Journal Article

Distinct thalamocortical circuits underlie allodynia induced by tissue injury and by depression-like states

Zhu, Xia, Zhou, Wenjie, Zhang, Zhi, Tao, Wenjuan, Li, Juan, Farzinpour, Zahra, Dong, Wan-Ying, Liu, An, Xie, Wen, Jin, Yan, Wang, Haitao, Kang, Fang, Zhang, Xulai, Xue, Tian, Zhang, Yan, Tang, Hao-Di, Mao, Yu, Song, Xiaoyuan, Cao, Peng

2021

Overview

In humans, tissue injury and depression can both cause pain hypersensitivity, but whether this involves distinct circuits remains unknown. Here, we identify two discrete glutamatergic neuronal circuits in male mice: a projection from the posterior thalamic nucleus (PO Glu ) to primary somatosensory cortex glutamatergic neurons (S1 Glu ) mediates allodynia from tissue injury, whereas a pathway from the parafascicular thalamic nucleus (PF Glu ) to anterior cingulate cortex GABA-containing neurons to glutamatergic neurons (ACC GABA→Glu ) mediates allodynia associated with a depression-like state. In vivo calcium imaging and multi-tetrode electrophysiological recordings reveal that PO Glu and PF Glu populations undergo different adaptations in the two conditions. Artificial manipulation of each circuit affects allodynia resulting from either tissue injury or depression-like states, but not both. Our study demonstrates that the distinct thalamocortical circuits PO Glu →S1 Glu and PF Glu →ACC GABA→Glu subserve allodynia associated with tissue injury and depression-like states, respectively, thus providing insights into the circuit basis of pathological pain resulting from different etiologies. Pain hypersensitivity can result from tissue injury and from depression. This study in mice shows that distinct thalamocortical pathways mediate allodynia associated with injury and a stress-induced depression-like state, respectively.

• Publisher: Nature Publishing Group US,Nature Publishing Group
• Subject: 13/51 / 14/19 / 14/69 / 631/378/3920 / 64/60 / 692/699/375/1692 / 9/74 / Adaptation / Animal Genetics and Genomics / Animals / Behavioral Sciences / Biological Techniques / Biomedical and Life Sciences / Biomedicine / Calcium / Calcium imaging / Circuits / Cortex (cingulate) / Cortex (somatosensory) / Depression - physiopathology / Depression, Mental / Development and progression / Etiology / Glutamatergic transmission / Health aspects / Hyperalgesia - physiopathology / Hypersensitivity / Injuries / Male / Mental depression / Mice / Neural circuitry / Neural Pathways - physiology / Neurobiology / Neuroimaging / Neurological research / Neurons / Neurons - physiology / Neurosciences / Pain / Pain perception / Parafascicular nucleus / Physiological aspects / Somatosensory Cortex - physiology / Thalamus / Thalamus - physiology / Tissues / γ-Aminobutyric acid