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Cited by 244Neurogenesis and neuroplasticity mechanismsNeuroscience and Neuropharmacology ResearchDevelopmental Biology and Gene Regulation

Excitatory projection neuron subtypes control the distribution of local inhibitory interneurons in the cerebral cortex

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Lodato, Simona, Rouaux, Caroline, Quast, Kathleen B., Jantrachotechatchawan, Chanati, Studer, Michèle, Hensch, Takao K., Arlotta, Paola·2011·Neuron
DOI 10.1016/j.neuron.2011.01.015PMC PMC3061282
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Abstract

In the mammalian cerebral cortex, the developmental events governing the integration of excitatory projection neurons and inhibitory interneurons into balanced local circuitry are poorly understood. We report that different subtypes of projection neurons uniquely and differentially determine the laminar distribution of cortical interneurons. We find that in Fezf2⁻/⁻ cortex, the exclusive absence of subcerebral projection neurons and their replacement by callosal projection neurons cause distinctly abnormal lamination of interneurons and altered GABAergic inhibition. In addition, experimental generation of either corticofugal neurons or callosal neurons below the cortex is sufficient to recruit cortical interneurons to these ectopic locations. Strikingly, the identity of the projection neurons generated, rather than strictly their birthdate, determines the specific types of interneurons recruited. These data demonstrate that in the neocortex individual populations of projection neurons cell-extrinsically control the laminar fate of interneurons and the assembly of local inhibitory circuitry.

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Crossref · 10.1016/j.neuron.2011.01.015

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  • Disrupting normal pyramidal cell layering changes the normal laminar distribution of interneurons.

    “Second, disruption of the normal layering of pyramidal cells modifies the normal laminar distribution of interneurons (Lodato et al., 2011; Pla et al., 2006).”

    From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Lodato et al., 2011

  • Interneurons adopt their laminar distribution in response to cues from pyramidal cells.

    “Several lines of evidence suggest that the interneurons adopt their laminar distribution in response to cues provided by pyramidal cells.”

    From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Lodato et al., 2011

  • Interneurons appear to interact with specific classes of pyramidal cells while acquiring their laminar position.

    “Importantly, interneurons seem to interact with specific classes of pyramidal cells when acquiring their laminar position (Lodato et al., 2011), which suggests that this interaction may actually predate the formation of specific connections between excitatory and inhibitory neurons in the developing cerebral cortex, at least for certain classes on interneurons (Ye et al., 2015).”

    From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Lodato et al., 2011

  • The excitatory identity controls the survival and wiring of local interneurons.

    “This observation is in line with previous findings that the excitatory identity controls the survival and wiring of local interneurons60,61.”

    From Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas (2019) · cites this paper as [60]

  • Overexpression of Fezf2 in utero produces ectopic subcerebral principal cells below the white matter that preferentially attract PV- and SST-expressing interneurons, but not subtypes primarily found in superficial layers.

    “overexpression of Fezf2 in utero produced ectopic subcerebral PCs below the white matter that preferentially attracted PV- and SST-expressing interneurons, but not subtypes primarily found in the superficial layers”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [687]

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Authors
Lodato, S., Rouaux, C., Quast, K. B., Jantrachotechatchawan, C., Studer, M., Hensch, T. K., & Arlotta, P.
Affiliations
  • Harvard University (US)
  • Inserm (FR)
Corresponding author
Arlotta, Paola
ORCID
Venue
Neuron
Publisher
Elsevier BV
Published
2011-02
Volume
69
Issue
4
Pages
763-779
ISSN
0896-6273 (ISSN-L)
DOI
10.1016/j.neuron.2011.01.015
PMC
PMC3061282
OpenAlex
W1982236792
Cited by
244
References
68
Citations by year
2026: 11 · 2025: 10 · 2024: 13 · 2023: 23 · 2022: 14 · 2021: 19 · 2020: 22 · 2019: 21 · 2018: 13 · 2017: 13 · 2016: 8 · 2015: 17 · 2014: 15 · 2013: 22 · 2012: 15
FWCI
6.20
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • Digital Access to Scholarship at Harvard (DASH) (Harvard University) (acceptedVersion)
Funders
  • Ellison Medical Foundation
  • National Institutes of Health (DP1OD003699)
  • Harvard Stem Cell Institute
  • National Institute of Neurological Disorders and Stroke (R01NS062849, NS062849)
Topics
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
cortical interneurons, laminar distribution, Fezf2, callosal projection neurons, corticofugal neurons, GABAergic inhibition, neocortex development, neuronal identity
MeSH terms
Age Factors, Animals, Animals, Newborn, Cell Count, Cell Movement, Cerebral Cortex, Corpus Callosum, DNA-Binding Proteins, Electric Stimulation, Embryo, Mammalian, Female, Glutamate Decarboxylase, Interneurons, Functional Laterality, Membrane Potentials, Mice, Transgenic, Nerve Net, Nerve Tissue Proteins, Neural Inhibition, Neural Pathways, Neurons, Pregnancy, Electroporation, Patch-Clamp Techniques, Gene Expression Regulation, Developmental, Green Fluorescent Proteins, Mice

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