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In-depth characterization of layer 5 output neurons of the primary somatosensory cortex innervating the mouse dorsal spinal cord

N. Frezel, J.M. Mateos, E. Platonova, U. Ziegler, H. Wildner, H.U. Zeilhofer
doi: https://doi.org/10.1101/2020.04.02.021311
N. Frezel
1Institute of Pharmacology and Toxicology, University of Zurich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
2Biologie Cellulaire de la Synapse, Inserm U1024, Institute of Biology, École Normale Supérieure (IBENS), 46 rue d’Ulm, Paris 75005, France
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J.M. Mateos
3Center for Microscopy and Image Analysis, University of Zürich, Zürich, Switzerland
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E. Platonova
3Center for Microscopy and Image Analysis, University of Zürich, Zürich, Switzerland
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U. Ziegler
3Center for Microscopy and Image Analysis, University of Zürich, Zürich, Switzerland
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H. Wildner
1Institute of Pharmacology and Toxicology, University of Zurich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
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  • For correspondence: zeilhofer@pharma.uzh.ch hwildner@pharma.uzh.ch
H.U. Zeilhofer
1Institute of Pharmacology and Toxicology, University of Zurich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
4Institute of Pharmaceutical Sciences, Swiss Federal Institute of Technology (ETH) Zürich, Vladimir-Prelog-Weg 1-5/10, CH-8090 Zürich, Switzerland
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  • For correspondence: zeilhofer@pharma.uzh.ch hwildner@pharma.uzh.ch
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Abstract

Neuronal circuits of the spinal dorsal horn integrate sensory information from the periphery with inhibitory and facilitating input from higher CNS areas. Most previous work focused on descending projections originating from the hindbrain. Less is known about the organisation of inputs descending from the cerebral cortex. Here, we identified cholecystokinin (CCK) positive layer 5 pyramidal neurons of the primary somatosensory cortex (S1-CST neurons) as a major source of descending input to the spinal dorsal horn. We combined intersectional genetics and virus-mediated gene transfer to characterize CCK+ S1-CST neurons and to define their presynaptic input and postsynaptic target neurons. We found that S1-CST neurons constitute a heterogeneous population that can be subdivided into distinct molecular subgroups. Rabies-based retrograde tracing revealed monosynaptic input from layer 2/3 pyramidal neurons, from parvalbumin (PV) and neuropeptide Y (NPY) positive cortical interneurons, and from thalamic relay neurons in the ventral posterolateral nucleus. WGA-based anterograde tracing identified postsynaptic target neurons in dorsal horn laminae III and IV. About 60% of these neurons were inhibitory and about 60% of all spinal target neurons expressed the transcription factor c-Maf. The heterogeneous nature of both S1-CST neurons and their spinal targets suggest sophisticated roles in the fine-tuning of sensory processing.

  • Abbreviations

    CST
    corticospinal tract
    rAAV
    recombinant adeno-associated virus
    RVM
    rostral ventromedial medulla
    S1
    primary somatosensory cortex
    S1hl
    hindlimb area of S1
    S1-CST
    corticospinal tract originating in S1
    7N
    facial nuclei
    ACC
    anterior cingulate cortex
    MnR
    median raphe nucleus
    PAG
    Periaqueductal grey
    S1hl
    somatosensory cortex, hindlimb area
    VPL
    ventral posterolateral nucleus of the thalamus
    WGA
    wheat germ agglutinin.
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    Posted April 03, 2020.
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    In-depth characterization of layer 5 output neurons of the primary somatosensory cortex innervating the mouse dorsal spinal cord
    N. Frezel, J.M. Mateos, E. Platonova, U. Ziegler, H. Wildner, H.U. Zeilhofer
    bioRxiv 2020.04.02.021311; doi: https://doi.org/10.1101/2020.04.02.021311
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    In-depth characterization of layer 5 output neurons of the primary somatosensory cortex innervating the mouse dorsal spinal cord
    N. Frezel, J.M. Mateos, E. Platonova, U. Ziegler, H. Wildner, H.U. Zeilhofer
    bioRxiv 2020.04.02.021311; doi: https://doi.org/10.1101/2020.04.02.021311

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