Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment

Anthony Burgos-Robles; Eyal Y. Kimchi; Ehsan M. Izadmehr; Mary Jane Porzenheim; William A. Ramos-Guasp; Edward H. Nieh; Ada C. Felix-Ortiz; Praneeth Namburi; Christopher A. Leppla; Kara N. Presbrey; Kavitha K. Anandalingam; Pablo A. Pagan-Rivera; Melodi Anahtar; Anna Beyeler; Kay M. Tye

doi:10.1038/nn.4553

Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment

Anthony Burgos-Robles, Eyal Y. Kimchi, Ehsan M. Izadmehr, Mary Jane Porzenheim, William A. Ramos-Guasp, Edward H. Nieh, Ada C. Felix-Ortiz, Praneeth Namburi, Christopher A. Leppla, Kara N. Presbrey, Kavitha K. Anandalingam, Pablo A. Pagan-Rivera, Melodi Anahtar, Anna Beyeler, Kay M. Tye^*

^*Corresponding author for this work

Neurology

Research output: Contribution to journal › Article › peer-review

215 Scopus citations

Abstract

Orchestrating appropriate behavioral responses in the face of competing signals that predict either rewards or threats in the environment is crucial for survival. The basolateral nucleus of the amygdala (BLA) and prelimbic (PL) medial prefrontal cortex have been implicated in reward-seeking and fear-related responses, but how information flows between these reciprocally connected structures to coordinate behavior is unknown. We recorded neuronal activity from the BLA and PL while rats performed a task wherein competing shock- and sucrose-predictive cues were simultaneously presented. The correlated firing primarily displayed a BLA→PL directionality during the shock-associated cue. Furthermore, BLA neurons optogenetically identified as projecting to PL more accurately predicted behavioral responses during competition than unidentified BLA neurons. Finally photostimulation of the BLA→PL projection increased freezing, whereas both chemogenetic and optogenetic inhibition reduced freezing. Therefore, the BLA→PL circuit is critical in governing the selection of behavioral responses in the face of competing signals.

Original language	English (US)
Pages (from-to)	824-835
Number of pages	12
Journal	Nature neuroscience
Volume	20
Issue number	6
DOIs	https://doi.org/10.1038/nn.4553
State	Published - Jun 1 2017

Funding

The authors thank S. Sorooshyari for discussion and assistance on Matlab programming, as well as C. Wildes, and the entire Tye laboratory for discussion and support on this project. A.B.-R. was supported by the Brain and Behavior Research Foundation (NARSAD Young Investigator Award) and NIMH (Research Supplement to Promote Diversity in Health-Related Sciences). E.Y.K. was supported by the Collaborative Clinical Neuroscience Fellowship and the American Brain Foundation Clinical Research Training Fellowship. W.A.R.-G. and P.A.P.-R. were supported by the MIT Summer Research Program, which received support from the Center for Brains, Minds and Machines (CBMM), NSF (STC Award CCF-1231216) and NIH (Endure Award 1R25-MH092912-01). E.H.N. was supported by the National Science Foundation Graduate Research Fellowship (NSF GRFP), the Integrative Neuronal Systems Training Fellowship (T32 GM007484) and the Training Program in the Neurobiology of Learning and Memory. A.C.F.-O. was supported by an institutional NRSA training grant (5T32GM007484-38). P.N. was supported by the Singleton, Leventhal and Whitaker fellowships. C.A.L. was supported by an NSF Graduate Research Fellowship, an Integrative Neuronal Systems Fellowship and the James R. Killian Fellowship. M.J.P., K.N.P. and M.A. were supported by the MIT Undergraduate Research Opportunities Program. K.K.A. was supported by the MIT Research Assistantship Program. K.M.T. is a New York Stem Cell Foundation - Robertson Investigator and McKnight Scholar, and this work was supported by funding from the JPB Foundation, PIIF, PNDRF, JFDP, Whitehall Foundation, Klingenstein Foundation, NARSAD Young Investigator Award, Alfred P Sloan Foundation, New York Stem Cell Foundation, McKnight Foundation, NIH R01-MH102441-01 (NIMH), R01-AA023305-01 (NIAAA) and NIH Director's New Innovator Award DP2-DK-102256-01 (NIDDK).

ASJC Scopus subject areas

General Neuroscience

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Burgos-Robles, A., Kimchi, E. Y., Izadmehr, E. M., Porzenheim, M. J., Ramos-Guasp, W. A., Nieh, E. H., Felix-Ortiz, A. C., Namburi, P., Leppla, C. A., Presbrey, K. N., Anandalingam, K. K., Pagan-Rivera, P. A., Anahtar, M., Beyeler, A., & Tye, K. M. (2017). Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment. Nature neuroscience, 20(6), 824-835. https://doi.org/10.1038/nn.4553

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title = "Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment",

abstract = "Orchestrating appropriate behavioral responses in the face of competing signals that predict either rewards or threats in the environment is crucial for survival. The basolateral nucleus of the amygdala (BLA) and prelimbic (PL) medial prefrontal cortex have been implicated in reward-seeking and fear-related responses, but how information flows between these reciprocally connected structures to coordinate behavior is unknown. We recorded neuronal activity from the BLA and PL while rats performed a task wherein competing shock- and sucrose-predictive cues were simultaneously presented. The correlated firing primarily displayed a BLA→PL directionality during the shock-associated cue. Furthermore, BLA neurons optogenetically identified as projecting to PL more accurately predicted behavioral responses during competition than unidentified BLA neurons. Finally photostimulation of the BLA→PL projection increased freezing, whereas both chemogenetic and optogenetic inhibition reduced freezing. Therefore, the BLA→PL circuit is critical in governing the selection of behavioral responses in the face of competing signals.",

author = "Anthony Burgos-Robles and Kimchi, {Eyal Y.} and Izadmehr, {Ehsan M.} and Porzenheim, {Mary Jane} and Ramos-Guasp, {William A.} and Nieh, {Edward H.} and Felix-Ortiz, {Ada C.} and Praneeth Namburi and Leppla, {Christopher A.} and Presbrey, {Kara N.} and Anandalingam, {Kavitha K.} and Pagan-Rivera, {Pablo A.} and Melodi Anahtar and Anna Beyeler and Tye, {Kay M.}",

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Burgos-Robles, A, Kimchi, EY, Izadmehr, EM, Porzenheim, MJ, Ramos-Guasp, WA, Nieh, EH, Felix-Ortiz, AC, Namburi, P, Leppla, CA, Presbrey, KN, Anandalingam, KK, Pagan-Rivera, PA, Anahtar, M, Beyeler, A & Tye, KM 2017, 'Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment', Nature neuroscience, vol. 20, no. 6, pp. 824-835. https://doi.org/10.1038/nn.4553

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AU - Namburi, Praneeth

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AU - Presbrey, Kara N.

AU - Anandalingam, Kavitha K.

AU - Pagan-Rivera, Pablo A.

AU - Anahtar, Melodi

AU - Beyeler, Anna

AU - Tye, Kay M.

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Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment

Abstract

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