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Pain is believed to be relayed from the spinal cord to brain through two major ascending pathways. One arises largely from the superficial dorsal horn, primarily targets the parabrachial nucleus (PBN), and is thought to mediate the aversive component of pain. The other arises predominantly from the deep dorsal horn, primarily targets the rostral aspect of the ventral posterior lateral (VPL) thalamus, and is thought to mediate the discriminative component of pain. However, the precise roles of these two populations have been a subject of ongoing controversy. Here, we investigate the anatomy and function of these output pathways at a new level of detail. Our study provides evidence that spinal-PBN neurons and spinal rostral VPL (rVPL) neurons are two distinct populations with different molecular characteristics by in situ hybridization and distinct patterns of collateralization through separate axon tracts. Chemogenetic activation of spinal-PBN neurons elicited spontaneous site-oriented nociceptive behavior (flinching/guarding and licking), and their collateral terminals were somatotopically organized in periductal gray (PAG) and caudal VPL. Moreover, optogenetic activation of different terminals of spinal-PBN neurons elicited distinct nociceptive behaviors. Meanwhile, chemogentic activation of spinal-rVPL neurons did not elicit spontaneous nociceptive behavior. Conversely, chemogenetically inhibiting spinal-rVPL neurons or VPL excitatory neurons did not affect pain behaviors but gave rise to a defect in fine motor coordination. Together, these findings challenge the current dogma and suggest that superficial spinal output neurons have a prominent role in conveying pain to the brain, whereas deep layer spinal output neurons are more likely to be involved in sensorimotor integration.
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