The Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn

Victoria E. Abraira; Emily D. Kuehn; Anda M. Chirila; Mark W. Springel; Alexis A. Toliver; Amanda L. Zimmerman; Lauren L. Orefice; Kieran A. Boyle; Ling Bai; Bryan J. Song; Karleena A. Bashista; Thomas G. O'Neill; Justin Zhuo; Connie Tsan; Jessica Hoynoski; Michael Rutlin; Laura Kus; Vera Niederkofler; Masahiko Watanabe; Susan M. Dymecki; Sacha B. Nelson; Nathaniel Heintz; David I. Hughes; David D. Ginty

doi:10.1016/j.cell.2016.12.010

The Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn

Victoria E. Abraira, Emily D. Kuehn, Anda M. Chirila, Mark W. Springel, Alexis A. Toliver, Amanda L. Zimmerman, Lauren L. Orefice, Kieran A. Boyle, Ling Bai, Bryan J. Song, Karleena A. Bashista, Thomas G. O'Neill, Justin Zhuo, Connie Tsan, Jessica Hoynoski, Michael Rutlin, Laura Kus, Vera Niederkofler, Masahiko Watanabe, Susan M. DymeckiSacha B. Nelson, Nathaniel Heintz, David I. Hughes, David D. Ginty

Research output: Contribution to journal › Article › peer-review

121 Scopus citations

Abstract

The deep dorsal horn is a poorly characterized spinal cord region implicated in processing low-threshold mechanoreceptor (LTMR) information. We report an array of mouse genetic tools for defining neuronal components and functions of the dorsal horn LTMR-recipient zone (LTMR-RZ), a role for LTMR-RZ processing in tactile perception, and the basic logic of LTMR-RZ organization. We found an unexpectedly high degree of neuronal diversity in the LTMR-RZ: seven excitatory and four inhibitory subtypes of interneurons exhibiting unique morphological, physiological, and synaptic properties. Remarkably, LTMRs form synapses on between four and 11 LTMR-RZ interneuron subtypes, while each LTMR-RZ interneuron subtype samples inputs from at least one to three LTMR classes, as well as spinal cord interneurons and corticospinal neurons. Thus, the LTMR-RZ is a somatosensory processing region endowed with a neuronal complexity that rivals the retina and functions to pattern the activity of ascending touch pathways that underlie tactile perception.

Original language	English (US)
Pages (from-to)	295-310.e19
Journal	Cell
Volume	168
Issue number	1-2
DOIs	https://doi.org/10.1016/j.cell.2016.12.010
State	Published - Jan 12 2017
Externally published	Yes

Keywords

low-threshold mechanoreceptors
mouse molecular genetics
somatosensation
spinal cord dorsal horn
spinal cord interneurons
synaptic connectivity

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2016.12.010

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Abraira, V. E., Kuehn, E. D., Chirila, A. M., Springel, M. W., Toliver, A. A., Zimmerman, A. L., Orefice, L. L., Boyle, K. A., Bai, L., Song, B. J., Bashista, K. A., O'Neill, T. G., Zhuo, J., Tsan, C., Hoynoski, J., Rutlin, M., Kus, L., Niederkofler, V., Watanabe, M., ... Ginty, D. D. (2017). The Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn. Cell, 168(1-2), 295-310.e19. https://doi.org/10.1016/j.cell.2016.12.010

Abraira, VE, Kuehn, ED, Chirila, AM, Springel, MW, Toliver, AA, Zimmerman, AL, Orefice, LL, Boyle, KA, Bai, L, Song, BJ, Bashista, KA, O'Neill, TG, Zhuo, J, Tsan, C, Hoynoski, J, Rutlin, M, Kus, L, Niederkofler, V, Watanabe, M, Dymecki, SM, Nelson, SB, Heintz, N, Hughes, DI & Ginty, DD 2017, 'The Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn', Cell, vol. 168, no. 1-2, pp. 295-310.e19. https://doi.org/10.1016/j.cell.2016.12.010

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title = "The Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn",

abstract = "The deep dorsal horn is a poorly characterized spinal cord region implicated in processing low-threshold mechanoreceptor (LTMR) information. We report an array of mouse genetic tools for defining neuronal components and functions of the dorsal horn LTMR-recipient zone (LTMR-RZ), a role for LTMR-RZ processing in tactile perception, and the basic logic of LTMR-RZ organization. We found an unexpectedly high degree of neuronal diversity in the LTMR-RZ: seven excitatory and four inhibitory subtypes of interneurons exhibiting unique morphological, physiological, and synaptic properties. Remarkably, LTMRs form synapses on between four and 11 LTMR-RZ interneuron subtypes, while each LTMR-RZ interneuron subtype samples inputs from at least one to three LTMR classes, as well as spinal cord interneurons and corticospinal neurons. Thus, the LTMR-RZ is a somatosensory processing region endowed with a neuronal complexity that rivals the retina and functions to pattern the activity of ascending touch pathways that underlie tactile perception.",

keywords = "low-threshold mechanoreceptors, mouse molecular genetics, somatosensation, spinal cord dorsal horn, spinal cord interneurons, synaptic connectivity",

author = "Abraira, {Victoria E.} and Kuehn, {Emily D.} and Chirila, {Anda M.} and Springel, {Mark W.} and Toliver, {Alexis A.} and Zimmerman, {Amanda L.} and Orefice, {Lauren L.} and Boyle, {Kieran A.} and Ling Bai and Song, {Bryan J.} and Bashista, {Karleena A.} and O'Neill, {Thomas G.} and Justin Zhuo and Connie Tsan and Jessica Hoynoski and Michael Rutlin and Laura Kus and Vera Niederkofler and Masahiko Watanabe and Dymecki, {Susan M.} and Nelson, {Sacha B.} and Nathaniel Heintz and Hughes, {David I.} and Ginty, {David D.}",

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doi = "10.1016/j.cell.2016.12.010",

language = "English (US)",

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AU - Abraira, Victoria E.

AU - Kuehn, Emily D.

AU - Chirila, Anda M.

AU - Springel, Mark W.

AU - Toliver, Alexis A.

AU - Zimmerman, Amanda L.

AU - Orefice, Lauren L.

AU - Boyle, Kieran A.

AU - Bai, Ling

AU - Song, Bryan J.

AU - Bashista, Karleena A.

AU - O'Neill, Thomas G.

AU - Zhuo, Justin

AU - Tsan, Connie

AU - Hoynoski, Jessica

AU - Rutlin, Michael

AU - Kus, Laura

AU - Niederkofler, Vera

AU - Watanabe, Masahiko

AU - Dymecki, Susan M.

AU - Nelson, Sacha B.

AU - Heintz, Nathaniel

AU - Hughes, David I.

AU - Ginty, David D.

PY - 2017/1/12

Y1 - 2017/1/12

N2 - The deep dorsal horn is a poorly characterized spinal cord region implicated in processing low-threshold mechanoreceptor (LTMR) information. We report an array of mouse genetic tools for defining neuronal components and functions of the dorsal horn LTMR-recipient zone (LTMR-RZ), a role for LTMR-RZ processing in tactile perception, and the basic logic of LTMR-RZ organization. We found an unexpectedly high degree of neuronal diversity in the LTMR-RZ: seven excitatory and four inhibitory subtypes of interneurons exhibiting unique morphological, physiological, and synaptic properties. Remarkably, LTMRs form synapses on between four and 11 LTMR-RZ interneuron subtypes, while each LTMR-RZ interneuron subtype samples inputs from at least one to three LTMR classes, as well as spinal cord interneurons and corticospinal neurons. Thus, the LTMR-RZ is a somatosensory processing region endowed with a neuronal complexity that rivals the retina and functions to pattern the activity of ascending touch pathways that underlie tactile perception.

AB - The deep dorsal horn is a poorly characterized spinal cord region implicated in processing low-threshold mechanoreceptor (LTMR) information. We report an array of mouse genetic tools for defining neuronal components and functions of the dorsal horn LTMR-recipient zone (LTMR-RZ), a role for LTMR-RZ processing in tactile perception, and the basic logic of LTMR-RZ organization. We found an unexpectedly high degree of neuronal diversity in the LTMR-RZ: seven excitatory and four inhibitory subtypes of interneurons exhibiting unique morphological, physiological, and synaptic properties. Remarkably, LTMRs form synapses on between four and 11 LTMR-RZ interneuron subtypes, while each LTMR-RZ interneuron subtype samples inputs from at least one to three LTMR classes, as well as spinal cord interneurons and corticospinal neurons. Thus, the LTMR-RZ is a somatosensory processing region endowed with a neuronal complexity that rivals the retina and functions to pattern the activity of ascending touch pathways that underlie tactile perception.

KW - low-threshold mechanoreceptors

KW - mouse molecular genetics

KW - somatosensation

KW - spinal cord dorsal horn

KW - spinal cord interneurons

KW - synaptic connectivity

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SP - 295-310.e19

JO - Cell

JF - Cell

IS - 1-2

ER -

The Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn

Abstract

Keywords

ASJC Scopus subject areas

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