Cardiogenic control of affective behavioural state

Brian Hsueh, Ritchie Chen, YoungJu Jo, Daniel Tang, Misha Raffiee, Yoon Seok Kim, Masatoshi Inoue, Sawyer Randles, Charu Ramakrishnan, Sneha Patel, Doo Kyung Kim, Tony X. Liu, Soo Hyun Kim, Longzhi Tan, Leili Mortazavi, Arjay Cordero, Jenny Shi, Mingming Zhao, Theodore T. Ho, Ailey Crow, Ai-Chi Wang Yoo, Cephra Raja, Kathryn Evans, Daniel Bernstein, Michael Zeineh, Maged Goubran and Karl Deisseroth ()
Additional contact information
Brian Hsueh: Stanford University
Ritchie Chen: Stanford University
YoungJu Jo: Stanford University
Daniel Tang: Stanford University
Misha Raffiee: Stanford University
Yoon Seok Kim: Stanford University
Masatoshi Inoue: Stanford University
Sawyer Randles: Stanford University
Charu Ramakrishnan: Stanford University
Sneha Patel: Stanford University
Doo Kyung Kim: Stanford University
Tony X. Liu: Stanford University
Soo Hyun Kim: Stanford University
Longzhi Tan: Stanford University
Leili Mortazavi: Stanford University
Arjay Cordero: Stanford University
Jenny Shi: Stanford University
Mingming Zhao: Stanford University
Theodore T. Ho: Stanford University
Ailey Crow: Stanford University
Ai-Chi Wang Yoo: Stanford University
Cephra Raja: Stanford University
Kathryn Evans: Stanford University
Daniel Bernstein: Stanford University
Michael Zeineh: Stanford University
Maged Goubran: Stanford University
Karl Deisseroth: Stanford University

Nature, 2023, vol. 615, issue 7951, 292-299

Abstract: Abstract Emotional states influence bodily physiology, as exemplified in the top-down process by which anxiety causes faster beating of the heart1–3. However, whether an increased heart rate might itself induce anxiety or fear responses is unclear3–8. Physiological theories of emotion, proposed over a century ago, have considered that in general, there could be an important and even dominant flow of information from the body to the brain9. Here, to formally test this idea, we developed a noninvasive optogenetic pacemaker for precise, cell-type-specific control of cardiac rhythms of up to 900 beats per minute in freely moving mice, enabled by a wearable micro-LED harness and the systemic viral delivery of a potent pump-like channelrhodopsin. We found that optically evoked tachycardia potently enhanced anxiety-like behaviour, but crucially only in risky contexts, indicating that both central (brain) and peripheral (body) processes may be involved in the development of emotional states. To identify potential mechanisms, we used whole-brain activity screening and electrophysiology to find brain regions that were activated by imposed cardiac rhythms. We identified the posterior insular cortex as a potential mediator of bottom-up cardiac interoceptive processing, and found that optogenetic inhibition of this brain region attenuated the anxiety-like behaviour that was induced by optical cardiac pacing. Together, these findings reveal that cells of both the body and the brain must be considered together to understand the origins of emotional or affective states. More broadly, our results define a generalizable approach for noninvasive, temporally precise functional investigations of joint organism-wide interactions among targeted cells during behaviour.

Date: 2023
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DOI: 10.1038/s41586-023-05748-8

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