TY - JOUR
T1 - Tiling and somatotopic alignment of mammalian low-threshold mechanoreceptors
AU - Kuehn, Emily D.
AU - Meltzer, Shan
AU - Abraira, Victoria E.
AU - Ho, Cheng Ying
AU - Ginty, David D.
N1 - Funding Information:
We thank Katherine West, Connie Tsan, Katelyn Comeau, and Annie Chen for expert technical support; and D.D.G. laboratory members for discussions and comments on the manuscript. This work was supported by NIH Grants 5R35NS097344-02 (to D.D.G.) and 1F32NS108507-01 (to S.M.); a Hanna Gray fellowship (to S.M.); and the Edward R. and Anne G. Lefler Center for the Study of Neurodegenerative Disorders (D.D.G.). D.D.G. is an investigator of the Howard Hughes Medical Institute.
Funding Information:
ACKNOWLEDGMENTS. We thank Katherine West, Connie Tsan, Katelyn Comeau, and Annie Chen for expert technical support; and D.D.G. laboratory members for discussions and comments on the manuscript. This work was supported by NIH Grants 5R35NS097344-02 (to D.D.G.) and 1F32NS108507-01 (to S.M.); a Hanna Gray fellowship (to S.M.); and the Edward R. and Anne G. Lefler Center for the Study of Neurodegenerative Disorders (D.D.G.). D.D.G. is an investigator of the Howard Hughes Medical Institute.
Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.
PY - 2019/5/7
Y1 - 2019/5/7
N2 - Innocuous mechanical stimuli acting on the skin are detected by sensory neurons, known as low-threshold mechanoreceptors (LTMRs). LTMRs are classified based on their response properties, action potential conduction velocity, rate of adaptation to static indentation of the skin, and terminal anatomy. Here, we report organizational properties of the cutaneous and central axonal projections of the five principal hairy skin LTMR subtypes. We find that axons of neurons within a particular LTMR class are largely nonoverlapping with respect to their cutaneous end organs (e.g., hair follicles), with Aβ rapidly adapting-LTMRs being the sole exception. Individual neurons of each LTMR class are mostly nonoverlapping with respect to their associated hair follicles, with the notable exception of C-LTMRs, which exhibit multiple branches that redundantly innervate individual hair follicles. In the spinal cord, LTMR central projections exhibit rostrocaudal elongation and mediolateral compression, compared with their cutaneous innervation patterns, and these central projections also exhibit a fine degree of homotypic topographic adjacency. These findings thus reveal homotypic tiling of LTMR subtype axonal projections in hairy skin and a remarkable degree of spatial precision of spinal cord axonal termination patterns, suggesting a somatotopically precise tactile encoding capability of the mechanosensory dorsal horn.
AB - Innocuous mechanical stimuli acting on the skin are detected by sensory neurons, known as low-threshold mechanoreceptors (LTMRs). LTMRs are classified based on their response properties, action potential conduction velocity, rate of adaptation to static indentation of the skin, and terminal anatomy. Here, we report organizational properties of the cutaneous and central axonal projections of the five principal hairy skin LTMR subtypes. We find that axons of neurons within a particular LTMR class are largely nonoverlapping with respect to their cutaneous end organs (e.g., hair follicles), with Aβ rapidly adapting-LTMRs being the sole exception. Individual neurons of each LTMR class are mostly nonoverlapping with respect to their associated hair follicles, with the notable exception of C-LTMRs, which exhibit multiple branches that redundantly innervate individual hair follicles. In the spinal cord, LTMR central projections exhibit rostrocaudal elongation and mediolateral compression, compared with their cutaneous innervation patterns, and these central projections also exhibit a fine degree of homotypic topographic adjacency. These findings thus reveal homotypic tiling of LTMR subtype axonal projections in hairy skin and a remarkable degree of spatial precision of spinal cord axonal termination patterns, suggesting a somatotopically precise tactile encoding capability of the mechanosensory dorsal horn.
KW - Mechanosensory
KW - Somatosensation
KW - Somatotopy
KW - Tiling
UR - http://www.scopus.com/inward/record.url?scp=85065626990&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85065626990&partnerID=8YFLogxK
U2 - 10.1073/pnas.1901378116
DO - 10.1073/pnas.1901378116
M3 - Article
C2 - 30996124
AN - SCOPUS:85065626990
VL - 116
SP - 9168
EP - 9177
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 19
ER -