A non-canonical retina-ipRGCs-SCN-PVT visual pathway for mediating contagious itch behavior

• Published in: Cell reports (Cambridge) Vol. 41; no. 1; p. 111444
• Main Authors: Gao, Fang, Ma, Jun, Yu, Yao-Qing, Gao, Xiao-Fei, Bai, Yang, Sun, Yi, Liu, Juan, Liu, Xianyu, Barry, Devin M., Wilhelm, Steven, Piccinni-Ash, Tyler, Wang, Na, Liu, Dongyang, Ross, Rachel A., Hao, Yan, Huang, Xu, Jia, Jin-Jing, Yang, Qianyi, Zheng, Hao, van Nispen, Johan, Chen, Jun, Li, Hui, Zhang, Jiayi, Li, Yun-Qing, Chen, Zhou-Feng
• Format: Journal Article
• Language: English
• Published: Elsevier Inc 04-10-2022; Elsevier
• Subjects: contagious itch behavior; CP: Neuroscience; GRP; GRPR; ipRGCs; itch stimuli; neural dynamics; PACAP; SCN; scratching motion; stress; ipRGCs; stress; GRP; PACAP; scratching motion; CP: Neuroscience; neural dynamics; contagious itch behavior; GRPR; itch stimuli; SCN
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2022.111444

Contagious itch behavior informs conspecifics of adverse environment and is crucial for the survival of social animals. Gastrin-releasing peptide (GRP) and its receptor (GRPR) in the suprachiasmatic nucleus (SCN) of the hypothalamus mediates contagious itch behavior in mice. Here, we show that intrinsically photosensitive retina ganglion cells (ipRGCs) convey visual itch information, independently of melanopsin, from the retina to GRP neurons via PACAP-PAC1R signaling. Moreover, GRPR neurons relay itch information to the paraventricular nucleus of the thalamus (PVT). Surprisingly, neither the visual cortex nor superior colliculus is involved in contagious itch. In vivo calcium imaging and extracellular recordings reveal contagious itch-specific neural dynamics of GRPR neurons. Thus, we propose that the retina-ipRGC-SCN-PVT pathway constitutes a previously unknown visual pathway that probably evolved for motion vision that encodes salient environmental cues and enables animals to imitate behaviors of conspecifics as an anticipatory mechanism to cope with adverse conditions.
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•SCN-projecting ipRGCs are necessary and sufficient for contagious itch behavior•Melanopsin is not required for contagious itch behavior•PACAP transmits itch information to SCN GRP neurons via PAC1R•SCN GRPR neurons display itch-specific neural dynamics and firing patterns
It has been shown that GRP-GRPR neuropeptide signaling in the SCN is important for contagious itch behavior in mice. Gao et al. find that SCN-projecting ipRGCs are sufficient to relay itch information from the retina to the SCN by releasing neuropeptide PACAP to activate the GRP-GRPR pathway.