nNOS-expressing neurons in the vmPFC transform pPVT-derived chronic pain signals into anxiety behaviors

Hai-Ying Liang, Zhi-Jin Chen, Hui Xiao, Yu-Hui Lin, Ying-Yi Hu, Lei Chang, Hai-Yin Wu, Peng Wang, Wei Lu, Dong-Ya Zhu and Chun-Xia Luo ()
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Hai-Ying Liang: Nanjing Medical University
Zhi-Jin Chen: Nanjing Medical University
Hui Xiao: Nanjing Medical University
Yu-Hui Lin: Nanjing Medical University
Ying-Yi Hu: Nanjing Medical University
Lei Chang: Nanjing Medical University
Hai-Yin Wu: Nanjing Medical University
Peng Wang: Jiangsu Simcere Pharmaceutical Co. Ltd.
Wei Lu: Southeast University
Dong-Ya Zhu: Nanjing Medical University
Chun-Xia Luo: Nanjing Medical University

Nature Communications, 2020, vol. 11, issue 1, 1-18

Abstract: Abstract Anxiety is common in patients suffering from chronic pain. Here, we report anxiety-like behaviors in mouse models of chronic pain and reveal that nNOS-expressing neurons in ventromedial prefrontal cortex (vmPFC) are essential for pain-induced anxiety but not algesia, using optogenetic and chemogenetic strategies. Additionally, we determined that excitatory projections from the posterior subregion of paraventricular thalamic nucleus (pPVT) provide a neuronal input that drives the activation of vmPFC nNOS-expressing neurons in our chronic pain models. Our results suggest that the pain signal becomes an anxiety signal after activation of vmPFC nNOS-expressing neurons, which causes subsequent release of nitric oxide (NO). Finally, we show that the downstream molecular mechanisms of NO likely involve enhanced glutamate transmission in vmPFC CaMKIIα-expressing neurons through S-nitrosylation-induced AMPAR trafficking. Overall, our data suggest that pPVT excitatory neurons drive chronic pain-induced anxiety through activation of vmPFC nNOS-expressing neurons, resulting in NO-mediated AMPAR trafficking in vmPFC pyramidal neurons.

Date: 2020
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DOI: 10.1038/s41467-020-16198-5

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