Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval

Seidenbecher, Thomas; Laxmi, T. Rao; Stork, Oliver; Pape, H.

doi:10.1515/nf-2003-0405

Cited by 182 publications

(276 citation statements)

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“…Additionally, correlational analysis of our data revealed that only stressed males showed a significant association between freezing during tone and the metabolic activation of hippocampus, basolateral amygdala and PVN. These results are consistent with previous studies showing a synchronization of the theta frequency range between basolateral amygdala and hippocampus during fear memory retrieval (Seidenbecher, Laxmi, Stork, & Pape, 2003) that declines during extinction learning (Lesting et al, 2011). Indeed, in our case we found a highly significant correlation between the metabolic activation of the hippocampus and the basolateral amygdala during extinction in stressed males and females, but not in the non-stressed groups.…”

Section: Sex-related Differences In Brain Metabolic Activation Duringsupporting

confidence: 93%

Stress during puberty boosts metabolic activation associated with fear-extinction learning in hippocampus, basal amygdala and cingulate cortex

Toledo-Rodriguez

Paus

Sandi

2012

Neurobiology of Learning and Memory

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a b s t r a c tAdolescence is characterized by major developmental changes that may render the individual vulnerable to stress and the development of psychopathologies in a sex-specific manner. Earlier we reported lower anxiety-like behavior and higher risk-taking and novelty seeking in rats previously exposed to peripubertal stress. Here we studied whether peri-pubertal stress affected the acquisition and extinction of fear memories and/or the associated functional engagement of various brain regions, as assessed with 2-deoxyglucose. We showed that while peri-pubertal stress reduced freezing during the acquisition of fear memories (training) in both sexes, it had a sex-specific effect on extinction of these memories. Moreover hippocampus, basal amygdala and cingulate and motor cortices showed higher metabolic rates during extinction in rats exposed to peri-pubertal stress. Interestingly, activation of the infralimbic cortex was negatively correlated with freezing during extinction only in control males, while only males stressed during puberty showed a significant correlation between behavior during extinction and metabolic activation of hippocampus, amygdala and paraventricular nucleus. No correlations between brain activation and behavior during extinction were observed in females (control or stress). These results indicate that exposure to peri-pubertal stress affects behavior and brain metabolism when the individual is exposed to an additional stressful challenge. Some of these effects are sex-specific.

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Section: Sex-related Differences In Brain Metabolic Activation Duringsupporting

confidence: 93%

Stress during puberty boosts metabolic activation associated with fear-extinction learning in hippocampus, basal amygdala and cingulate cortex

Toledo-Rodriguez

Paus

Sandi

2012

Neurobiology of Learning and Memory

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“…It was previously reported that the amygdalohippocampal network exhibits synchronized theta activity during CS presentations after conditioning (36), and it was proposed that this activity supports system consolidation of fear memories (47). However, because this increased coherence was observed during CS presentations, its potential involvement in fear memory consolidation vs. expression could not be disentangled.…”

Section: Discussionmentioning

confidence: 98%

Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep

Popa

Duvarci

Popescu

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

304

244

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Brain activity in sleep plays a crucial role in memory consolidation, an offline process that determines the long-term strength of memory traces. Consolidation efficacy differs across individuals, but the brain activity dynamics underlying these differences remain unknown. Here, we studied how interindividual variability in fear memory consolidation relates to neural activity in brain structures that participate in Pavlovian fear learning. From the end of training to testing 24 h later, some rats showed increased and others decreased conditioned fear responses. We found that overnight bidirectional changes in fear memory were selectively correlated with modifications in theta coherence between the amygdala, medial prefrontal cortex, and hippocampus during paradoxical sleep. Thus, our results suggest that theta coordination in the limbic system may influence interindividual differences in memory consolidation of aversive experiences.amygdala | fear conditioning | prefrontal cortex | hippocampus | Granger causality R ecently formed memories undergo a period of consolidation (1, 2), and neuronal activity taking place during sleep is thought to play a critical role in this process (3-7). Consolidation of emotional memories determines their long-term retention, and interindividual variations in memory performance have been related to various factors affecting consolidation, including neuromodulatory transmission (8), levels of circulating stress hormones (9), or genetic factors (10). Several strongly interconnected brain structures are involved in the formation and maintenance of emotional memories, including the hippocampus (Hi), medial prefrontal cortex (mPFC), and basolateral amygdala (BLA) (11-13). The latter structure in particular was shown to mediate the facilitating effects of emotions on memory consolidation (14). Indeed, we form more vivid and enduring memories for emotionally arousing experiences (15). Via the release of peripheral stress hormones (16), emotional arousal causes long-lasting increases in the firing rate of BLA neurons (17), and pharmacologic manipulations that prevent this increased activity interfere with memory for events that took place shortly before, in many learning tasks (18). Importantly, in most learning paradigms, the same interventions performed shortly before testing long-term memory recall have no effect, indicating that the BLA can facilitate the consolidation of memories in other brain structures (14,18).Potentially related to the facilitation of emotional memories by BLA activity, various lines of evidence implicate posttraining paradoxical sleep (PS) in memory consolidation (6,19). These include PS reactivation of brain areas implicated in prior learning (20) and spontaneous replay of waking activity patterns during PS (21). In fact, it was suggested that the distinct pattern of neuronal activity occurring during PS favors memory consolidation (4,22) and that emotional memories are particularly susceptible to this effect (5, 23). Indeed, after fear conditioning, the respons...

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“…Theta rhythm synchrony between HPC and amygdala may underlie anxiety behaviors, as well, as crosscorrelation of activity in the theta frequency in LA and CA1 increase in response to the CS following fear conditioning 133 . Following extinction of fear conditioning, spontaneous freezing to the extinguished CS, representing an inappropriate assessment of threat, is associated with synchronized theta rhythms among IL, CA1 of HPC, and LA 134 .…”

Section: Synchrony Between Interpretation and Evaluation Circuitsmentioning

confidence: 99%

Resolving the neural circuits of anxiety

2015

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Although anxiety disorders represent a major societal problem demanding new therapeutic targets, these efforts have languished in the absence of a mechanistic understanding of this subjective emotional state. While it is impossible to know with absolute certainty the subjective experience of a rodent, rodent models hold promise in dissecting wellconserved limbic circuits. The application of modern approaches in neuroscience has already begun to unmask the neural circuit intricacies underlying anxiety by allowing direct examination of hypotheses drawn from existing psychological concepts. This information points toward an updated conceptual model for what neural circuit perturbations could give rise to pathological anxiety, and thereby provides a roadmap for future therapeutic development.3

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Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval

Cited by 182 publications

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Stress during puberty boosts metabolic activation associated with fear-extinction learning in hippocampus, basal amygdala and cingulate cortex

Stress during puberty boosts metabolic activation associated with fear-extinction learning in hippocampus, basal amygdala and cingulate cortex

Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep

Resolving the neural circuits of anxiety

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