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Glucocorticoid Enhancement of Recognition Memory Via Basolateral Amygdala-Driven Facilitation of Prelimbic Cortex Interactions

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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 Areg Barsegyana,b, Gabriele Mironea,b, Giacomo Ronzonia,b, Chunan Guoa,b, Qi Songa,b, Daan van Kuppevelda,b, Evelien H. S. Schuta,b, Piray Atsaka,b, Selina Teurlingsa,b, James L. McGaughc,d,1, Dirk Schuberta,b, and Benno Roozendaala,b,1 aDepartment of Cognitive Neuroscience, Radboud University Medical Center, 6500 HB Nijmegen, The Netherlands; bDonders Institute for Brain, Cognition and Behaviour, Radboud University, 6525 EN Nijmegen, The Netherlands; cCenter for the Neurobiology of Learning and Memory, University of California, Irvine, CA 92697-3800; and dDepartment of Neurobiology and Behavior, University of California, Irvine, CA 92697-3800 Contributed by James L. McGaugh, February 15, 2019 (sent for review January 28, 2019; reviewed by Ivan Izquierdo and Barry Setlow) Extensive evidence indicates that the basolateral amygdala (BLA) We investigated whether BLA noradrenergic activity enables interacts with other brain regions in mediating stress hormone and functional interactions between the medial prefrontal cortex emotional arousal effects on memory consolidation. Brain activation (mPFC) and the anterior insular cortex (aIC) and dorsal hippo- studies have shown that arousing conditions lead to the activation of campus (dHPC) in mediating glucocorticoid hormone enhance- large-scale neural networks and several functional connections ment of recognition memory for objects and their location. between brain regions beyond the BLA. Whether such distal Previous findings indicate that the mPFC contributes to memory interactions on memory consolidation also depend on BLA activity through cognitive or strategic control over memory processes is not as yet known. We investigated, in male Sprague–Dawley rats, within other brain areas (16, 17) and that the aIC is involved in whether BLA activity enables prelimbic cortex (PrL) interactions with memory for the identity of an object (18). Functional interactions the anterior insular cortex (aIC) and dorsal hippocampus (dHPC) in between the mPFC and aIC might occur when emotionally salient regulating glucocorticoid effects on different components of object information, including novel objects, is detected (19, 20). Previous NEUROSCIENCE recognition memory. The glucocorticoid receptor (GR) agonist RU findings also indicate that the dHPC is involved in associating an – 28362 administered into the PrL, but not infralimbic cortex, immedi- object with its context or place (21 23) and that the processing of ately after object recognition training enhanced 24-hour memory of contextual information engages a functional cross talk between the – both the identity and location of the object via functional interac- mPFC and dHPC (24 26). Importantly, the mPFC (27), aIC (28), tions with the aIC and dHPC, respectively. Importantly, posttraining and dHPC (29) all receive strong inputs from the BLA. We show inactivation of the BLA by the noradrenergic antagonist propranolol that a glucocorticoid receptor (GR) agonist administered into the abolished the effect of GR agonist administration into the PrL on prelimbic cortex (PrL) but not the infralimbic cortex (IL) of the memory enhancement of both the identity and location of the ob- mPFC after an object recognition training experience enhances ject. BLA inactivation by propranolol also blocked the effect of GR the consolidation of memory of both the identity and location of an agonist administration into the PrL on inducing changes in neuronal object via functional cross talk with the aIC and dHPC, respectively. activity within the aIC and dHPC during the postlearning consolida- Most importantly, we show that BLA noradrenergic activity drives tion period as well as on structural changes in spine morphology functional interactions between these distal brain regions. These findings indicate that the BLA influences large-scale brain networks 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 emo- Significance tional arousal effects on memory. Stress hormones are known to facilitate memory of emotion- basolateral amygdala | medial prefrontal cortex | anterior insular cortex | ally arousing experiences, an effect that is mediated by the dorsal hippocampus | norepinephrine basolateral amygdala (BLA) and its interaction with other brain regions. Brain activation studies also indicate that emotional tressful and emotional experiences activate hormonal and arousal activates several functional connections beyond the Sbrain systems that create strong memories (1, 2). Extensive BLA. However, it is largely unknown whether BLA activity in- evidence indicates that noradrenergic activation of the baso- fluences these connections. Here, we report that BLA activity lateral amygdala (BLA), induced by emotional arousal, is cru- enables functional interactions between the prelimbic cortex, cially involved in strengthening the consolidation of long-term anterior insular cortex, and dorsal hippocampus in regulating memory (2). We have reported extensive evidence indicating glucocorticoid hormone effects on recognition memory. These that noradrenergic activation of the BLA also plays a critical role findings increase our understanding of how BLA activity af- in enabling the enhancing effects of adrenal stress hormones, fects emotional memory within large brain networks. that is, epinephrine and glucocorticoids, on memory consolida- – Author contributions: A.B., J.L.M., D.S., and B.R. designed research; A.B., G.M., G.R., C.G., tion (3 5). Many previous studies have investigated how such 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., BLA activation enhances the consolidation of memory by 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. influencing neural plasticity and information storage processes Reviewers: I.I., Pontifical Catholic University of Rio Grande do Sul; and B.S., University within specific target regions, such as the hippocampus (2, 6–10). of Florida. Accumulating evidence from brain activation studies indicates The authors declare no conflict of interest. that arousing conditions increase activation of large-scale neural Published under the PNAS license. – networks (11 13) and also affect numerous functional interactions 1To whom correspondence may be addressed. Email: [email protected] or benno. between brain regions beyond the amygdala (14, 15). However, [email protected]. it is not known whether BLA activity is required for regulating This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. emotional arousal effects on functional interactions between such 1073/pnas.1901513116/-/DCSupplemental. distal brain regions. www.pnas.org/cgi/doi/10.1073/pnas.1901513116 PNAS Latest Articles | 1of6 Downloaded by guest on September 28, 2021 in regulating stress hormone and emotional arousal effects on of GR activity with posttraining infusions of the GR antagonist RU memory (13). 38486 (3 or 10 ng in 0.5 μL) impairs memory of that training. To determine whether animals exhibit a memory for the identity of the Results object (object recognition memory, ORM), some rats were given a Effect of GR Agonist Administration into the PrL and IL on the 24-h retention test in which one object was familiar and the other Consolidation of Object Recognition Memory and Object Location object was novel. This protocol is depicted in Fig. 1A. To determine Memory. We investigated whether GR agonist administration whether animals exhibit a memory for the location of the object into the PrL and IL, two subregions of the mPFC, enhances the (object location memory, OLM), other rats were given a 24-h re- consolidation of memory of different components of object tention test in which both objects were familiar but one was placed in recognition training. Male Sprague–Dawley rats were trained on a novel location (Fig. 1E). a 3-min object recognition trial during which they could freely ORM task. GR agonist administration into the PrL immediately explore two identical objects, immediately followed by bilateral after a 3-min training trial enhanced 24-h memory for the identity F = microinfusions of the GR agonist RU 28362 (3 or 10 ng in 0.5 μL) of the object (one-way ANOVA for discrimination index: 2,33 or vehicle administered into either the PrL or IL (Fig. 1I and SI 10.02, P = 0.0004). As shown in Fig. 1B, vehicle-treated control rats t t = Appendix, Fig. S1 for infusion sites). Other groups of rats were did not express 24-h retention of the object (one-sample test: 11 trained on a 10-min training trial, which induces robust long- 0.40, P = 0.69), and both doses of the GR agonist significantly term memory (23, 30), and we examined whether a blockade enhanced retention (3 ng: P < 0.05; 10 ng: P < 0.01 vs. vehicle). In contrast, GR agonist infusions administered into the IL did not affect 24-h retention (F2,33 = 0.25, P = 0.78; Fig. 1C). As shown in Fig. 1D, GR antagonist administration into the PrL after a 10-min A ORM E OLM I training session significantly impaired 24-h memory for the identity Drug infusion Drug infusion of the object (F2,32 = 13.14, P < 0.0001). Vehicle-treated rats expressed significant retention (t12 = 12.08, P < 0.0001), and both 24 h 24 h doses of the GR antagonist impaired retention
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