Xiphoid nucleus of the midline thalamus controls cold-induced food seeking

Neeraj K. Lal, Phuong Le, Samarth Aggarwal, Alan Zhang, Kristina Wang, Tianbo Qi, Zhengyuan Pang, Dong Yang, Victoria Nudell, Gene W. Yeo, Alexander S. Banks and Li Ye ()
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Neeraj K. Lal: The Scripps Research Institute
Phuong Le: University of California San Diego
Samarth Aggarwal: The Scripps Research Institute
Alan Zhang: The Scripps Research Institute
Kristina Wang: The Scripps Research Institute
Tianbo Qi: The Scripps Research Institute
Zhengyuan Pang: The Scripps Research Institute
Dong Yang: The Scripps Research Institute
Victoria Nudell: The Scripps Research Institute
Gene W. Yeo: University of California San Diego
Alexander S. Banks: Beth Israel Deaconess Medical Center
Li Ye: The Scripps Research Institute

Nature, 2023, vol. 621, issue 7977, 138-145

Abstract: Abstract Maintaining body temperature is calorically expensive for endothermic animals1. Mammals eat more in the cold to compensate for energy expenditure2, but the neural mechanism underlying this coupling is not well understood. Through behavioural and metabolic analyses, we found that mice dynamically switch between energy-conservation and food-seeking states in the cold, the latter of which are primarily driven by energy expenditure rather than the sensation of cold. To identify the neural mechanisms underlying cold-induced food seeking, we used whole-brain c-Fos mapping and found that the xiphoid (Xi), a small nucleus in the midline thalamus, was selectively activated by prolonged cold associated with elevated energy expenditure but not with acute cold exposure. In vivo calcium imaging showed that Xi activity correlates with food-seeking episodes under cold conditions. Using activity-dependent viral strategies, we found that optogenetic and chemogenetic stimulation of cold-activated Xi neurons selectively recapitulated food seeking under cold conditions whereas their inhibition suppressed it. Mechanistically, Xi encodes a context-dependent valence switch that promotes food-seeking behaviours under cold but not warm conditions. Furthermore, these behaviours are mediated by a Xi-to-nucleus accumbens projection. Our results establish Xi as a key region in the control of cold-induced feeding, which is an important mechanism in the maintenance of energy homeostasis in endothermic animals.

Date: 2023
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DOI: 10.1038/s41586-023-06430-9

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