Neuronal activity is required for the development of specific cortical interneuron subtypes

Natalia V. De Marco García, Theofanis Karayannis, Gordon Fishell

    Research output: Contribution to journalArticle

    Abstract

    Electrical activity has been shown to regulate development in a variety of species and in various structures, including the retina, spinal cord and cortex. Within the mammalian cortex specifically, the development of dendrites and commissural axons in pyramidal cells is activity-dependent. However, little is known about the developmental role of activity in the other major cortical population of neurons, the GABA-producing interneurons. These neurons are morphologically and functionally heterogeneous and efforts over the past decade have focused on determining the mechanisms that contribute to this diversity. It was recently discovered that 30% of all cortical interneurons arise from a relatively novel source within the ventral telencephalon, the caudal ganglionic eminence (CGE). Owing to their late birth date, these interneurons populate the cortex only after the majority of other interneurons and pyramidal cells are already in place and have started to functionally integrate. Here we demonstrate in mice that for CGE-derived reelin (Re)-positive and calretinin (Cr)-positive (but not vasoactive intestinal peptide (VIP)-positive) interneurons, activity is essential before postnatal day 3 for correct migration, and that after postnatal day 3, glutamate-mediated activity controls the development of their axons and dendrites. Furthermore, we show that the engulfment and cell motility 1 gene (Elmo1), a target of the transcription factor distal-less homeobox 1 (Dlx1), is selectively expressed in Re + and Cr + interneurons and is both necessary and sufficient for activity-dependent interneuron migration. Our findings reveal a selective requirement for activity in shaping the cortical integration of specific neuronal subtypes.

    Original languageEnglish (US)
    Pages (from-to)351-355
    Number of pages5
    JournalNature
    Volume472
    Issue number7343
    DOIs
    StatePublished - Apr 21 2011

    Fingerprint

    Interneurons
    Calbindin 2
    Pyramidal Cells
    Dendrites
    Axons
    GABAergic Neurons
    Telencephalon
    Homeobox Genes
    Vasoactive Intestinal Peptide
    Cell Movement
    Retina
    Glutamic Acid
    Spinal Cord
    Transcription Factors
    Parturition
    Neurons
    Population
    Genes

    ASJC Scopus subject areas

    • Medicine(all)
    • General

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    Neuronal activity is required for the development of specific cortical interneuron subtypes. / De Marco García, Natalia V.; Karayannis, Theofanis; Fishell, Gordon.

    In: Nature, Vol. 472, No. 7343, 21.04.2011, p. 351-355.

    Research output: Contribution to journalArticle

    De Marco García, NV, Karayannis, T & Fishell, G 2011, 'Neuronal activity is required for the development of specific cortical interneuron subtypes', Nature, vol. 472, no. 7343, pp. 351-355. https://doi.org/10.1038/nature09865
    De Marco García, Natalia V. ; Karayannis, Theofanis ; Fishell, Gordon. / Neuronal activity is required for the development of specific cortical interneuron subtypes. In: Nature. 2011 ; Vol. 472, No. 7343. pp. 351-355.
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