Glucocorticoid enhancement of recognition memory via basolateral amygdala-driven facilitation of prelimbic cortex interactions

Glucocorticoid enhancement of recognition memory via basolateral amygdala-driven facilitation of prelimbic cortex interactions

Extensive evidence indicates that the basolateral amygdala (BLA) interacts with other brain regions in mediating stress hormone and emotional arousal effects on memory consolidation. Brain activation studies have shown that arousing conditions lead to the activation of large-scale neural networks an...

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Published in:Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 14; pp. 7077 - 7082
Main Authors: Barsegyan, Areg, Mirone, Gabriele, Ronzoni, Giacomo, Guo, Chunan, Song, Qi, van Kuppeveld, Daan, Schut, Evelien H. S., Atsak, Piray, Teurlings, Selina, McGaugh, James L., Schubert, Dirk, Roozendaal, Benno
Format: Journal Article
Language:English
Published: United States National Academy of Sciences 02-04-2019
Subjects:
Activation
Agonists
Amygdala
Animal behavior
Arousal
Biological Sciences
Brain
Consolidation
Cortex (insular)
Deactivation
Emotions
Glucocorticoids
Inactivation
Morphology
Neural networks
Norepinephrine
Object recognition
Pattern recognition
Propranolol
norepinephrine
dorsal hippocampus
medial prefrontal cortex
anterior insular cortex
basolateral amygdala
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Summary:Extensive evidence indicates that the basolateral amygdala (BLA) interacts with other brain regions in mediating stress hormone and emotional arousal effects on memory consolidation. Brain activation studies have shown that arousing conditions lead to the activation of large-scale neural networks and several functional connections between brain regions beyond the BLA. Whether such distal interactions on memory consolidation also depend on BLA activity is not as yet known. We investigated, in male Sprague–Dawley rats, whether BLA activity enables prelimbic cortex (PrL) interactions with the anterior insular cortex (aIC) and dorsal hippocampus (dHPC) in regulating glucocorticoid effects on different components of object recognition memory. The glucocorticoid receptor (GR) agonist RU 28362 administered into the PrL, but not infralimbic cortex, immediately after object recognition training enhanced 24-hour memory of both the identity and location of the object via functional interactions with the aIC and dHPC, respectively. Importantly, posttraining inactivation of the BLA by the noradrenergic antagonist propranolol abolished the effect of GR agonist administration into the PrL on memory enhancement of both the identity and location of the object. BLA inactivation by propranolol also blocked the effect of GR agonist administration into the PrL on inducing changes in neuronal activity within the aIC and dHPC during the postlearning consolidation period as well as on structural changes in spine morphology assessed 24 hours later. These findings provide evidence that BLA noradrenergic activity enables functional interactions between the PrL and the aIC and dHPC in regulating stress hormone and emotional arousal effects on memory.
Bibliography:Author contributions: A.B., J.L.M., D.S., and B.R. designed research; A.B., G.M., G.R., C.G., Q.S., D.v.K., E.H.S.S., P.A., S.T., and B.R. performed research; A.B., G.M., G.R., C.G., Q.S., D.v.K., S.T., D.S., and B.R. analyzed data; and A.B., J.L.M., D.S., and B.R. wrote the paper.
Contributed by James L. McGaugh, February 15, 2019 (sent for review January 28, 2019; reviewed by Ivan Izquierdo and Barry Setlow)
Reviewers: I.I., Pontifical Catholic University of Rio Grande do Sul; and B.S., University of Florida.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1901513116