic stress disorder (PTSD)—related memory in mice: both maladaptive hypermnesia for a salient but irrelevant simple cue and amnesia for the traumatic context. However, accumulated evidence indicates a functional dissociation within the hippocampus such that contextual learning is primarily associated with the DH whereas emotional processes are more linked to the ventral hippocampus (VH). This suggests that CORT might have different effects on fear memories as a function of the hippocampal sector preferentially targeted and the type of fear learning (contextual vs. cued) considered. We tested this hypothesis in mice using CORT infusion into the DH or VH after fear conditioning, during which a tone was either paired (predicting-tone) or unpaired (predicting-context) with the shock. We first replicate our previous results showing that intra-DH CORT infusion impairs contextual fear conditioning while inducing fear responses to the not predictive tone. Second, we show that, in contrast, intra-VH CORT infusion has opposite effects on fear memories: in the predicting-tone situation, it blocks tone fear conditioning while enhancing the fear responses to the context. In both situations, a false fear memory is formed based on an erroneous selection of the predictor of the threat. Third, these opposite effects of CORT on fear memory are both mediated by glucocorticoid receptor (GR) activation, and reproduced by post-conditioning stress or systemic CORT injection. These findings demonstrate that false opposing fear memories can be produced depending on the hippocampal sector in which the GRs are activated.https://www.frontiersin.org/article/10.3389/fnbeh.2020.00144/fulldorsal hippocampusventral hippocampusfear memoryfear conditioningglucocorticoid receptorsmice |
| spellingShingle | Nadia Kaouane Nadia Kaouane Eva-Gunnel Ducourneau Eva-Gunnel Ducourneau Aline Marighetto Aline Marighetto Menahem Segal Aline Desmedt Aline Desmedt False Opposing Fear Memories Are Produced as a Function of the Hippocampal Sector Where Glucocorticoid Receptors Are Activated Frontiers in Behavioral Neuroscience dorsal hippocampus ventral hippocampus fear memory fear conditioning glucocorticoid receptors mice |
| title | False Opposing Fear Memories Are Produced as a Function of the Hippocampal Sector Where Glucocorticoid Receptors Are Activated |
| title_full | False Opposing Fear Memories Are Produced as a Function of the Hippocampal Sector Where Glucocorticoid Receptors Are Activated |
| title_fullStr | False Opposing Fear Memories Are Produced as a Function of the Hippocampal Sector Where Glucocorticoid Receptors Are Activated |
| title_full_unstemmed | False Opposing Fear Memories Are Produced as a Function of the Hippocampal Sector Where Glucocorticoid Receptors Are Activated |
| title_short | False Opposing Fear Memories Are Produced as a Function of the Hippocampal Sector Where Glucocorticoid Receptors Are Activated |
| title_sort | false opposing fear memories are produced as a function of the hippocampal sector where glucocorticoid receptors are activated |
| topic | dorsal hippocampus ventral hippocampus fear memory fear conditioning glucocorticoid receptors mice |
| url | https://www.frontiersin.org/article/10.3389/fnbeh.2020.00144/full |
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