Cargando…
Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity
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 dynamicall...
Autores principales: | , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9295787/ https://www.ncbi.nlm.nih.gov/pubmed/35622887 http://dx.doi.org/10.1073/pnas.2203680119 |
_version_ | 1784750127085256704 |
---|---|
author | Chen, Yan-Fen Song, Qi Colucci, Paola Maltese, Federica Siller-Pérez, Cristina Prins, Karina McGaugh, James L. Hermans, Erno J. Campolongo, Patrizia Kasri, Nael Nadif Roozendaal, Benno |
author_facet | Chen, Yan-Fen Song, Qi Colucci, Paola Maltese, Federica Siller-Pérez, Cristina Prins, Karina McGaugh, James L. Hermans, Erno J. Campolongo, Patrizia Kasri, Nael Nadif Roozendaal, Benno |
author_sort | Chen, Yan-Fen |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-9295787 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-92957872022-07-20 Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity Chen, Yan-Fen Song, Qi Colucci, Paola Maltese, Federica Siller-Pérez, Cristina Prins, Karina McGaugh, James L. Hermans, Erno J. Campolongo, Patrizia Kasri, Nael Nadif Roozendaal, Benno Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2022-05-27 2022-05-31 /pmc/articles/PMC9295787/ /pubmed/35622887 http://dx.doi.org/10.1073/pnas.2203680119 Text en Copyright © 2022 the Author(s). Published by PNAS https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Biological Sciences Chen, Yan-Fen Song, Qi Colucci, Paola Maltese, Federica Siller-Pérez, Cristina Prins, Karina McGaugh, James L. Hermans, Erno J. Campolongo, Patrizia Kasri, Nael Nadif Roozendaal, Benno Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity |
title | Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity |
title_full | Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity |
title_fullStr | Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity |
title_full_unstemmed | Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity |
title_short | Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity |
title_sort | basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9295787/ https://www.ncbi.nlm.nih.gov/pubmed/35622887 http://dx.doi.org/10.1073/pnas.2203680119 |
work_keys_str_mv | AT chenyanfen basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity AT songqi basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity AT coluccipaola basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity AT maltesefederica basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity AT sillerperezcristina basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity AT prinskarina basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity AT mcgaughjamesl basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity AT hermansernoj basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity AT campolongopatrizia basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity AT kasrinaelnadif basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity AT roozendaalbenno basolateralamygdalaactivationenhancesobjectrecognitionmemorybyinhibitinganteriorinsularcortexactivity |