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Brain Structure and Function

, Volume 223, Issue 7, pp 3279–3295 | Cite as

The caudo-ventral pallium is a novel pallial domain expressing Gdf10 and generating Ebf3-positive neurons of the medial amygdala

  • Nuria Ruiz-Reig
  • Belen Andres
  • Thomas Lamonerie
  • Thomas Theil
  • Alfonso Fairén
  • Michèle Studer
Original Article
  • 140 Downloads

Abstract

In rodents, the medial nucleus of the amygdala receives direct inputs from the accessory olfactory bulbs and is mainly implicated in pheromone-mediated reproductive and defensive behaviors. The principal neurons of the medial amygdala are GABAergic neurons generated principally in the caudo-ventral medial ganglionic eminence and preoptic area. Beside GABAergic neurons, the medial amygdala also contains glutamatergic Otp-expressing neurons cells generated in the lateral hypothalamic neuroepithelium and a non-well characterized Pax6-positive population. In the present work, we describe a novel glutamatergic Ebf3-expressing neuronal subpopulation distributed within the periphery of the postero-ventral medial amygdala. These neurons are generated in a pallial domain characterized by high expression of Gdf10. This territory is topologically the most caudal tier of the ventral pallium and accordingly, we named it Caudo-Ventral Pallium (CVP). In the absence of Pax6, the CVP is disrupted and Ebf3-expressing neurons fail to be generated. Overall, this work proposes a novel model of the neuronal composition of the medial amygdala and unravels for the first time a new novel pallial subpopulation originating from the CVP and expressing the transcription factor Ebf3.

Keywords

Telencephalon Ventral pallium Medial amygdala Gdf10 Ebf3 Pax6 Caudo-ventral pallium 

Abbreviations

BLA

Basolateral complex of the amygdala

BMA

Basomedial nucleus of the amygdala

C

Caudal

CBP

Cranial bone progenitors

CGE

Caudal ganglionic eminence

CRC

Cajal–Retzius cells

cvMGE

Caudo-ventral MGE

CVP

Caudo-ventral pallium

Cx

Cortex

D

Dorsal

Dg

Diagonal area

dLGE

Dorsal LGE

DLP

Dorsolateral pallium

DP

Dorsal pallium

GE

Ganglionic eminences

HC

Hippocampus

ISH

In situ hybridization

L

Lateral

LGE

Lateral ganglionic eminence.

LP

Lateral pallium

LTE

Lateral thalamic eminence.

M

Medial

MeA

Medial amygdala

MeAa

Antero-medial Amygdala

MePD

Posterodorsal medial Amygdala

MePV

Posteroventral medial amygdala

MGE

Medial ganglionic eminence

MP

Medial pallium

MTE

Medial thalamic eminence

MZ

Mantle zone

OB

Olfactory bulb

PAS

Preoptic amygdala stream

POA

Preoptic area

PSB

Pallial-subpallial boundary

PVH

Paraventricular hypothalamic domain

pTh

Prethalamus

R

Rostral

SlMe

Superficial layer of the medial nucleus

SVZ

Subventricular zone

TE

Thalamic eminence

TF

Transcription factor

Th

Thalamus

V

Ventral

VAPv

Ventropallial amygdalopiriform area

VLP

Ventrolateral caudal pallium

VP

Ventral pallium

VZ

Ventricular zone

ZLI

Zona limitants intrathalamica

Notes

Acknowledgements

We thank Dr. F. Vaccarino and L. Tomasini for Otp antibody, and Dr. A. Mansouri for the Pax6KO colony. Special thanks to Dr. M. Bertacchi for sharing the Pax6KO colony.

Funding

This work was supported by Grants of the French National Research Agency (Agence Nationale de la Recherche; ANR) [ANR-13-BSV4-0011] and by the French Government through the ‘Investments for the Future’ LABEX SIGNALIFE [ANR-11-LABX-0028-01] to M.S., by the Spanish Government (BFU2007-60263 and BFU2010-17305) to A.F, and by the Medical Research Council (MR/K013750/1) to T.T. N.R.-R. is funded by a postdoctoral fellowship from the Ville de Nice, France (“Aide Individuelle aux Jeunes Chercheurs 2016”).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. The care and handling of mice prior or during the experimental procedures followed European Union rules (2010/63/UE) and were approved by the Animal Care and Use Committees of Spain and France.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

429_2018_1687_MOESM1_ESM.tif (5.6 mb)
Figure S1. The telencephalic Gdf10+ territory does not belong to the ganglionic eminences. (a–cʹ) In situ hybridization for Ascl1, Gsx2 and Gdf10 in coronal sections taken at two different rostro-caudal levels of E12.5 wild type brains. The telencephalic Gdf10+ territory is negative for Ascl1 and Gsx2, two markers expressed in the ganglionic eminences Scale bar: 100 µm (TIFF 5720 KB)
429_2018_1687_MOESM2_ESM.tif (5.5 mb)
Figure S2. Emx1 is not expressed in the VZ of the telencephalic Gdf10+ territory. (a, b) In situ hybridization for Gdf10 and Emx1 in consecutive coronal sections of the same E12.5 wild type brain. (aʹ, bʹ) High magnification views of the boxes in a and  b showing that at this stage the Gdf10+ territory in the VZ is negative for Emx1, which is restricted to the SVZ. Scale bar: 100 µm (TIFF 5587 KB)
429_2018_1687_MOESM3_ESM.tif (12.2 mb)
Figure S3. Additional markers located in the CVP. (a–aʹ, b–bʹ) In situ hybridization for Ptch1 and Mdga1 in coronal sections at two different caudo-rostral levels of E12.5 wild type brains. Ptch1 is expressed in the VZ, while Mdga1 expression is restricted to the SVZ of the telencephalic Gdf10+ territory (or CVP as indicated by black arrowheads). Green arrowheads point to the VP. (c, d) Triple immunofluorescence for two pallial markers, Tbr2 and Pax6, and COUP-TFII in coronal sections (c) and horizontal sections (d) of E12.5 wild type brains. (cʹ–dʹ) High magnification views of the boxes in c and d showing co-expression of Pax6 and COUP-TFII in the VZ, and Tbr2 and COUP-TFII in the SVZ of the CVP. Scale bars: (a–d) 100 µm; (cʹ–dʹ) 50 µm (TIFF 12479 KB)
429_2018_1687_MOESM4_ESM.tif (8.2 mb)
Figure S4. Ebf3-, nNOS- and Tbr2-expressing cells form three independent neuronal populations in the MePV nucleus. (a) Double immunofluorescence for GABA and Ebf3 in a coronal section of P0 wild type brains. (aʹ, a″) High magnification views of the shell of the MePV showing lack of Ebf3+ (red) cells co-localization with GABA+ (green) neurons (white arrowheads). (b) Triple immunofluorescence for Tbr2, Ebf3 and nNOS in a coronal section of E15.5 wild type brains. (bʹ, b″) High magnification views of the core of the MePV showing no co-localization between Tbr2+ (green) and nNOS+ (blue) cells, which are located as a separate population with respect to Ebf3+ cells (red). Scale bars: (a, b) 100 µm; (aʹ–b″) 50 µm (TIFF 8369 KB)
429_2018_1687_MOESM5_ESM.tif (5.2 mb)
Figure S5. The MePV contains Pax6+Tbr2+ cells in addition to Shh+ and nNOS+ neuronal subpopulations. (a) Triple immunofluorescence for Tbr2, Pax6 and Ki67 in a coronal section of E12.5 wild type brain. (a1ʹ, a1″) High magnification views of the square in a showing in yellow cells positive c-l for Pax6 and Tbr2 but negative for Ki67 in the core of the MePV. Green Tbr2+ single cells are most probably intermediate progenitors. a1″ display cells positive for Pax6. (b) In situ hybridization of Shh in a coronal section of E12.5 wild type brains shows expression in the MePV region. (c) Immunofluorescence for nNOS in a coronal section of E15.5 wild type embryos indicates high expression in the MePV region. Scale bars: (a–c) 100 µm; (a1ʹ–a1″) 50 µm (TIFF 5372 KB)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Université Côte d’Azur (UCA), CNRS, Inserm, Institut de Biologie Valrose (iBV)NiceFrance
  2. 2.Instituto de Neurociencias (Consejo Superior de Investigaciones Científicas-Universidad Miguel Hernández, CSIC-UMH)San Juan de AlicanteSpain
  3. 3.Centre for Discovery Brain Sciences, Hugh Robson BuildingUniversity of EdinburghEdinburghUK
  4. 4.San Juan de AlicanteSpain

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