Four unique interneuron populations reside in neocortical layer 1

Benjamin Schuman, Robert P. Machold, Yoshiko Hashikawa, János Fuzik, Gordon Fishell, Bernardo Rudy

    Research output: Contribution to journalArticle

    Abstract

    Sensory perception depends on neocortical computations that contextually adjust sensory signals in different internal and environmental contexts. Neocortical layer 1 (L1) is the main target of cortical and subcortical inputs that provide “top-down” information for context-dependent sensory processing. Although L1 is devoid of excitatory cells, it contains the distal “tuft” dendrites of pyramidal cells (PCs) located in deeper layers. L1 also contains a poorly characterized population of GABAergic interneurons (INs), which regulate the impact that different top-down inputs have on PCs. A poor comprehension of L1 IN subtypes and how they affect PC activity has hampered our understanding of the mechanisms that underlie contextual modulation of sensory processing. We used novel genetic strategies in male and female mice combined with electrophysiological and morphological methods to help resolve differences that were unclear when using only electrophysiological and/or morphological approaches. We discovered that L1 contains four distinct populations of INs, each with a unique molecular profile, morphology, and electrophysiology, including a previously overlooked IN population (named here “canopy cells”) representing 40% of L1 INs. In contrast to what is observed in other layers, most L1 neurons appear to be unique to the layer, highlighting the specialized character of the signal processing that takes place in L1. This new understanding of INs in L1, as well as the application of genetic methods based on the markers described here, will enable investigation of the cellular and circuit mechanisms of top-down processing in L1 with unprecedented detail.

    Original languageEnglish (US)
    Pages (from-to)125-139
    Number of pages15
    JournalJournal of Neuroscience
    Volume39
    Issue number1
    DOIs
    StatePublished - Jan 2 2019

    Fingerprint

    Interneurons
    Pyramidal Cells
    Population
    Electrophysiology
    Dendrites
    Neurons

    Keywords

    • Barrel cortex
    • Interneurons
    • Layer 1
    • Neocortex
    • Top-down modulation

    ASJC Scopus subject areas

    • Neuroscience(all)

    Cite this

    Schuman, B., Machold, R. P., Hashikawa, Y., Fuzik, J., Fishell, G., & Rudy, B. (2019). Four unique interneuron populations reside in neocortical layer 1. Journal of Neuroscience, 39(1), 125-139. https://doi.org/10.1523/JNEUROSCI.1613-18.2018

    Four unique interneuron populations reside in neocortical layer 1. / Schuman, Benjamin; Machold, Robert P.; Hashikawa, Yoshiko; Fuzik, János; Fishell, Gordon; Rudy, Bernardo.

    In: Journal of Neuroscience, Vol. 39, No. 1, 02.01.2019, p. 125-139.

    Research output: Contribution to journalArticle

    Schuman, B, Machold, RP, Hashikawa, Y, Fuzik, J, Fishell, G & Rudy, B 2019, 'Four unique interneuron populations reside in neocortical layer 1', Journal of Neuroscience, vol. 39, no. 1, pp. 125-139. https://doi.org/10.1523/JNEUROSCI.1613-18.2018
    Schuman B, Machold RP, Hashikawa Y, Fuzik J, Fishell G, Rudy B. Four unique interneuron populations reside in neocortical layer 1. Journal of Neuroscience. 2019 Jan 2;39(1):125-139. https://doi.org/10.1523/JNEUROSCI.1613-18.2018
    Schuman, Benjamin ; Machold, Robert P. ; Hashikawa, Yoshiko ; Fuzik, János ; Fishell, Gordon ; Rudy, Bernardo. / Four unique interneuron populations reside in neocortical layer 1. In: Journal of Neuroscience. 2019 ; Vol. 39, No. 1. pp. 125-139.
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