A disinhibitory circuit mediates motor integration in the somatosensory cortex

Soohyun Lee, Illya Kruglikov, Z. Josh Huang, Gordon Fishell, Bernardo Rudy

    Research output: Contribution to journalArticle

    Abstract

    The influence of motor activity on sensory processing is crucial for perception and motor execution. However, the underlying circuits are not known. To unravel the circuit by which activity in the primary vibrissal motor cortex (vM1) modulates sensory processing in the primary somatosensory barrel cortex (S1), we used optogenetics to examine the long-range inputs from vM1 to the various neuronal elements in S1. We found that S1-projecting vM1 pyramidal neurons strongly recruited vasointestinal peptide (VIP)-expressing GABAergic interneurons, a subset of serotonin receptor-expressing interneurons. These VIP interneurons preferentially inhibited somatostatin-expressing interneurons, neurons that target the distal dendrites of pyramidal cells. Consistent with this vM1-mediated disinhibitory circuit, the activity of VIP interneurons in vivo increased and that of somatostatin interneurons decreased during whisking. These changes in firing rates during whisking depended on vM1 activity. Our results suggest previously unknown circuitry by which inputs from motor cortex influence sensory processing in sensory cortex.

    Original languageEnglish (US)
    Pages (from-to)1662-1670
    Number of pages9
    JournalNature Neuroscience
    Volume16
    Issue number11
    DOIs
    StatePublished - Nov 1 2013

    Fingerprint

    Somatosensory Cortex
    Interneurons
    Vasoactive Intestinal Peptide
    Pyramidal Cells
    Somatostatin
    Optogenetics
    Serotonin Receptors
    Motor Cortex
    Dendrites
    Motor Activity
    Neurons

    ASJC Scopus subject areas

    • Neuroscience(all)

    Cite this

    Lee, S., Kruglikov, I., Huang, Z. J., Fishell, G., & Rudy, B. (2013). A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nature Neuroscience, 16(11), 1662-1670. https://doi.org/10.1038/nn.3544

    A disinhibitory circuit mediates motor integration in the somatosensory cortex. / Lee, Soohyun; Kruglikov, Illya; Huang, Z. Josh; Fishell, Gordon; Rudy, Bernardo.

    In: Nature Neuroscience, Vol. 16, No. 11, 01.11.2013, p. 1662-1670.

    Research output: Contribution to journalArticle

    Lee, S, Kruglikov, I, Huang, ZJ, Fishell, G & Rudy, B 2013, 'A disinhibitory circuit mediates motor integration in the somatosensory cortex', Nature Neuroscience, vol. 16, no. 11, pp. 1662-1670. https://doi.org/10.1038/nn.3544
    Lee, Soohyun ; Kruglikov, Illya ; Huang, Z. Josh ; Fishell, Gordon ; Rudy, Bernardo. / A disinhibitory circuit mediates motor integration in the somatosensory cortex. In: Nature Neuroscience. 2013 ; Vol. 16, No. 11. pp. 1662-1670.
    @article{697ca1aad95e41c9b0a6e29b29aa452d,
    title = "A disinhibitory circuit mediates motor integration in the somatosensory cortex",
    abstract = "The influence of motor activity on sensory processing is crucial for perception and motor execution. However, the underlying circuits are not known. To unravel the circuit by which activity in the primary vibrissal motor cortex (vM1) modulates sensory processing in the primary somatosensory barrel cortex (S1), we used optogenetics to examine the long-range inputs from vM1 to the various neuronal elements in S1. We found that S1-projecting vM1 pyramidal neurons strongly recruited vasointestinal peptide (VIP)-expressing GABAergic interneurons, a subset of serotonin receptor-expressing interneurons. These VIP interneurons preferentially inhibited somatostatin-expressing interneurons, neurons that target the distal dendrites of pyramidal cells. Consistent with this vM1-mediated disinhibitory circuit, the activity of VIP interneurons in vivo increased and that of somatostatin interneurons decreased during whisking. These changes in firing rates during whisking depended on vM1 activity. Our results suggest previously unknown circuitry by which inputs from motor cortex influence sensory processing in sensory cortex.",
    author = "Soohyun Lee and Illya Kruglikov and Huang, {Z. Josh} and Gordon Fishell and Bernardo Rudy",
    year = "2013",
    month = "11",
    day = "1",
    doi = "10.1038/nn.3544",
    language = "English (US)",
    volume = "16",
    pages = "1662--1670",
    journal = "Nature Neuroscience",
    issn = "1097-6256",
    publisher = "Nature Publishing Group",
    number = "11",

    }

    TY - JOUR

    T1 - A disinhibitory circuit mediates motor integration in the somatosensory cortex

    AU - Lee, Soohyun

    AU - Kruglikov, Illya

    AU - Huang, Z. Josh

    AU - Fishell, Gordon

    AU - Rudy, Bernardo

    PY - 2013/11/1

    Y1 - 2013/11/1

    N2 - The influence of motor activity on sensory processing is crucial for perception and motor execution. However, the underlying circuits are not known. To unravel the circuit by which activity in the primary vibrissal motor cortex (vM1) modulates sensory processing in the primary somatosensory barrel cortex (S1), we used optogenetics to examine the long-range inputs from vM1 to the various neuronal elements in S1. We found that S1-projecting vM1 pyramidal neurons strongly recruited vasointestinal peptide (VIP)-expressing GABAergic interneurons, a subset of serotonin receptor-expressing interneurons. These VIP interneurons preferentially inhibited somatostatin-expressing interneurons, neurons that target the distal dendrites of pyramidal cells. Consistent with this vM1-mediated disinhibitory circuit, the activity of VIP interneurons in vivo increased and that of somatostatin interneurons decreased during whisking. These changes in firing rates during whisking depended on vM1 activity. Our results suggest previously unknown circuitry by which inputs from motor cortex influence sensory processing in sensory cortex.

    AB - The influence of motor activity on sensory processing is crucial for perception and motor execution. However, the underlying circuits are not known. To unravel the circuit by which activity in the primary vibrissal motor cortex (vM1) modulates sensory processing in the primary somatosensory barrel cortex (S1), we used optogenetics to examine the long-range inputs from vM1 to the various neuronal elements in S1. We found that S1-projecting vM1 pyramidal neurons strongly recruited vasointestinal peptide (VIP)-expressing GABAergic interneurons, a subset of serotonin receptor-expressing interneurons. These VIP interneurons preferentially inhibited somatostatin-expressing interneurons, neurons that target the distal dendrites of pyramidal cells. Consistent with this vM1-mediated disinhibitory circuit, the activity of VIP interneurons in vivo increased and that of somatostatin interneurons decreased during whisking. These changes in firing rates during whisking depended on vM1 activity. Our results suggest previously unknown circuitry by which inputs from motor cortex influence sensory processing in sensory cortex.

    UR - http://www.scopus.com/inward/record.url?scp=84886950236&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=84886950236&partnerID=8YFLogxK

    U2 - 10.1038/nn.3544

    DO - 10.1038/nn.3544

    M3 - Article

    VL - 16

    SP - 1662

    EP - 1670

    JO - Nature Neuroscience

    JF - Nature Neuroscience

    SN - 1097-6256

    IS - 11

    ER -