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

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The Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn

Journal article

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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, …

Cell (Cambridge), Vol.168(1-2), pp.295-310.e19

12/29/2016

DOI: https://doi.org/10.1016/j.cell.2016.12.010

PMCID: PMC5236062

PMID: 28041852

Abstract

somatosensation

synaptic connectivity

low-threshold mechanoreceptors

mouse molecular genetics

spinal cord interneurons

spinal cord dorsal horn

Genetics

Neuroscience

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. [Display omitted] •Convergent LTMR and cortical inputs define the mechanosensory dorsal horn•A dorsal horn molecular-genetic toolbox defines 11 interneuron subtypes•Dorsal horn interneurons receive specific patterns of cortical and LTMR inputs•Dorsal horn interneurons modulate output pathways and tactile perception The blueprint of dorsal horn reveals the organizational logic of the low-threshold mechanoreceptor-recipient zone that is essential for tactile perception.

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Title: The Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn
Creators: Victoria E Abraira - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Emily D Kuehn - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Anda M Chirila - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Mark W Springel - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Alexis A Toliver - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Amanda L Zimmerman - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Lauren L Orefice - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Kieran A Boyle - Institute of Neuroscience and Psychology, University of Glasgow, Glasgow G12 8QQ, UK
Ling Bai - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Bryan J Song - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Karleena A Bashista - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Thomas G O'Neill - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Justin Zhuo - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Connie Tsan - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Jessica Hoynoski - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Michael Rutlin - Department of Biology and National Center for Behavioral Genomics, Brandeis University, Waltham, MA 02453, USA
Laura Kus - The Laboratory of Molecular Biology, Howard Hughes Medical Institute, The Rockefeller University, New York, NY 10065, USA
Vera Niederkofler - Department of Genetics, Harvard Medical School, 77 Avenue Louis Pasteur, Boston, MA 02115, USA
Masahiko Watanabe - Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060-8638, Japan
Susan M Dymecki - Department of Genetics, Harvard Medical School, 77 Avenue Louis Pasteur, Boston, MA 02115, USA
Sacha B Nelson (Author) - Department of Biology and National Center for Behavioral Genomics, Brandeis University, Waltham, MA 02453, USA
Nathaniel Heintz - The Laboratory of Molecular Biology, Howard Hughes Medical Institute, The Rockefeller University, New York, NY 10065, USA
David I Hughes - Institute of Neuroscience and Psychology, University of Glasgow, Glasgow G12 8QQ, UK
David D Ginty - Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA
Publication Details: Cell (Cambridge), Vol.168(1-2), pp.295-310.e19
Publisher: Elsevier Inc
Identifiers: 9923974393701921
Academic Unit: Department of Biology; Benjamin and Mae Volen National Center for Complex Systems; Interdepartmental Program in Neuroscience
Language: English
Resource Type: Journal article

The Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn

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