Parallel ascending spinal pathways for affective touch and pain

Seungwon Choi, Junichi Hachisuka, Matthew A. Brett, Alexandra R. Magee, Yu Omori, Noor-ul-Aine Iqbal, Dawei Zhang, Michelle M. DeLisle, Rachel L. Wolfson, Ling Bai, Celine Santiago, Shiaoching Gong, Martyn Goulding, Nathaniel Heintz, H. Richard Koerber, Sarah E. Ross and David D. Ginty ()
Additional contact information
Seungwon Choi: Howard Hughes Medical Institute, Harvard Medical School
Junichi Hachisuka: University of Pittsburgh
Matthew A. Brett: Howard Hughes Medical Institute, Harvard Medical School
Alexandra R. Magee: Howard Hughes Medical Institute, Harvard Medical School
Yu Omori: University of Pittsburgh
Noor-ul-Aine Iqbal: Howard Hughes Medical Institute, Harvard Medical School
Dawei Zhang: Howard Hughes Medical Institute, Harvard Medical School
Michelle M. DeLisle: Howard Hughes Medical Institute, Harvard Medical School
Rachel L. Wolfson: Howard Hughes Medical Institute, Harvard Medical School
Ling Bai: Howard Hughes Medical Institute, Harvard Medical School
Celine Santiago: Howard Hughes Medical Institute, Harvard Medical School
Shiaoching Gong: The Rockefeller University
Martyn Goulding: The Salk Institute for Biological Studies
Nathaniel Heintz: The Rockefeller University
H. Richard Koerber: University of Pittsburgh
Sarah E. Ross: University of Pittsburgh
David D. Ginty: Howard Hughes Medical Institute, Harvard Medical School

Nature, 2020, vol. 587, issue 7833, 258-263

Abstract: Abstract The anterolateral pathway consists of ascending spinal tracts that convey pain, temperature and touch information from the spinal cord to the brain1–4. Projection neurons of the anterolateral pathway are attractive therapeutic targets for pain treatment because nociceptive signals emanating from the periphery are channelled through these spinal projection neurons en route to the brain. However, the organizational logic of the anterolateral pathway remains poorly understood. Here we show that two populations of projection neurons that express the structurally related G-protein-coupled receptors (GPCRs) TACR1 and GPR83 form parallel ascending circuit modules that cooperate to convey thermal, tactile and noxious cutaneous signals from the spinal cord to the lateral parabrachial nucleus of the pons. Within this nucleus, axons of spinoparabrachial (SPB) neurons that express Tacr1 or Gpr83 innervate distinct sets of subnuclei, and strong optogenetic stimulation of the axon terminals induces distinct escape behaviours and autonomic responses. Moreover, SPB neurons that express Gpr83 are highly sensitive to cutaneous mechanical stimuli and receive strong synaptic inputs from both high- and low-threshold primary mechanosensory neurons. Notably, the valence associated with activation of SPB neurons that express Gpr83 can be either positive or negative, depending on stimulus intensity. These findings reveal anatomically, physiologically and functionally distinct subdivisions of the SPB tract that underlie affective aspects of touch and pain.

Date: 2020
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DOI: 10.1038/s41586-020-2860-1

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