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Cell-type specific parallel circuits in the bed nucleus of the stria terminalis and the central nucleus of the amygdala of the mouse

  • Jiahao YeEmail author
  • Pierre VeinanteEmail author
Original Article
  • 132 Downloads

Abstract

The central extended amygdala (EAc) is a forebrain macrosystem which has been widely implicated in reward, fear, anxiety, and pain. Its two key structures, the lateral bed nucleus of the stria terminalis (BSTL) and the central nucleus of the amygdala (CeA), share similar mesoscale connectivity. However, it is not known whether they also share similar cell-specific neuronal circuits. We addressed this question using tract-tracing and immunofluorescence to reveal the EAc microcircuits involving two neuronal populations expressing either protein kinase C delta (PKCδ) or somatostatin (SOM). PKCδ and SOM are expressed predominantly in the dorsal BSTL (BSTLD) and in the lateral/capsular parts of CeA (CeL/C). We found that, in both BSTLD and CeL/C, PKCδ+ cells are the main recipient of extra-EAc inputs from the lateral parabrachial nucleus (LPB), while SOM+ cells constitute the main source of long-range projections to extra-EAc targets, including LPB and periaqueductal gray. PKCδ+ cells can also integrate inputs from the basolateral nucleus of the amygdala or insular cortex. Within EAc, PKCδ+, but not SOM+ neurons, serve as the major source of inputs to the ventral BSTL and to the medial part of CeA. However, both cell types can be involved in mutual connections between BSTLD and CeL/C. These results unveil the pivotal positions of PKCδ+ and SOM+ neurons in organizing parallel cell-specific neuronal circuits within CeA and BSTL, but also between them, which further reinforce the notion of EAc as a structural and functional macrosystem.

Keywords

Central extended amygdala Protein kinase C delta type Somatostatin Neuronal tracing Microcircuit 

Abbreviations

ac

Anterior commissure

ASt

Amygdalostriatal transition area

BDA

Biotin dextran amine, 10000 MW

BL

Basolateral nucleus of the amygdala

BLA

Basolateral nucleus of the amygdala, anterior

BLP

Basolateral nucleus of the amygdala, posterior

BMP

Basomedial nucleus of the amygdala, posterior

CARD

Combined catalyzed reporter deposition

CeA

Central nucleus of the amygdala

CeC

Central nucleus of the amygdala, capsular part

CeL

Central nucleus of the amygdala, lateral part

CeL/C

Central nucleus of the amygdala, lateral and capsular part

CeM

Central nucleus of the amygdala, medial part

CGRP

Calcitonin gene-related peptide

CGRPR

Calcitonin gene-related peptide receptor

CPu

Caudate putamen

CRF

Corticotropin-releasing factor

cst

Commissural stria terminalis

CTb

Cholera toxin B subunit

D2R

Dopamine receptor D2

DAPI

4′,6-Diamidino-2-Phenylindole, Dihydrochloride

DMPAG

Dorsomedial periaqueductal gray

DR

Dorsal raphe nucleus

EAc

Central extended amygdala

ENK

Enkephalin

FG

Fluorogold

Fu

Fusiform nucleus

GI/DI

Granular and dysgranular insular cortex

GP

Globus pallidus

Htr2a

Serotonin receptor 2a

i.p.

Intraperitoneal injection

InsCx

Insular cortex

KLH

Keyhole limpet hemocyanin

LaVM

Lateral nucleus of the amygdala, ventromedial

LPAG

Lateral periaqueductal gray

LPB

Lateral parabrachial nucleus

LPBE

External lateral parabrachial nucleus

MPB

Medial parabrachial nucleus

NPY

Neuropeptide Y

PAG

Periaqueductal gray

PB

Phosphate buffer

PBS

Phosphate-buffered saline

PHA-L

Phaseolus vulgaris leucoagglutinin

Pir

Piriform cortex

PKCδ

Protein kinase C, delta type

Ppp1r1b

Phosphatase 1 regulatory subunit 1B

Rspo2

R-spondin 2

s.c.

Subcutaneous injection

S2

Secondary somatosensory cortex

scp

Superior cerebellar peduncle

SEM

Standard error of the mean

SOM

Somatostatin

BST

Bed nucleus of the stria terminalis

BSTL

Lateral bed nucleus of the stria terminalis

BSTLD

Dorsal lateral bed nucleus of the stria terminalis

BSTLP

Posterior lateral bed nucleus of the stria terminalis

BSTLV

Ventral lateral bed nucleus of the stria terminalis

BSTMA

Anterior medial bed nucleus of the stria terminalis

BSTMV

Ventral medial bed nucleus of the stria terminalis

VLPAG

Ventral lateral periaqueductal gray

Notes

Acknowledgements

This work was supported by the Centre National de la Recherche Scientifique (contract UPR3212), the University of Strasbourg, and the NeuroTime Erasmus Mundus Joint Doctorate Program. We thank the Chronobiotron UMS3415 for animal housing and care, and the platform “in vivo imaging” at UPS3156. We thank Dr. Paul Klosen for the helpful advices in CARD method and Dr. Alessandro Bilella for the help in using NanoZoomer S60 platform.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Informed consent

No human subject was used in this study.

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Centre National de la Recherche Scientifique UPR3212, Institut des Neurosciences Cellulaires et IntégrativesUniversité de StrasbourgStrasbourgFrance

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