A circuit mechanism for differentiating positive and negative associations

The ability to differentiate stimuli predicting positive or negative outcomes is critical for survival, and perturbations of emotional processing underlie many psychiatric disease states. Synaptic plasticity in the basolateral amygdala complex (BLA) mediates the acquisition of associative memories,...

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Main Authors: Namburi, Praneeth (Contributor), Beyeler, Anna (Contributor), Yorozu, Suzuko (Author), Calhoon, Gwendolyn G. (Contributor), Wichmann, Romy (Contributor), Holden, Stephanie S. (Contributor), Mertens, Kim L. (Contributor), Wickersham, Ian R. (Contributor), Gray, Jesse M. (Author), Halbert, Sarah (Contributor), Anahtar, Melodi N. (Contributor), Felix-Ortiz, Ada Celis (Contributor), Tye, Kay (Contributor)
Other Authors: Massachusetts Institute of Technology. Department of Biological Engineering (Contributor), Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences (Contributor), McGovern Institute for Brain Research at MIT (Contributor), Picower Institute for Learning and Memory (Contributor)
Format: Article
Language:English
Published: Nature Publishing Group, 2016-05-18T13:58:05Z.
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Summary:The ability to differentiate stimuli predicting positive or negative outcomes is critical for survival, and perturbations of emotional processing underlie many psychiatric disease states. Synaptic plasticity in the basolateral amygdala complex (BLA) mediates the acquisition of associative memories, both positive and negative. Different populations of BLA neurons may encode fearful or rewarding associations, but the identifying features of these populations and the synaptic mechanisms of differentiating positive and negative emotional valence have remained unknown. Here we show that BLA neurons projecting to the nucleus accumbens (NAc projectors) or the centromedial amygdala (CeM projectors) undergo opposing synaptic changes following fear or reward conditioning. We find that photostimulation of NAc projectors supports positive reinforcement while photostimulation of CeM projectors mediates negative reinforcement. Photoinhibition of CeM projectors impairs fear conditioning and enhances reward conditioning. We characterize these functionally distinct neuronal populations by comparing their electrophysiological, morphological and genetic features. Overall, we provide a mechanistic explanation for the representation of positive and negative associations within the amygdala.
National Institute of Mental Health (U.S.) (R01-MH102441-01)
National Institute of Diabetes and Digestive and Kidney Diseases (U.S.) (DP2-DK-102256-01)
JPB Foundation
Brain & Behavior Research Foundation
Klingenstein Foundation
Whitehall Foundation
Alfred P. Sloan Foundation
Singleton Fellowship
MIT Presidential Marcus Fellowship to Honor Norman B. Leventhal
Whitaker Foundation (Fellowship)
Swiss National Science Foundation (Fellowship)
Massachusetts Institute of Technology. Simons Center for the Social Brain (Postdoctoral Fellowship)
NWO of the Netherlands (Rubicon Award)
McGovern Institute for Brain Research at MIT (Seed Grant)
Picower Institute for Learning and Memory (Seed Grant)
Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences (Seed Grant)
Massachusetts Institute of Technology. Simons Center for the Social Brain (Seed Grant)
National Institute of Mental Health (U.S.) (BRAIN Initiative Award)
National Eye Institute (BRAIN Initiative Award)
National Institute of Neurological Disorders and Stroke (U.S.) (BRAIN Initiative Award U01-MH106018)
National Institute of Neurological Disorders and Stroke (U.S.) (BRAIN Initiative Award U01-NS090473)
National Science Foundation (U.S.) (IOS-1451202)