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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

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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.

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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

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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.

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Correspondence to Jiahao Ye or Pierre Veinante.

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Ye, J., Veinante, P. Cell-type specific parallel circuits in the bed nucleus of the stria terminalis and the central nucleus of the amygdala of the mouse. Brain Struct Funct 224, 1067–1095 (2019). https://doi.org/10.1007/s00429-018-01825-1

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  • DOI: https://doi.org/10.1007/s00429-018-01825-1

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