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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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