Dynamic changes in interneuron morphophysiological properties mark the maturation of hippocampal network activity

Camille Allene, Michel A. Picardo, Hélène Becq, Goichi Miyoshi, Gordon Fishell, Rosa Cossart

    Research output: Contribution to journalArticle

    Abstract

    During early postnatal development, neuronal networks successively produce various forms of spontaneous patterned activity that provide key signals for circuit maturation. Initially, in both rodent hippocampus and neocortex, coordinated activity emerges in the form of synchronous plateau assemblies (SPAs) that are initiated by sparse groups of gap-junction-coupled oscillating neurons. Subsequently, SPAs are replaced by synapse-driven giant depolarizing potentials (GDPs). Whether these sequential changes in mechanistically distinct network activities correlate with modifications in single-cell properties is unknown. To determine this, we studied the morphophysiological fate of single SPA cells as a function of development. We focused on CA3 GABAergic interneurons, which are centrally involved in generating GDPs in the hippocampus. As the network matures, GABAergic neurons are engaged more in GDPs and less in SPAs. Using inducible genetic fate mapping, we show that the individual involvement of GABAergic neurons in SPAs is correlated to their temporal origin. In addition, we demonstrate that the SPA-to-GDP transition is paralleled by a remarkable maturation in the morphophysiological properties of GABAergic neurons. Compared with those involved in GDPs, interneurons participating in SPAs possess immature intrinsic properties, receive synaptic inputs spanning awide amplitude range, and display large so mata as well as membrane protrusions. Thus, a developmental switch in the morphophysiological properties of GABAergic interneurons as they progress from SPAs to GDPs marks the emergence of synapse-driven network oscillations.

    Original languageEnglish (US)
    Pages (from-to)6688-6698
    Number of pages11
    JournalJournal of Neuroscience
    Volume32
    Issue number19
    DOIs
    StatePublished - May 9 2012

    Fingerprint

    GABAergic Neurons
    Interneurons
    Synapses
    Hippocampus
    Gap Junctions
    Neocortex
    Rodentia
    Neurons
    Membranes

    ASJC Scopus subject areas

    • Neuroscience(all)

    Cite this

    Dynamic changes in interneuron morphophysiological properties mark the maturation of hippocampal network activity. / Allene, Camille; Picardo, Michel A.; Becq, Hélène; Miyoshi, Goichi; Fishell, Gordon; Cossart, Rosa.

    In: Journal of Neuroscience, Vol. 32, No. 19, 09.05.2012, p. 6688-6698.

    Research output: Contribution to journalArticle

    Allene, Camille ; Picardo, Michel A. ; Becq, Hélène ; Miyoshi, Goichi ; Fishell, Gordon ; Cossart, Rosa. / Dynamic changes in interneuron morphophysiological properties mark the maturation of hippocampal network activity. In: Journal of Neuroscience. 2012 ; Vol. 32, No. 19. pp. 6688-6698.
    @article{5fdf21686a6747cf8a52a1139b529047,
    title = "Dynamic changes in interneuron morphophysiological properties mark the maturation of hippocampal network activity",
    abstract = "During early postnatal development, neuronal networks successively produce various forms of spontaneous patterned activity that provide key signals for circuit maturation. Initially, in both rodent hippocampus and neocortex, coordinated activity emerges in the form of synchronous plateau assemblies (SPAs) that are initiated by sparse groups of gap-junction-coupled oscillating neurons. Subsequently, SPAs are replaced by synapse-driven giant depolarizing potentials (GDPs). Whether these sequential changes in mechanistically distinct network activities correlate with modifications in single-cell properties is unknown. To determine this, we studied the morphophysiological fate of single SPA cells as a function of development. We focused on CA3 GABAergic interneurons, which are centrally involved in generating GDPs in the hippocampus. As the network matures, GABAergic neurons are engaged more in GDPs and less in SPAs. Using inducible genetic fate mapping, we show that the individual involvement of GABAergic neurons in SPAs is correlated to their temporal origin. In addition, we demonstrate that the SPA-to-GDP transition is paralleled by a remarkable maturation in the morphophysiological properties of GABAergic neurons. Compared with those involved in GDPs, interneurons participating in SPAs possess immature intrinsic properties, receive synaptic inputs spanning awide amplitude range, and display large so mata as well as membrane protrusions. Thus, a developmental switch in the morphophysiological properties of GABAergic interneurons as they progress from SPAs to GDPs marks the emergence of synapse-driven network oscillations.",
    author = "Camille Allene and Picardo, {Michel A.} and H{\'e}l{\`e}ne Becq and Goichi Miyoshi and Gordon Fishell and Rosa Cossart",
    year = "2012",
    month = "5",
    day = "9",
    doi = "10.1523/JNEUROSCI.0081-12.2012",
    language = "English (US)",
    volume = "32",
    pages = "6688--6698",
    journal = "Journal of Neuroscience",
    issn = "0270-6474",
    publisher = "Society for Neuroscience",
    number = "19",

    }

    TY - JOUR

    T1 - Dynamic changes in interneuron morphophysiological properties mark the maturation of hippocampal network activity

    AU - Allene, Camille

    AU - Picardo, Michel A.

    AU - Becq, Hélène

    AU - Miyoshi, Goichi

    AU - Fishell, Gordon

    AU - Cossart, Rosa

    PY - 2012/5/9

    Y1 - 2012/5/9

    N2 - During early postnatal development, neuronal networks successively produce various forms of spontaneous patterned activity that provide key signals for circuit maturation. Initially, in both rodent hippocampus and neocortex, coordinated activity emerges in the form of synchronous plateau assemblies (SPAs) that are initiated by sparse groups of gap-junction-coupled oscillating neurons. Subsequently, SPAs are replaced by synapse-driven giant depolarizing potentials (GDPs). Whether these sequential changes in mechanistically distinct network activities correlate with modifications in single-cell properties is unknown. To determine this, we studied the morphophysiological fate of single SPA cells as a function of development. We focused on CA3 GABAergic interneurons, which are centrally involved in generating GDPs in the hippocampus. As the network matures, GABAergic neurons are engaged more in GDPs and less in SPAs. Using inducible genetic fate mapping, we show that the individual involvement of GABAergic neurons in SPAs is correlated to their temporal origin. In addition, we demonstrate that the SPA-to-GDP transition is paralleled by a remarkable maturation in the morphophysiological properties of GABAergic neurons. Compared with those involved in GDPs, interneurons participating in SPAs possess immature intrinsic properties, receive synaptic inputs spanning awide amplitude range, and display large so mata as well as membrane protrusions. Thus, a developmental switch in the morphophysiological properties of GABAergic interneurons as they progress from SPAs to GDPs marks the emergence of synapse-driven network oscillations.

    AB - During early postnatal development, neuronal networks successively produce various forms of spontaneous patterned activity that provide key signals for circuit maturation. Initially, in both rodent hippocampus and neocortex, coordinated activity emerges in the form of synchronous plateau assemblies (SPAs) that are initiated by sparse groups of gap-junction-coupled oscillating neurons. Subsequently, SPAs are replaced by synapse-driven giant depolarizing potentials (GDPs). Whether these sequential changes in mechanistically distinct network activities correlate with modifications in single-cell properties is unknown. To determine this, we studied the morphophysiological fate of single SPA cells as a function of development. We focused on CA3 GABAergic interneurons, which are centrally involved in generating GDPs in the hippocampus. As the network matures, GABAergic neurons are engaged more in GDPs and less in SPAs. Using inducible genetic fate mapping, we show that the individual involvement of GABAergic neurons in SPAs is correlated to their temporal origin. In addition, we demonstrate that the SPA-to-GDP transition is paralleled by a remarkable maturation in the morphophysiological properties of GABAergic neurons. Compared with those involved in GDPs, interneurons participating in SPAs possess immature intrinsic properties, receive synaptic inputs spanning awide amplitude range, and display large so mata as well as membrane protrusions. Thus, a developmental switch in the morphophysiological properties of GABAergic interneurons as they progress from SPAs to GDPs marks the emergence of synapse-driven network oscillations.

    UR - http://www.scopus.com/inward/record.url?scp=84860653952&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=84860653952&partnerID=8YFLogxK

    U2 - 10.1523/JNEUROSCI.0081-12.2012

    DO - 10.1523/JNEUROSCI.0081-12.2012

    M3 - Article

    VL - 32

    SP - 6688

    EP - 6698

    JO - Journal of Neuroscience

    JF - Journal of Neuroscience

    SN - 0270-6474

    IS - 19

    ER -