Experience-dependent information routing through the basolateral amygdala shapes behavioral outcomes

It is well established that the basolateral amygdala (BLA) is an emotional processing hub that governs a diverse repertoire of behaviors. Selective engagement of a heterogeneous cell population in the BLA is thought to contribute to this flexibility in behavioral outcomes. However, whether this proc...

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Published inCell reports (Cambridge) Vol. 43; no. 7; p. 114489
Main Authors Antonoudiou, Pantelis, Stone, Bradly T., Colmers, Phillip L.W., Evans-Strong, Aidan, Teboul, Eric, Walton, Najah L., Weiss, Grant L., Maguire, Jamie
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 23.07.2024
Elsevier
Subjects
Animals
avoidance behaviors
basolateral amygdala
Basolateral Nuclear Complex - physiology
bed nucleus of the stria terminalis
Behavior, Animal
circuits
CP: Neuroscience
ensembles
Male
Mice
Mice, Inbred C57BL
Neurons - physiology
nucleus accumbens
Nucleus Accumbens - physiology
Septal Nuclei - physiology
stress
Stress, Psychological
stress-induced helplessness
stress
avoidance behaviors
bed nucleus of the stria terminalis
CP: Neuroscience
basolateral amygdala
nucleus accumbens
circuits
stress-induced helplessness
ensembles
Online AccessGet full text
ISSN2211-1247
2211-1247
DOI10.1016/j.celrep.2024.114489

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Abstract It is well established that the basolateral amygdala (BLA) is an emotional processing hub that governs a diverse repertoire of behaviors. Selective engagement of a heterogeneous cell population in the BLA is thought to contribute to this flexibility in behavioral outcomes. However, whether this process is impacted by previous experiences that influence emotional processing remains unclear. Here we demonstrate that previous positive (enriched environment [EE]) or negative (chronic unpredictable stress [CUS]) experiences differentially influence the activity of populations of BLA principal neurons projecting to either the nucleus accumbens core or bed nucleus of the stria terminalis. Chemogenetic manipulation of these projection-specific neurons can mimic or occlude the effects of CUS and EE on behavioral outcomes to bidirectionally control avoidance behaviors and stress-induced helplessness. These data demonstrate that previous experiences influence the responsiveness of projection-specific BLA principal neurons, biasing information routing through the BLA, to drive divergent behavioral outcomes. [Display omitted] •Previous experiences alter electrophysiological properties of principal neurons in the BLA•Previous experiences differentially alter the activity of projection-specific BLA neurons•Chemogenetic biasing of information flow through the BLA bidirectionally impacts behavior•Previous experiences bias information routing through the BLA to drive divergent behaviors Antonoudiou et al. demonstrate that previous experiences, both positive and negative, influence information routing through the BLA to produce divergent behaviors. They demonstrate that CUS or EE exposure differentially impact the activity of projection-specific BLA neurons and that manipulating these unique circuits can bidirectionally control behavioral outcomes.
AbstractList It is well established that the basolateral amygdala (BLA) is an emotional processing hub that governs a diverse repertoire of behaviors. Selective engagement of a heterogeneous cell population in the BLA is thought to contribute to this flexibility in behavioral outcomes. However, whether this process is impacted by previous experiences that influence emotional processing remains unclear. Here we demonstrate that previous positive (enriched environment [EE]) or negative (chronic unpredictable stress [CUS]) experiences differentially influence the activity of populations of BLA principal neurons projecting to either the nucleus accumbens core or bed nucleus of the stria terminalis. Chemogenetic manipulation of these projection-specific neurons can mimic or occlude the effects of CUS and EE on behavioral outcomes to bidirectionally control avoidance behaviors and stress-induced helplessness. These data demonstrate that previous experiences influence the responsiveness of projection-specific BLA principal neurons, biasing information routing through the BLA, to drive divergent behavioral outcomes.It is well established that the basolateral amygdala (BLA) is an emotional processing hub that governs a diverse repertoire of behaviors. Selective engagement of a heterogeneous cell population in the BLA is thought to contribute to this flexibility in behavioral outcomes. However, whether this process is impacted by previous experiences that influence emotional processing remains unclear. Here we demonstrate that previous positive (enriched environment [EE]) or negative (chronic unpredictable stress [CUS]) experiences differentially influence the activity of populations of BLA principal neurons projecting to either the nucleus accumbens core or bed nucleus of the stria terminalis. Chemogenetic manipulation of these projection-specific neurons can mimic or occlude the effects of CUS and EE on behavioral outcomes to bidirectionally control avoidance behaviors and stress-induced helplessness. These data demonstrate that previous experiences influence the responsiveness of projection-specific BLA principal neurons, biasing information routing through the BLA, to drive divergent behavioral outcomes.
It is well established that the basolateral amygdala (BLA) is an emotional processing hub that governs a diverse repertoire of behaviors. Selective engagement of a heterogeneous cell population in the BLA is thought to contribute to this flexibility in behavioral outcomes. However, whether this process is impacted by previous experiences that influence emotional processing remains unclear. Here we demonstrate that previous positive (enriched environment [EE]) or negative (chronic unpredictable stress [CUS]) experiences differentially influence the activity of populations of BLA principal neurons projecting to either the nucleus accumbens core or bed nucleus of the stria terminalis. Chemogenetic manipulation of these projection-specific neurons can mimic or occlude the effects of CUS and EE on behavioral outcomes to bidirectionally control avoidance behaviors and stress-induced helplessness. These data demonstrate that previous experiences influence the responsiveness of projection-specific BLA principal neurons, biasing information routing through the BLA, to drive divergent behavioral outcomes. Antonoudiou et al. demonstrate that previous experiences, both positive and negative, influence information routing through the BLA to produce divergent behaviors. They demonstrate that CUS or EE exposure differentially impact the activity of projection-specific BLA neurons and that manipulating these unique circuits can bidirectionally control behavioral outcomes.
It is well established that the basolateral amygdala (BLA) is an emotional processing hub that governs a diverse repertoire of behaviors. Selective engagement of a heterogeneous cell population in the BLA is thought to contribute to this flexibility in behavioral outcomes. However, whether this process is impacted by previous experiences that influence emotional processing remains unclear. Here we demonstrate that previous positive (enriched environment [EE]) or negative (chronic unpredictable stress [CUS]) experiences differentially influence the activity of populations of BLA principal neurons projecting to either the nucleus accumbens core or bed nucleus of the stria terminalis. Chemogenetic manipulation of these projection-specific neurons can mimic or occlude the effects of CUS and EE on behavioral outcomes to bidirectionally control avoidance behaviors and stress-induced helplessness. These data demonstrate that previous experiences influence the responsiveness of projection-specific BLA principal neurons, biasing information routing through the BLA, to drive divergent behavioral outcomes. [Display omitted] •Previous experiences alter electrophysiological properties of principal neurons in the BLA•Previous experiences differentially alter the activity of projection-specific BLA neurons•Chemogenetic biasing of information flow through the BLA bidirectionally impacts behavior•Previous experiences bias information routing through the BLA to drive divergent behaviors Antonoudiou et al. demonstrate that previous experiences, both positive and negative, influence information routing through the BLA to produce divergent behaviors. They demonstrate that CUS or EE exposure differentially impact the activity of projection-specific BLA neurons and that manipulating these unique circuits can bidirectionally control behavioral outcomes.
It is well established that the basolateral amygdala (BLA) is an emotional processing hub that governs a diverse repertoire of behaviors. Selective engagement of a heterogeneous cell population in the BLA is thought to contribute to this flexibility in behavioral outcomes. However, whether this process is impacted by previous experiences that influence emotional processing remains unclear. Here we demonstrate that previous positive (enriched environment [EE]) or negative (chronic unpredictable stress [CUS]) experiences differentially influence the activity of populations of BLA principal neurons projecting to either the nucleus accumbens core or bed nucleus of the stria terminalis. Chemogenetic manipulation of these projection-specific neurons can mimic or occlude the effects of CUS and EE on behavioral outcomes to bidirectionally control avoidance behaviors and stress-induced helplessness. These data demonstrate that previous experiences influence the responsiveness of projection-specific BLA principal neurons, biasing information routing through the BLA, to drive divergent behavioral outcomes.
ArticleNumber 114489
Author Teboul, Eric
Maguire, Jamie
Antonoudiou, Pantelis
Walton, Najah L.
Stone, Bradly T.
Colmers, Phillip L.W.
Evans-Strong, Aidan
Weiss, Grant L.
AuthorAffiliation 4 Lead contact
1 Department of Neuroscience, Tufts University School of Medicine, Boston, MA, USA
3 These authors contributed equally
2 Neuroscience Program, Graduate School of Biomedical Sciences, Tufts University School of Medicine, Boston, MA, USA
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Issue 7
Keywords stress
avoidance behaviors
bed nucleus of the stria terminalis
CP: Neuroscience
basolateral amygdala
nucleus accumbens
circuits
stress-induced helplessness
ensembles
Language English
License This is an open access article under the CC BY-NC-ND license.
Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.
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AUTHOR CONTRIBUTIONS
Writing – original draft: P.A., B.T.S., and J.L.M.; writing – editing: P.A., B.T.S., G.L.W., and J.L.M.; data curation: P.A., B.T.S., and G.L.W.; software and algorithms: P.A., G.L.W., B.T.S., and P.L.W.C.; formal analysis: P.A, G.L.W., and B.T.S; visualization: P.A., G.L.W., and B.T.S; methodology: N.L.W, A.E., E.T., and J.L.M; conceptualization, funding acquisition, supervision, and resources: J.L.M.
ORCID 0000-0002-4085-8605
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Snippet It is well established that the basolateral amygdala (BLA) is an emotional processing hub that governs a diverse repertoire of behaviors. Selective engagement...
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SubjectTerms Animals
avoidance behaviors
basolateral amygdala
Basolateral Nuclear Complex - physiology
bed nucleus of the stria terminalis
Behavior, Animal
circuits
CP: Neuroscience
ensembles
Male
Mice
Mice, Inbred C57BL
Neurons - physiology
nucleus accumbens
Nucleus Accumbens - physiology
Septal Nuclei - physiology
stress
Stress, Psychological
stress-induced helplessness
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Title Experience-dependent information routing through the basolateral amygdala shapes behavioral outcomes
URI https://dx.doi.org/10.1016/j.celrep.2024.114489
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