Persistence of fear memory across time requires the basolateral amygdala complex

Poulos, Andrew M.; Li, Veronica; Sterlace, Sarah S.; Tokushige, Fonda; Ponnusamy, Ravikumar; Fanselow, Michael S.

doi:10.1073/pnas.0905257106

Cited by 64 publications

(61 citation statements)

References 40 publications

(51 reference statements)

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“…Many reports have shown that IA training with high-intensity foot shocks reduced the memory impairment caused by hippocampal inactivation (38)(39)(40), thus suggesting that consolidation of intense emotional experiences do not require a functioning hippocampus. However, this fear memory is acquired slowly and forgotten when remote memory is tested (41). We suggest that histamine in the BLA promoted inhibitory avoidance learning independently of hippocampus by increasing the emotional value of IA training.…”

Section: Discussionmentioning

confidence: 98%

Histamine in the basolateral amygdala promotes inhibitory avoidance learning independently of hippocampus

Benetti

Furini

Myskiw

et al. 2015

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

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Recent discoveries demonstrated that recruitment of alternative brain circuits permits compensation of memory impairments following damage to brain regions specialized in integrating and/or storing specific memories, including both dorsal hippocampus and basolateral amygdala (BLA). Here, we first report that the integrity of the brain histaminergic system is necessary for long-term, but not for short-term memory of step-down inhibitory avoidance (IA). Second, we found that phosphorylation of cyclic adenosine monophosphate (cAMP) responsive-element-binding protein, a crucial mediator in long-term memory formation, correlated anatomically and temporally with histamine-induced memory retrieval, showing the active involvement of histamine function in CA1 and BLA in different phases of memory consolidation. Third, we found that exogenous application of histamine in either hippocampal CA1 or BLA of brain histamine-depleted rats, hence amnesic, restored long-term memory; however, the time frame of memory rescue was different for the two brain structures, short lived (immediately posttraining) for BLA, long lasting (up to 6 h) for the CA1. Moreover, long-term memory was formed immediately after training restoring of histamine transmission only in the BLA. These findings reveal the essential role of histaminergic neurotransmission to provide the brain with the plasticity necessary to ensure memorization of emotionally salient events, through recruitment of alternative circuits. Hence, our findings indicate that the histaminergic system comprises parallel, coordinated pathways that provide compensatory plasticity when one brain structure is compromised.histamine | hippocampus | amygdala | lateral ventricle | inhibitory avoidance

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Section: Discussionmentioning

confidence: 98%

Histamine in the basolateral amygdala promotes inhibitory avoidance learning independently of hippocampus

Benetti

Furini

Myskiw

et al. 2015

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

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“…[46][47][48][49][50][51] Unlike the hippocampus, the amygdala is necessary for the acquisition of fearful memories and their long-term storage and retrieval. 38,[52][53][54] In summary, explicit memory requires structures in the medial temporal lobe, such as the hippocampal formation and several cortical regions. Implicit memory involves a number of diverse brain regions, including the cerebellum, striatum, and midbrain.…”

Section: Learning and Memorymentioning

confidence: 99%

Inhibition de l’apprentissage et de la mémoire par les anesthésiques généraux

Wang

Orser

2010

Can J Anesth/J Can Anesth

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“…However, if information flow is precluded in such a neural pathway, plasticity in alternate regions is capable of compensating, albeit with less efficiency (27,31). This theory is evident, as animals that learn fear in the absence of the primary pathway require significant overtraining (>50 trials) and begin to display significant forgetting after 7 d (25,32). Thus, although plasticity in the BLA normally supports contextual fear-conditioning, without the BLA, some alternate regions must compensate.…”

mentioning

confidence: 96%

Compensation in the neural circuitry of fear conditioning awakens learning circuits in the bed nuclei of the stria terminalis

Poulos

Ponnusamy²,

Dong³

et al. 2010

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

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The basolateral amygdala (BLA) is thought to be essential for fear learning. However, extensive training can overcome the loss of conditional fear evident following lesions and inactivation of the BLA. Such results suggest the existence of a primary BLA-dependent and a compensatory BLA-independent neural circuit. We tested the hypothesis that the bed nuclei of the stria terminalis (BST) provides this compensatory plasticity. Using extensive context-fear conditioning, we demonstrate that combined BLA and BST lesions prevented fear acquisition and expression. Additionally, protein synthesis in the BST was critical only for consolidation of BLA-independent but not BLA-dependent fear. Moreover, fear acquired after BLA lesions resulted in greater activation of BST regions that receive hippocampal efferents. These results suggest that the BST is capable of functioning as a compensatory site in the acquisition and consolidation of context-fear memories. Unlocking such neural compensation holds promise for understanding situations when brain damage impairs normal function or failure to regulate compensatory sites leads to anxiety disorders. amygdala | basolateral amygdala | context | plasticity | bed nucleus of the stria terminalis A largely supported view in the neuroscience of associative memory is the existence of essential neural circuits that have the capacity to learn, retain, and retrieve specific classes of experience 1-7). For example, in reflexive motor learning or Pavlovian eyeblink-conditioning, the integration of sensory stimuli within the cerebellar interpositus nuclei are required for the acquisition, retention, and retrieval conditional responses (8). Similarly, the striatum is considered critical for habit learning (9, 10) and the hippocampus essential for spatial learning (11). In fearconditioning, a circuit centered around the basolateral amygdala complex (BLA; consisting of the lateral amygdala, basomedial, basolateral, and posterior nuclei) is viewed essential for the acquisition and expression of fear memories (12-16). The importance of the BLA for fear memory has been supported by numerous studies showing that disruption of protein synthesis, NMDA receptor function, neuronal activity, synaptic transmission, and plasticity all prevent the establishment of fear memories (14-18).Context fear learning normally occurs when hippocampal context information, which exits the subiculum, converges with aversive information in the BLA (15). In turn, when the contextual information activates the BLA, this information is relayed to the central nucleus of the amygdala (CEA), whose efferents to the ventral periaqueductal gray (vPAG) trigger the expression of fear as indexed by conditional freezing (conditional response) (19). Lesions or inactivations of the CEA can disrupt contextual fear (20, 21; but see 22). Of particular relevance in this study is that pretraining lesions or inactivations of the BLA have been shown to strongly impair the acquisition of fear (23-25). However, with extensive overtraining (∼75 tr...

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Persistence of fear memory across time requires the basolateral amygdala complex

Cited by 64 publications

References 40 publications

Histamine in the basolateral amygdala promotes inhibitory avoidance learning independently of hippocampus

Histamine in the basolateral amygdala promotes inhibitory avoidance learning independently of hippocampus

Inhibition de l’apprentissage et de la mémoire par les anesthésiques généraux

Compensation in the neural circuitry of fear conditioning awakens learning circuits in the bed nuclei of the stria terminalis

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