The Reuniens and Rhomboid Nuclei Are Required for Acquisition of Pavlovian Trace Fear Conditioning in Rats

Lin, Yu-Ju; Chiou, Ruei Jen; Chang, Chung-Yi

doi:10.1523/eneuro.0106-20.2020

Cited by 25 publications

(23 citation statements)

References 74 publications

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“…In particular, the RE appears necessary for contextual memory, as illustrated in studies using contextual fear conditioning. For example, muscimol inactivation before acquisition or retrieval impaired contextual fear conditioning ( Ramanathan et al, 2018 ), and the acquisition, but not retrieval, of trace fear conditioning ( Lin, Chiou, & Chang, 2020 ) in male rats. Further, chemogenetic inactivation using hM4Di also impaired contextual fear conditioning in male mice ( Vetere et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Chemogenetic inactivation of the nucleus reuniens impairs object placement memory in female mice

Schwabe

Lincoln

Ivers

et al. 2021

Neurobiology of Learning and Memory

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Episodic memory is a complex process requiring input from several regions of the brain. Emerging evidence suggests that coordinated activity between the dorsal hippocampus (DH) and medial prefrontal cortex (mPFC) is required for episodic memory consolidation. However, the mechanisms through which the DH and mPFC interact to promote memory consolidation remain poorly understood. A growing body of research suggests that the nucleus reuniens of the thalamus (RE) is one of several structures that facilitate communication between the DH and mPFC during memory and may do so through bidirectional excitatory projections to both regions. Furthermore, recent work from other labs indicates that the RE is necessary for spatial working memory. However, it is not clear to what extent the RE is necessary for memory of object locations. The goal of this study was to determine whether activity in the RE is necessary for spatial memory as measured by the object placement (OP) task in female mice. A kappa-opioid receptor DREADD (KORD) virus was used to inactivate excitatory neurons in the RE pre- or post-training to establish a role for the RE in spatial memory acquisition and consolidation, respectively. RE inactivation prior to, or immediately after, object training blocked OP memory formation relative to chance and to control mice. Moreover, expression of the immediate early gene EGR-1 was reduced in the RE 1 hour after an object training trial, supporting the conclusion that reduced neuronal activity in the RE impairs the formation of object location memories. In summary, the findings of this study support a key role for the RE in spatial memory acquisition and consolidation.

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Section: Discussionmentioning

confidence: 99%

Chemogenetic inactivation of the nucleus reuniens impairs object placement memory in female mice

Schwabe

Lincoln

Ivers

et al. 2021

Neurobiology of Learning and Memory

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“…While the role of RE in cognitive functions is generally well established, relatively little is known regarding its involvement in affective behavior-possibly linked to HF-mPFC communication. The majority of studies on this topic have focused on the role of RE in learned fear (Lin, Chiou, & Chang, 2020;Moscarello, 2020;Quet et al, 2020;Ramanathan, Jin, Giustino, Payne, & Maren, 2018a;Ramanathan & Maren, 2019;Ramanathan, Ressler, Jin, & Maren, 2018b;Sierra et al, 2017;Troyner, Bicca, & Bertoglio, 2018;Xu & Südhof, 2013). For instance, in an initial report, Xu and Südhof (2013) demonstrated that inactivation of mPFC terminals to RE produced an overgeneralization of contextual fear memory, and that suppressing or enhancing RE terminals to the HF resulted in an overgeneralization or a reduction of contextual fear memory, respectively.…”

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confidence: 99%

Role of the reuniens and rhomboid thalamic nuclei in anxiety‐like avoidance behavior in the rat

et al. 2021

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The nucleus reuniens (RE) and rhomboid (RH) nuclei of the ventral midline thalamus are reciprocally connected with the prefrontal cortex (PFC) and the hippocampus (HF) and serve as key intermediaries between these structures, regulating cognitive and emotional behaviors. Regarding affective behavior, several recent reports have described the involvement of RE/RH in the acquisition and retention of conditioned fear, but little is known regarding their role (RE/RH) in anxiety-like behaviors. We examined the role of RH/RE on avoidance and defensive behaviors in male Long Evans rats using the elevated plus maze (EPM). We found that the reversible suppression of RE/RH with muscimol increased avoidance behavior to the open arms of the plus maze as shown by: (a) significant reductions in open arm entries; (b) reductions in the mean duration of time spent in the open arms; and (c) significant increases in retreats during open arm exploration. This was coupled with decreases inthe number of head dips in the maze. Consistent with these behavioral effects, a single exposure of naïve rats to the plus maze produced significant increases in c-fos expression selectively in RE and RH of midline thalamic nuclei. We posit that RE/RH normally acts to optimize adaptive responses to anxiety-eliciting situations, and disruptions of RE/RH produce severe deficits in coping behaviors-or as shown here increases in avoidance/defensive behaviors. In sum, the present results establish a novel role for RE/RH in anxiety-like avoidance behavior. In addition to its role in attention, working memory, and executive control, RE/RH also regulates adaptative responses to not only fear but also to anxiogenic stimuli. As such, dysfunction of RE/RH may contribute to the amalgamation of symptoms common to many mental health disorders including anxiety, depression, schizophrenia, and PTSD.

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“…Interestingly, previous research shows that exposure to acute stress (swim and restraint stress) produces high levels of c-fos mRNA expression in the RE (Cullinan, Herman, Battaglia, Akil, & Watson, 1995;Kafetzopoulos et al, 2018), suggesting possible recruitment of the region during a stressor. It is known that the RE is recruited during encoding of contextual information during fear conditioning (Lin, Chiou, & Chang, 2020), suggesting this region is involved in the formation and acquisition of stressor or context-related memory (Eichenbaum, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…During encoding of contextual information during fear conditioning (Lin et al, 2020), the RE coordinates mPFC-hippocampal interactions (Eichenbaum, 2017). Further, connectivity between the medial prefrontal cortex (mPFC) and RE may be distinctly involved in regulating immobility behavior during stressor exposure and re-exposure to the stressor-paired context.…”

Section: Discussionmentioning

confidence: 99%

The Role of the Nucleus Reuniens in Regulating Contextual Conditioning with the Predator Odor TMT

Lc¹,

K²,

Besheer

2021

Preprint

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Experiencing intrusive distressing memories of a traumatic event(s) is a prominent symptom profile for post-traumatic stress disorder (PTSD). Understanding the neurobiological mechanisms associated with this symptom profile can be invaluable for effective treatment for PTSD. Here, we investigated the functional role of the nucleus reuniens (RE), a midline thalamic in modulating stressor-related memory. Female Long Evans rats were implanted with a cannula aimed at the RE. The RE was pharmacologically inactivated via muscimol (0.5 mM) prior to exposure to the predator odor stressor trimethylthiazoline (TMT; synthetically derived fox feces component) or water (controls) in a distinct context with bedding material (Experiment 1) or no bedding (Experiment 2). To measure context reactivity, the index of the contextual memory, 2 weeks following exposure to TMT, rats were re-exposed to the TMT-paired context (in the absence of TMT). In Experiment 1, during context re-exposure (with bedding), inactivation of the RE had no effect on context reactivity. In Experiment 2, during context re-exposure (no bedding), rats previous exposed to TMT showed decreased immobility compared to controls, indicating reactivity to the context and likely related to increased exploration of the environment. Rats in the TMT group that received RE inactivation showed increased immobility relative to rats that received aCSF, suggesting that muscimol pre-treatment blunted context reactivity. In conclusion, recruitment of the RE in stressor-related contextual memory appears to be dependent on the contextual environment and whether the animal is able to engage in different stress coping strategies.

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The Reuniens and Rhomboid Nuclei Are Required for Acquisition of Pavlovian Trace Fear Conditioning in Rats

Cited by 25 publications

References 74 publications

Chemogenetic inactivation of the nucleus reuniens impairs object placement memory in female mice

Chemogenetic inactivation of the nucleus reuniens impairs object placement memory in female mice

Role of the reuniens and rhomboid thalamic nuclei in anxiety‐like avoidance behavior in the rat

The Role of the Nucleus Reuniens in Regulating Contextual Conditioning with the Predator Odor TMT

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