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Thalamus sends information about arousal but not valence to the amygdala

RATIONALE: The basolateral amygdala (BLA) and medial geniculate nucleus of the thalamus (MGN) have both been shown to be necessary for the formation of associative learning. While the role that the BLA plays in this process has long been emphasized, the MGN has been less well-studied and surrounded...

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Autores principales: Leppla, Chris A., Keyes, Laurel R., Glober, Gordon, Matthews, Gillian A., Batra, Kanha, Jay, Maya, Feng, Yu, Chen, Hannah S., Mills, Fergil, Delahanty, Jeremy, Olson, Jacob M., Nieh, Edward H., Namburi, Praneeth, Wildes, Craig, Wichmann, Romy, Beyeler, Anna, Kimchi, Eyal Y., Tye, Kay M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9928937/
https://www.ncbi.nlm.nih.gov/pubmed/36522481
http://dx.doi.org/10.1007/s00213-022-06284-5
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author Leppla, Chris A.
Keyes, Laurel R.
Glober, Gordon
Matthews, Gillian A.
Batra, Kanha
Jay, Maya
Feng, Yu
Chen, Hannah S.
Mills, Fergil
Delahanty, Jeremy
Olson, Jacob M.
Nieh, Edward H.
Namburi, Praneeth
Wildes, Craig
Wichmann, Romy
Beyeler, Anna
Kimchi, Eyal Y.
Tye, Kay M.
author_facet Leppla, Chris A.
Keyes, Laurel R.
Glober, Gordon
Matthews, Gillian A.
Batra, Kanha
Jay, Maya
Feng, Yu
Chen, Hannah S.
Mills, Fergil
Delahanty, Jeremy
Olson, Jacob M.
Nieh, Edward H.
Namburi, Praneeth
Wildes, Craig
Wichmann, Romy
Beyeler, Anna
Kimchi, Eyal Y.
Tye, Kay M.
author_sort Leppla, Chris A.
collection PubMed
description RATIONALE: The basolateral amygdala (BLA) and medial geniculate nucleus of the thalamus (MGN) have both been shown to be necessary for the formation of associative learning. While the role that the BLA plays in this process has long been emphasized, the MGN has been less well-studied and surrounded by debate regarding whether the relay of sensory information is active or passive. OBJECTIVES: We seek to understand the role the MGN has within the thalamoamgydala circuit in the formation of associative learning. METHODS: Here, we use optogenetics and in vivo electrophysiological recordings to dissect the MGN-BLA circuit and explore the specific subpopulations for evidence of learning and synthesis of information that could impact downstream BLA encoding. We employ various machine learning techniques to investigate function within neural subpopulations. We introduce a novel method to investigate tonic changes across trial-by-trial structure, which offers an alternative approach to traditional trial-averaging techniques. RESULTS: We find that the MGN appears to encode arousal but not valence, unlike the BLA which encodes for both. We find that the MGN and the BLA appear to react differently to expected and unexpected outcomes; the BLA biased responses toward reward prediction error and the MGN focused on anticipated punishment. We uncover evidence of tonic changes by visualizing changes across trials during inter-trial intervals (baseline epochs) for a subset of cells. CONCLUSION: We conclude that the MGN-BLA projector population acts as both filter and transferer of information by relaying information about the salience of cues to the amygdala, but these signals are not valence-specified. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00213-022-06284-5.
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spelling pubmed-99289372023-02-16 Thalamus sends information about arousal but not valence to the amygdala Leppla, Chris A. Keyes, Laurel R. Glober, Gordon Matthews, Gillian A. Batra, Kanha Jay, Maya Feng, Yu Chen, Hannah S. Mills, Fergil Delahanty, Jeremy Olson, Jacob M. Nieh, Edward H. Namburi, Praneeth Wildes, Craig Wichmann, Romy Beyeler, Anna Kimchi, Eyal Y. Tye, Kay M. Psychopharmacology (Berl) Original Investigation RATIONALE: The basolateral amygdala (BLA) and medial geniculate nucleus of the thalamus (MGN) have both been shown to be necessary for the formation of associative learning. While the role that the BLA plays in this process has long been emphasized, the MGN has been less well-studied and surrounded by debate regarding whether the relay of sensory information is active or passive. OBJECTIVES: We seek to understand the role the MGN has within the thalamoamgydala circuit in the formation of associative learning. METHODS: Here, we use optogenetics and in vivo electrophysiological recordings to dissect the MGN-BLA circuit and explore the specific subpopulations for evidence of learning and synthesis of information that could impact downstream BLA encoding. We employ various machine learning techniques to investigate function within neural subpopulations. We introduce a novel method to investigate tonic changes across trial-by-trial structure, which offers an alternative approach to traditional trial-averaging techniques. RESULTS: We find that the MGN appears to encode arousal but not valence, unlike the BLA which encodes for both. We find that the MGN and the BLA appear to react differently to expected and unexpected outcomes; the BLA biased responses toward reward prediction error and the MGN focused on anticipated punishment. We uncover evidence of tonic changes by visualizing changes across trials during inter-trial intervals (baseline epochs) for a subset of cells. CONCLUSION: We conclude that the MGN-BLA projector population acts as both filter and transferer of information by relaying information about the salience of cues to the amygdala, but these signals are not valence-specified. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00213-022-06284-5. Springer Berlin Heidelberg 2022-12-16 2023 /pmc/articles/PMC9928937/ /pubmed/36522481 http://dx.doi.org/10.1007/s00213-022-06284-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Investigation
Leppla, Chris A.
Keyes, Laurel R.
Glober, Gordon
Matthews, Gillian A.
Batra, Kanha
Jay, Maya
Feng, Yu
Chen, Hannah S.
Mills, Fergil
Delahanty, Jeremy
Olson, Jacob M.
Nieh, Edward H.
Namburi, Praneeth
Wildes, Craig
Wichmann, Romy
Beyeler, Anna
Kimchi, Eyal Y.
Tye, Kay M.
Thalamus sends information about arousal but not valence to the amygdala
title Thalamus sends information about arousal but not valence to the amygdala
title_full Thalamus sends information about arousal but not valence to the amygdala
title_fullStr Thalamus sends information about arousal but not valence to the amygdala
title_full_unstemmed Thalamus sends information about arousal but not valence to the amygdala
title_short Thalamus sends information about arousal but not valence to the amygdala
title_sort thalamus sends information about arousal but not valence to the amygdala
topic Original Investigation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9928937/
https://www.ncbi.nlm.nih.gov/pubmed/36522481
http://dx.doi.org/10.1007/s00213-022-06284-5
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