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Cited by 309Neuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanismsNeural dynamics and brain function

Transcriptional and Electrophysiological Maturation of Neocortical Fast-Spiking GABAergic Interneurons

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Okaty, Benjamin W., Miller, Mark N., Sugino, Ken, Hempel, Chris M., Nelson, Sacha B.·2009·The Journal of Neuroscience
DOI 10.1523/jneurosci.0105-09.2009PMC PMC2749660
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Abstract

Fast-spiking (FS) interneurons are important elements of neocortical circuitry that constitute the primary source of synaptic inhibition in adult cortex and impart temporal organization on ongoing cortical activity. The highly specialized intrinsic membrane and firing properties that allow cortical FS interneurons to perform these functions are attributable to equally specialized gene expression, which is ultimately coordinated by cell-type-specific transcriptional regulation. Although embryonic transcriptional events govern the initial steps of cell-type specification in most cortical interneurons, including FS cells, the electrophysiological properties that distinguish adult cortical cell types emerge relatively late in postnatal development, and the transcriptional events that drive this maturational process are not known. To address this, we used mouse whole-genome microarrays and whole-cell patch clamp to characterize the transcriptional and electrophysiological maturation of cortical FS interneurons between postnatal day 7 (P7) and P40. We found that the intrinsic and synaptic physiology of FS cells undergoes profound regulation over the first 4 postnatal weeks and that these changes are correlated with primarily monotonic but bidirectional transcriptional regulation of thousands of genes belonging to multiple functional classes. Using our microarray screen as a guide, we discovered that upregulation of two-pore K+leak channels between P10 and P25 contributes to one of the major differences between the intrinsic membrane properties of immature and adult FS cells and found a number of other candidate genes that likely confer cell-type specificity on mature FS cells.

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  • Adamts8 and Adamts15 were also identified previously in FS-PV interneurons by Nelson et al.

    “Adamts8 and Adamts15 were also identified previously in FS-PV interneurons by Nelson et al.20”

    From Cortical fast-spiking parvalbumin interneurons enwrapped in the perineuronal net express the metallopeptidases Adamts8, Adamts15 and Neprilysin (2015) · cites this paper as [20]

  • The molecular identities of Na+ channels in interneurons suggest that at least in PVBCs the vast majority of Na+ channels are formed by Nav1.1 and Nav1.6 subunits with a lesser contribution from Nav1.2, Nav1.4, and Nav1.7.

    “The molecular identities of Na+ channels in interneurons suggest that at least in PVBCs the vast majority of Na+ channels are formed by Nav1.1 and Nav1.6 subunits with a lesser contribution from Nav1.2, Nav1.4, and Nav1.7 (502, 695, 857, 852).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [857]

  • Cav3.1 expression in G42-positive cortical fast spiking basket cells is downregulated during the first few weeks of postnatal life, likely contributing to a decrease in cell excitability upon maturation.

    “In contrast, Cav3.1 expression in G42-positive cortical fast spiking basket cells is downregulated during the first few weeks of postnatal life, likely contributing to a decrease in cell excitability upon maturation (857).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [857]

  • Tetrodotoxin-insensitive depolarizations and action potentials are common in young (PN5-7) PV-containing cells but largely absent by PN25, consistent with loss of functional T-type channels.

    “Although tetrodotoxin-insensitive depolarizations and action potentials are common in young (PN5–7) PV-containing cells, they are largely absent by PN25 consistent with the loss of functional T-type channels in these cells (857).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [857]

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Authors
Okaty, B. W., Miller, M. N., Sugino, K., Hempel, C. M., & Nelson, S. B.
Affiliations
  • Brandeis University (US)
  • University of California, San Francisco (US)
ORCID
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2009-05-27
Volume
29
Issue
21
Pages
7040-7052
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.0105-09.2009
PMC
PMC2749660
OpenAlex
W2070264536
Cited by
309
References
80
Citations by year
2026: 13 · 2025: 13 · 2024: 17 · 2023: 9 · 2022: 10 · 2021: 24 · 2020: 23 · 2019: 18 · 2018: 17 · 2017: 22 · 2016: 17 · 2015: 25 · 2014: 32 · 2013: 18 · 2012: 14
FWCI
6.91
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Simons Foundation
  • National Institute of Mental Health (R01MH066338)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
fast-spiking interneurons, GABAergic interneurons, neocortex, postnatal development, neuronal maturation, transcriptional regulation, electrophysiological maturation, intrinsic membrane properties, synaptic inhibition, cell specification, gene expression profiling
MeSH terms
Action Potentials, Age Factors, Analysis of Variance, Animals, Animals, Newborn, Biophysics, Electric Stimulation, Flow Cytometry, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Interneurons, Ion Channels, Lysine, Mice, Transgenic, Patch-Clamp Techniques, Gene Expression Regulation, Developmental, Excitatory Amino Acid Antagonists, Neocortex, Microarray Analysis, Green Fluorescent Proteins, Mice, Gene Regulatory Networks, Inhibitory Postsynaptic Potentials

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