Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons

Goichi Miyoshi, Jens Hjerling-Leffler, Theofanis Karayannis, Vitor H. Sousa, Simon J B Butt, James Battiste, Jane E. Johnson, Robert P. Machold, Gord Fishell

Research output: Contribution to journalArticle

314 Citations (Scopus)

Abstract

By combining an inducible genetic fate mapping strategy with electrophysiological analysis, we have systematically characterized the populations of cortical GABAergic interneurons that originate from the caudal ganglionic eminence (CGE). Interestingly, compared with medial ganglionic eminence (MGE)-derived cortical interneuron populations, the initiation [embryonic day 12.5 (E12.5)] and peak production (E16.5) of interneurons from this embryonic structure occurs 3 d later in development. Moreover, unlike either pyramidal cells or MGE-derived cortical interneurons, CGE-derived interneurons do not integrate into the cortex in an inside-out manner but preferentially (75%) occupy superficial cortical layers independent of birthdate. In contrast to previous estimates, CGE-derived interneurons are both considerably greater in number (∼30% of all cortical interneurons) and diversity (comprised by at least nine distinct subtypes). Furthermore,wefound that a large proportion of CGE-derived interneurons, including the neurogliaform subtype, express the glycoprotein Reelin. In fact, most CGE-derived cortical interneurons express either Reelin or vasoactive intestinal polypeptide. Thus, in conjunction with previous studies, we have now determined the spatial and temporal origins of the vast majority of cortical interneuron subtypes.

Original languageEnglish (US)
Pages (from-to)1582-1594
Number of pages13
JournalJournal of Neuroscience
Volume30
Issue number5
DOIs
StatePublished - Feb 3 2010

Fingerprint

Interneurons
Population
Median Eminence
Pyramidal Cells
Vasoactive Intestinal Peptide
Glycoproteins
Embryonic Structures

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J. B., Battiste, J., ... Fishell, G. (2010). Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. Journal of Neuroscience, 30(5), 1582-1594. https://doi.org/10.1523/JNEUROSCI.4515-09.2010

Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. / Miyoshi, Goichi; Hjerling-Leffler, Jens; Karayannis, Theofanis; Sousa, Vitor H.; Butt, Simon J B; Battiste, James; Johnson, Jane E.; Machold, Robert P.; Fishell, Gord.

In: Journal of Neuroscience, Vol. 30, No. 5, 03.02.2010, p. 1582-1594.

Research output: Contribution to journalArticle

Miyoshi, G, Hjerling-Leffler, J, Karayannis, T, Sousa, VH, Butt, SJB, Battiste, J, Johnson, JE, Machold, RP & Fishell, G 2010, 'Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons', Journal of Neuroscience, vol. 30, no. 5, pp. 1582-1594. https://doi.org/10.1523/JNEUROSCI.4515-09.2010
Miyoshi, Goichi ; Hjerling-Leffler, Jens ; Karayannis, Theofanis ; Sousa, Vitor H. ; Butt, Simon J B ; Battiste, James ; Johnson, Jane E. ; Machold, Robert P. ; Fishell, Gord. / Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. In: Journal of Neuroscience. 2010 ; Vol. 30, No. 5. pp. 1582-1594.
@article{aab09644d45b43e694cc86c4196c5ee6,
title = "Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons",
abstract = "By combining an inducible genetic fate mapping strategy with electrophysiological analysis, we have systematically characterized the populations of cortical GABAergic interneurons that originate from the caudal ganglionic eminence (CGE). Interestingly, compared with medial ganglionic eminence (MGE)-derived cortical interneuron populations, the initiation [embryonic day 12.5 (E12.5)] and peak production (E16.5) of interneurons from this embryonic structure occurs 3 d later in development. Moreover, unlike either pyramidal cells or MGE-derived cortical interneurons, CGE-derived interneurons do not integrate into the cortex in an inside-out manner but preferentially (75{\%}) occupy superficial cortical layers independent of birthdate. In contrast to previous estimates, CGE-derived interneurons are both considerably greater in number (∼30{\%} of all cortical interneurons) and diversity (comprised by at least nine distinct subtypes). Furthermore,wefound that a large proportion of CGE-derived interneurons, including the neurogliaform subtype, express the glycoprotein Reelin. In fact, most CGE-derived cortical interneurons express either Reelin or vasoactive intestinal polypeptide. Thus, in conjunction with previous studies, we have now determined the spatial and temporal origins of the vast majority of cortical interneuron subtypes.",
author = "Goichi Miyoshi and Jens Hjerling-Leffler and Theofanis Karayannis and Sousa, {Vitor H.} and Butt, {Simon J B} and James Battiste and Johnson, {Jane E.} and Machold, {Robert P.} and Gord Fishell",
year = "2010",
month = "2",
day = "3",
doi = "10.1523/JNEUROSCI.4515-09.2010",
language = "English (US)",
volume = "30",
pages = "1582--1594",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "5",

}

TY - JOUR

T1 - Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons

AU - Miyoshi, Goichi

AU - Hjerling-Leffler, Jens

AU - Karayannis, Theofanis

AU - Sousa, Vitor H.

AU - Butt, Simon J B

AU - Battiste, James

AU - Johnson, Jane E.

AU - Machold, Robert P.

AU - Fishell, Gord

PY - 2010/2/3

Y1 - 2010/2/3

N2 - By combining an inducible genetic fate mapping strategy with electrophysiological analysis, we have systematically characterized the populations of cortical GABAergic interneurons that originate from the caudal ganglionic eminence (CGE). Interestingly, compared with medial ganglionic eminence (MGE)-derived cortical interneuron populations, the initiation [embryonic day 12.5 (E12.5)] and peak production (E16.5) of interneurons from this embryonic structure occurs 3 d later in development. Moreover, unlike either pyramidal cells or MGE-derived cortical interneurons, CGE-derived interneurons do not integrate into the cortex in an inside-out manner but preferentially (75%) occupy superficial cortical layers independent of birthdate. In contrast to previous estimates, CGE-derived interneurons are both considerably greater in number (∼30% of all cortical interneurons) and diversity (comprised by at least nine distinct subtypes). Furthermore,wefound that a large proportion of CGE-derived interneurons, including the neurogliaform subtype, express the glycoprotein Reelin. In fact, most CGE-derived cortical interneurons express either Reelin or vasoactive intestinal polypeptide. Thus, in conjunction with previous studies, we have now determined the spatial and temporal origins of the vast majority of cortical interneuron subtypes.

AB - By combining an inducible genetic fate mapping strategy with electrophysiological analysis, we have systematically characterized the populations of cortical GABAergic interneurons that originate from the caudal ganglionic eminence (CGE). Interestingly, compared with medial ganglionic eminence (MGE)-derived cortical interneuron populations, the initiation [embryonic day 12.5 (E12.5)] and peak production (E16.5) of interneurons from this embryonic structure occurs 3 d later in development. Moreover, unlike either pyramidal cells or MGE-derived cortical interneurons, CGE-derived interneurons do not integrate into the cortex in an inside-out manner but preferentially (75%) occupy superficial cortical layers independent of birthdate. In contrast to previous estimates, CGE-derived interneurons are both considerably greater in number (∼30% of all cortical interneurons) and diversity (comprised by at least nine distinct subtypes). Furthermore,wefound that a large proportion of CGE-derived interneurons, including the neurogliaform subtype, express the glycoprotein Reelin. In fact, most CGE-derived cortical interneurons express either Reelin or vasoactive intestinal polypeptide. Thus, in conjunction with previous studies, we have now determined the spatial and temporal origins of the vast majority of cortical interneuron subtypes.

UR - http://www.scopus.com/inward/record.url?scp=76149146046&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=76149146046&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.4515-09.2010

DO - 10.1523/JNEUROSCI.4515-09.2010

M3 - Article

C2 - 20130169

AN - SCOPUS:76149146046

VL - 30

SP - 1582

EP - 1594

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 5

ER -