Common origins of hippocampal ivy and nitric oxide synthase expressing neurogliaform cells

Ludovic Tricoire, Kenneth A. Pelkey, Michael I. Daw, Vitor H. Sousa, Goichi Miyoshi, Brian Jeffries, Bruno Cauli, Gordon Fishell, Chris J. McBain

Research output: Contribution to journalArticle

Abstract

GABAergic interneurons critically regulate cortical computation through exquisite spatiotemporal control over excitatory networks. Precision of this inhibitory control requires a remarkable diversity within interneuron populations that is largely specified during embryogenesis. Although interneurons expressing the neuronal isoform of nitric oxide synthase (nNOS) constitute the largest hippocampal interneuron cohort their origin and specification remain unknown. Thus, as neurogliaform cells (NGC) and Ivy cells (IvC) represent the main nNOS+ interneurons, we investigated their developmental origins. Although considered distinct interneuron subtypes, NGCs and IvCs exhibited similar neurochemical and electrophysiological signatures, including NPY expression and late spiking. Moreover, lineage analyses, including loss-of-function experiments and inducible fate-mapping, indicated that nNOS+ IvCs and NGCs are both derived from medial ganglionic eminence (MGE) progenitors under control of the transcription factor Nkx2-1. Surprisingly, a subset of NGCs lacking nNOS arises from caudal ganglionic eminence (CGE) progenitors. Thus, while nNOS+ NGCs and IvCs arise from MGE progenitors, a CGE origin distinguishes a discrete population of nNOS- NGCs.

Original languageEnglish (US)
Pages (from-to)2165-2176
Number of pages12
JournalJournal of Neuroscience
Volume30
Issue number6
DOIs
StatePublished - Feb 10 2010

Fingerprint

Nitric Oxide Synthase Type I
Interneurons
Nitric Oxide Synthase
Protein Isoforms
Median Eminence
Population
Embryonic Development
Transcription Factors

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Tricoire, L., Pelkey, K. A., Daw, M. I., Sousa, V. H., Miyoshi, G., Jeffries, B., ... McBain, C. J. (2010). Common origins of hippocampal ivy and nitric oxide synthase expressing neurogliaform cells. Journal of Neuroscience, 30(6), 2165-2176. https://doi.org/10.1523/JNEUROSCI.5123-09.2010

Common origins of hippocampal ivy and nitric oxide synthase expressing neurogliaform cells. / Tricoire, Ludovic; Pelkey, Kenneth A.; Daw, Michael I.; Sousa, Vitor H.; Miyoshi, Goichi; Jeffries, Brian; Cauli, Bruno; Fishell, Gordon; McBain, Chris J.

In: Journal of Neuroscience, Vol. 30, No. 6, 10.02.2010, p. 2165-2176.

Research output: Contribution to journalArticle

Tricoire, L, Pelkey, KA, Daw, MI, Sousa, VH, Miyoshi, G, Jeffries, B, Cauli, B, Fishell, G & McBain, CJ 2010, 'Common origins of hippocampal ivy and nitric oxide synthase expressing neurogliaform cells', Journal of Neuroscience, vol. 30, no. 6, pp. 2165-2176. https://doi.org/10.1523/JNEUROSCI.5123-09.2010
Tricoire, Ludovic ; Pelkey, Kenneth A. ; Daw, Michael I. ; Sousa, Vitor H. ; Miyoshi, Goichi ; Jeffries, Brian ; Cauli, Bruno ; Fishell, Gordon ; McBain, Chris J. / Common origins of hippocampal ivy and nitric oxide synthase expressing neurogliaform cells. In: Journal of Neuroscience. 2010 ; Vol. 30, No. 6. pp. 2165-2176.
@article{7f638256b101436cb193307616dba3e1,
title = "Common origins of hippocampal ivy and nitric oxide synthase expressing neurogliaform cells",
abstract = "GABAergic interneurons critically regulate cortical computation through exquisite spatiotemporal control over excitatory networks. Precision of this inhibitory control requires a remarkable diversity within interneuron populations that is largely specified during embryogenesis. Although interneurons expressing the neuronal isoform of nitric oxide synthase (nNOS) constitute the largest hippocampal interneuron cohort their origin and specification remain unknown. Thus, as neurogliaform cells (NGC) and Ivy cells (IvC) represent the main nNOS+ interneurons, we investigated their developmental origins. Although considered distinct interneuron subtypes, NGCs and IvCs exhibited similar neurochemical and electrophysiological signatures, including NPY expression and late spiking. Moreover, lineage analyses, including loss-of-function experiments and inducible fate-mapping, indicated that nNOS+ IvCs and NGCs are both derived from medial ganglionic eminence (MGE) progenitors under control of the transcription factor Nkx2-1. Surprisingly, a subset of NGCs lacking nNOS arises from caudal ganglionic eminence (CGE) progenitors. Thus, while nNOS+ NGCs and IvCs arise from MGE progenitors, a CGE origin distinguishes a discrete population of nNOS- NGCs.",
author = "Ludovic Tricoire and Pelkey, {Kenneth A.} and Daw, {Michael I.} and Sousa, {Vitor H.} and Goichi Miyoshi and Brian Jeffries and Bruno Cauli and Gordon Fishell and McBain, {Chris J.}",
year = "2010",
month = "2",
day = "10",
doi = "10.1523/JNEUROSCI.5123-09.2010",
language = "English (US)",
volume = "30",
pages = "2165--2176",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "6",

}

TY - JOUR

T1 - Common origins of hippocampal ivy and nitric oxide synthase expressing neurogliaform cells

AU - Tricoire, Ludovic

AU - Pelkey, Kenneth A.

AU - Daw, Michael I.

AU - Sousa, Vitor H.

AU - Miyoshi, Goichi

AU - Jeffries, Brian

AU - Cauli, Bruno

AU - Fishell, Gordon

AU - McBain, Chris J.

PY - 2010/2/10

Y1 - 2010/2/10

N2 - GABAergic interneurons critically regulate cortical computation through exquisite spatiotemporal control over excitatory networks. Precision of this inhibitory control requires a remarkable diversity within interneuron populations that is largely specified during embryogenesis. Although interneurons expressing the neuronal isoform of nitric oxide synthase (nNOS) constitute the largest hippocampal interneuron cohort their origin and specification remain unknown. Thus, as neurogliaform cells (NGC) and Ivy cells (IvC) represent the main nNOS+ interneurons, we investigated their developmental origins. Although considered distinct interneuron subtypes, NGCs and IvCs exhibited similar neurochemical and electrophysiological signatures, including NPY expression and late spiking. Moreover, lineage analyses, including loss-of-function experiments and inducible fate-mapping, indicated that nNOS+ IvCs and NGCs are both derived from medial ganglionic eminence (MGE) progenitors under control of the transcription factor Nkx2-1. Surprisingly, a subset of NGCs lacking nNOS arises from caudal ganglionic eminence (CGE) progenitors. Thus, while nNOS+ NGCs and IvCs arise from MGE progenitors, a CGE origin distinguishes a discrete population of nNOS- NGCs.

AB - GABAergic interneurons critically regulate cortical computation through exquisite spatiotemporal control over excitatory networks. Precision of this inhibitory control requires a remarkable diversity within interneuron populations that is largely specified during embryogenesis. Although interneurons expressing the neuronal isoform of nitric oxide synthase (nNOS) constitute the largest hippocampal interneuron cohort their origin and specification remain unknown. Thus, as neurogliaform cells (NGC) and Ivy cells (IvC) represent the main nNOS+ interneurons, we investigated their developmental origins. Although considered distinct interneuron subtypes, NGCs and IvCs exhibited similar neurochemical and electrophysiological signatures, including NPY expression and late spiking. Moreover, lineage analyses, including loss-of-function experiments and inducible fate-mapping, indicated that nNOS+ IvCs and NGCs are both derived from medial ganglionic eminence (MGE) progenitors under control of the transcription factor Nkx2-1. Surprisingly, a subset of NGCs lacking nNOS arises from caudal ganglionic eminence (CGE) progenitors. Thus, while nNOS+ NGCs and IvCs arise from MGE progenitors, a CGE origin distinguishes a discrete population of nNOS- NGCs.

UR - http://www.scopus.com/inward/record.url?scp=76649137940&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=76649137940&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.5123-09.2010

DO - 10.1523/JNEUROSCI.5123-09.2010

M3 - Article

C2 - 20147544

AN - SCOPUS:76649137940

VL - 30

SP - 2165

EP - 2176

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 6

ER -