Nucleus reuniens of the thalamus controls fear memory intensity, specificity and long‐term maintenance during consolidation

Troyner, Fernanda; Bicca, Maíra A.; Bertoglio, Leandro J.

doi:10.1002/hipo.22964

Cited by 54 publications

(34 citation statements)

References 77 publications

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“…And how do different connections between the hippocampus and prefrontal cortex contribute to this process? There is a direct connection not only from ventral hippocampus (Jay and Witter, 1991) but also indirect pathways through reuniens (Barker and Warburton, 2018;Ferraris et al, 2018;Mei et al, 2018;Troyner et al, 2018;Wagner et al, 2019) and mPFC (Olafsdottir et al, 2017), but which pathways relate to which role remains unclear.…”

Section: Resultsmentioning

confidence: 99%

Naïve to expert: Considering the role of previous knowledge in memory

Alonso

Meij

Tse

et al. 2020

Brain and Neuroscience Advances

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In humans, most of our new memories are in some way or another related to what we have already experienced. However, in memory research, especially in non-human animal research, subjects are often mostly naïve to the world. But we know that previous knowledge will change how memories are processed and which brain areas are critical at which time point. Each process from encoding, consolidation, to memory retrieval will be affected. Here, we summarise previous knowledge effects on the neurobiology of memory in both humans and non-human animals, with a special focus on schemas – associative network structures. Furthermore, we propose a new theory on how there may be a continuous gradient from naïve to expert, which would modulate the importance and role of brain areas, such as the hippocampus and prefrontal cortex.

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Section: Resultsmentioning

confidence: 99%

Naïve to expert: Considering the role of previous knowledge in memory

Alonso

Meij

Tse

et al. 2020

Brain and Neuroscience Advances

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“…Most aspects mentioned in this section were conducted as fully described elsewhere 20 , 29 , 30 . Briefly, contextual fear conditioning was performed in a rectangular chamber (35 × 20 × 30 cm), with aluminum sidewalls and a front wall and ceiling-door made of Plexiglas, designated herein as context A.…”

Section: Methodsmentioning

confidence: 99%

“…contextual fear conditioning and elevated plus-maze apparatuses, behavioral procedures, and data collection. Most aspects mentioned in this section were conducted as fully described elsewhere 20,29,30 .…”

Section: Infralimbic Cortex Controls Fear Memory Generalization and Smentioning

confidence: 99%

“…In contrast, there were no effects of temporary IL inactivation with muscimol on inhibitory avoidance memory consolidation 17 . Studies focusing on cued or contextual fear memory consolidation have also reported changes in the IL, including depressed intrinsic neuronal excitability 18 , 19 and increased Arc expression 20 , but not c-fos induction or histone acetylation 21 , 22 . Post-acquisition gamma irradiation potentiated the consolidation of a contextual fear memory trace, an effect associated with reduced IL neuronal activation 23 .…”

Section: Introductionmentioning

confidence: 99%

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Infralimbic cortex controls fear memory generalization and susceptibility to extinction during consolidation

Bayer

Bertoglio

2020

Sci Rep

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Lesioning or inactivating the infralimbic (IL) subregion of the medial prefrontal cortex before acquisition produces more generalized and extinction-resistant fear memories. However, whether and how it modulates memory specificity and extinction susceptibility while consolidation takes place is still unknown. The present study aims to investigate these questions using muscimol-induced temporary inactivation and anisomycin-induced protein synthesis inhibition in the rat IL following contextual fear conditioning. Results indicate that the IL activity immediately after acquisition, but not six hours later, controls memory generalization over a week, regardless of its strength. Such IL function depends on the context-shock pairing since muscimol induced no changes in animals exposed to immediate shocks or the conditioning context only. Animals in which the IL was inactivated during consolidation extinguished similarly to controls within the session but were unable to recall the extinction memory the following day. Noteworthy, these post-acquisition IL inactivation-induced effects were not associated with changes in anxiety, as assessed in the elevated plus-maze test. Anisomycin results indicate that the IL protein synthesis during consolidation contributes more to producing extinction-sensitive fear memories than memory specificity. Collectively, present results provide evidence for the IL's role in controlling generalization and susceptibility to extinction during fear memory consolidation.

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“…Specifically, permanent RE inactivation increased the generalization of fear to a novel context after contextual fear conditioning. These results suggest that the RE is involved in encoding or consolidating (Vetere et al, 2017;Troyner et al, 2018) precise context representations that normally limit the generalization of fear from the conditioning context to other, dissimilar contexts.…”

Section: Introductionmentioning

confidence: 87%

Nucleus reuniens is required for encoding and retrieving precise, hippocampal-dependent contextual fear memories in rats

Ramanathan

Ressler

Jin

et al. 2018

Preprint

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The nucleus reuniens (RE) is a ventral midline thalamic nucleus that interconnects the medial prefrontal cortex (mPFC) and hippocampus (HPC). Considerable data indicate that HPC-mPFC circuits are involved in contextual and spatial memory; however, it is not clear whether the RE mediates the acquisition or retrieval of these memories. To examine this question, we inactivated the RE with muscimol before either the acquisition or retrieval of Pavlovian fear conditioning in rats; freezing served as the index of fear. We found that RE inactivation before conditioning impaired the acquisition of contextual freezing, whereas inactivation of the RE prior to retrieval testing increased the generalization of freezing to a novel context; inactivation of the RE did not affect either the acquisition or expression of auditory fear conditioning. Interestingly, contextual conditioning impairments were absent when retrieval testing was also conducted after RE inactivation. Contextual memories acquired under RE inactivation were hippocampalindependent, insofar as contextual freezing in rats conditioned under RE inactivation was insensitive to intra-hippocampal infusions of the NMDA receptor antagonist, D,L-amino-5phosophonovaleric acid (APV). Together, these data reveal that the RE supports hippocampaldependent encoding of precise contextual memories that allow discrimination of dangerous from safe contexts. When the RE is inactive, however, alternate neural systems acquire an impoverished contextual memory that is only expressed when the RE is offline. SIGNIFICANCE STATEMENTThe midline thalamic nucleus reuniens (RE) coordinates communication between the hippocampus and medial prefrontal cortex, brain areas critical for contextual and spatial memory.Here we show that temporary pharmacological inactivation of RE impairs the acquisition and precision of contextual fear memories after Pavlovian fear conditioning in rats. However, inactivating the RE prior to retrieval testing restored contextual memory in rats conditioned after RE inactivation. Critically, we show that imprecise contextual memories acquired under RE inactivation are learned independently of the hippocampus. These data reveal that the RE is required for hippocampal-dependent encoding of precise contextual memories to support the discrimination of safe and dangerous contexts.

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Nucleus reuniens of the thalamus controls fear memory intensity, specificity and long‐term maintenance during consolidation

Cited by 54 publications

References 77 publications

Naïve to expert: Considering the role of previous knowledge in memory

Naïve to expert: Considering the role of previous knowledge in memory

Infralimbic cortex controls fear memory generalization and susceptibility to extinction during consolidation

Nucleus reuniens is required for encoding and retrieving precise, hippocampal-dependent contextual fear memories in rats

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