Top-down control of flight by a non-canonical cortico-amygdala pathway

Chandrashekhar D. Borkar, Claire E. Stelly, Xin Fu, Maria Dorofeikova, Quan-Son Eric Le, Rithvik Vutukuri, Catherine Vo, Alex Walker, Samhita Basavanhalli, Anh Duong, Erin Bean, Alexis Resendez, Jones G. Parker, Jeffrey G. Tasker and Jonathan P. Fadok ()
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Chandrashekhar D. Borkar: Tulane University
Claire E. Stelly: Tulane University
Xin Fu: Tulane University
Maria Dorofeikova: Tulane University
Quan-Son Eric Le: Tulane University
Rithvik Vutukuri: Tulane University
Catherine Vo: Tulane University
Alex Walker: Tulane University
Samhita Basavanhalli: Tulane University
Anh Duong: Tulane University
Erin Bean: Tulane University
Alexis Resendez: Tulane University
Jones G. Parker: Northwestern University
Jeffrey G. Tasker: Tulane University
Jonathan P. Fadok: Tulane University

Nature, 2024, vol. 625, issue 7996, 743-749

Abstract: Abstract Survival requires the selection of appropriate behaviour in response to threats, and dysregulated defensive reactions are associated with psychiatric illnesses such as post-traumatic stress and panic disorder1. Threat-induced behaviours, including freezing and flight, are controlled by neuronal circuits in the central amygdala (CeA)2; however, the source of neuronal excitation of the CeA that contributes to high-intensity defensive responses is unknown. Here we used a combination of neuroanatomical mapping, in vivo calcium imaging, functional manipulations and electrophysiology to characterize a previously unknown projection from the dorsal peduncular (DP) prefrontal cortex to the CeA. DP-to-CeA neurons are glutamatergic and specifically target the medial CeA, the main amygdalar output nucleus mediating conditioned responses to threat. Using a behavioural paradigm that elicits both conditioned freezing and flight, we found that CeA-projecting DP neurons are activated by high-intensity threats in a context-dependent manner. Functional manipulations revealed that the DP-to-CeA pathway is necessary and sufficient for both avoidance behaviour and flight. Furthermore, we found that DP neurons synapse onto neurons within the medial CeA that project to midbrain flight centres. These results elucidate a non-canonical top-down pathway regulating defensive responses.

Date: 2024
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DOI: 10.1038/s41586-023-06912-w

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