期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：22
DOI：10.1073/pnas.2203680119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
The basolateral amygdala is known to mediate emotional arousal effects on different forms of recognition memory via functional interactions with the insular cortex. Human neuroimaging studies have revealed that emotional stimulation first rapidly increases activity of the anterior division of the insular cortex, as part of the large-scale salience network, but suppresses anterior insular cortex activity in a delayed fashion. Here, we show that the effect of noradrenergic activation of the basolateral amygdala on enhancing object recognition memory is associated with a suppression of anterior insular cortex activity during the postlearning consolidation period. Such delayed emotional arousal effects on brain network dynamics might disrupt attentional reorienting toward new external stimuli and thereby protect the ongoing consolidation process from interference.
Noradrenergic activation of the basolateral amygdala (BLA) by emotional arousal enhances different forms of recognition memory via functional interactions with the insular cortex (IC). Human neuroimaging studies have revealed that the anterior IC (aIC), as part of the salience network, is dynamically regulated during arousing situations. Emotional stimulation first rapidly increases aIC activity but suppresses it in a delayed fashion. Here, we investigated in male Sprague-Dawley rats whether the BLA influence on recognition memory is associated with an increase or suppression of aIC activity during the postlearning consolidation period. We first employed anterograde and retrograde viral tracing and found that the BLA sends dense monosynaptic projections to the aIC. Memory-enhancing norepinephrine administration into the BLA following an object training experience suppressed aIC activity 1 h later, as determined by a reduced expression of the phosphorylated form of the transcription factor cAMP response element-binding (pCREB) protein and neuronal activity marker c-Fos. In contrast, the number of perisomatic γ-aminobutyric acid (GABA)ergic inhibitory synapses per pCREB-positive neuron was significantly increased, suggesting a dynamic up-regulation of GABAergic tone. In support of this possibility, pharmacological inhibition of aIC activity with a GABAergic agonist during consolidation enhanced object recognition memory. Norepinephrine administration into the BLA did not affect neuronal activity within the posterior IC, which receives sparse innervation from the BLA. The evidence that noradrenergic activation of the BLA enhances the consolidation of object recognition memory via a mechanism involving a suppression of aIC activity provides insight into the broader brain network dynamics underlying emotional regulation of memory.
