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Neurotensin orchestrates valence assignment in the amygdala

Hao Li, Praneeth Namburi, Jacob M. Olson, Matilde Borio, Mackenzie E. Lemieux, Anna Beyeler, Gwendolyn G. Calhoon, Natsuko Hitora-Imamura, Austin A. Coley, Avraham Libster, Aneesh Bal, Xin Jin, Huan Wang, Caroline Jia, Sourav R. Choudhury, Xi Shi, Ada C. Felix-Ortiz, Verónica de la Fuente, Vanessa P. Barth, Hunter O. King, Ehsan M. Izadmehr, Jasmin S. Revanna, Kanha Batra, Kyle B. Fischer, Laurel R. Keyes, Nancy Padilla-Coreano, Cody A. Siciliano, Kenneth M. McCullough, Romy Wichmann, Kerry J. Ressler, Ila R. Fiete, Feng Zhang, Yulong Li and Kay M. Tye ()
Additional contact information
Hao Li: Salk Institute for Biological Studies
Praneeth Namburi: Massachusetts Institute of Technology
Jacob M. Olson: Massachusetts Institute of Technology
Matilde Borio: Salk Institute for Biological Studies
Mackenzie E. Lemieux: Salk Institute for Biological Studies
Anna Beyeler: Massachusetts Institute of Technology
Gwendolyn G. Calhoon: Massachusetts Institute of Technology
Natsuko Hitora-Imamura: Massachusetts Institute of Technology
Austin A. Coley: Salk Institute for Biological Studies
Avraham Libster: Salk Institute for Biological Studies
Aneesh Bal: Salk Institute for Biological Studies
Xin Jin: Society of Fellows
Huan Wang: IDG/McGovern Institute for Brain Research at PKU
Caroline Jia: Salk Institute for Biological Studies
Sourav R. Choudhury: Broad Institute of MIT and Harvard
Xi Shi: Broad Institute of MIT and Harvard
Ada C. Felix-Ortiz: Massachusetts Institute of Technology
Verónica de la Fuente: Massachusetts Institute of Technology
Vanessa P. Barth: Massachusetts Institute of Technology
Hunter O. King: Massachusetts Institute of Technology
Ehsan M. Izadmehr: Massachusetts Institute of Technology
Jasmin S. Revanna: Salk Institute for Biological Studies
Kanha Batra: Salk Institute for Biological Studies
Kyle B. Fischer: Salk Institute for Biological Studies
Laurel R. Keyes: Salk Institute for Biological Studies
Nancy Padilla-Coreano: Salk Institute for Biological Studies
Cody A. Siciliano: Massachusetts Institute of Technology
Kenneth M. McCullough: McLean Hospital
Romy Wichmann: Salk Institute for Biological Studies
Kerry J. Ressler: McLean Hospital
Ila R. Fiete: Massachusetts Institute of Technology
Feng Zhang: Broad Institute of MIT and Harvard
Yulong Li: IDG/McGovern Institute for Brain Research at PKU
Kay M. Tye: Salk Institute for Biological Studies

Nature, 2022, vol. 608, issue 7923, 586-592

Abstract: Abstract The ability to associate temporally segregated information and assign positive or negative valence to environmental cues is paramount for survival. Studies have shown that different projections from the basolateral amygdala (BLA) are potentiated following reward or punishment learning1–7. However, we do not yet understand how valence-specific information is routed to the BLA neurons with the appropriate downstream projections, nor do we understand how to reconcile the sub-second timescales of synaptic plasticity8–11 with the longer timescales separating the predictive cues from their outcomes. Here we demonstrate that neurotensin (NT)-expressing neurons in the paraventricular nucleus of the thalamus (PVT) projecting to the BLA (PVT-BLA:NT) mediate valence assignment by exerting NT concentration-dependent modulation in BLA during associative learning. We found that optogenetic activation of the PVT-BLA:NT projection promotes reward learning, whereas PVT-BLA projection-specific knockout of the NT gene (Nts) augments punishment learning. Using genetically encoded calcium and NT sensors, we further revealed that both calcium dynamics within the PVT-BLA:NT projection and NT concentrations in the BLA are enhanced after reward learning and reduced after punishment learning. Finally, we showed that CRISPR-mediated knockout of the Nts gene in the PVT-BLA pathway blunts BLA neural dynamics and attenuates the preference for active behavioural strategies to reward and punishment predictive cues. In sum, we have identified NT as a neuropeptide that signals valence in the BLA, and showed that NT is a critical neuromodulator that orchestrates positive and negative valence assignment in amygdala neurons by extending valence-specific plasticity to behaviourally relevant timescales.

Date: 2022
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DOI: 10.1038/s41586-022-04964-y

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