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Common and distinct neural inputs to the medial central nucleus of the amygdala and anterior ventrolateral bed nucleus of stria terminalis in rats

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Abstract

The central nucleus of the amygdala (CEA) and lateral bed nucleus of stria terminalis (BST) are highly interconnected limbic forebrain regions that share similar connectivity with other brain regions that coordinate behavioral and physiological responses to internal and environmental stressors. Their similar connectivity is frequently referred to when describing the CEA and lateral BST together as a unified “central extended amygdala”. However, the CEA and BST reportedly play distinct roles in behavioral and physiological responses associated with fear, anxiety, and social defeat, presumably due to differences in connectivity. To identify common and unique sources of input to the CEA and lateral BST, we performed dual retrograde tracing. Fluorogold and cholera toxin β were iontophoresed into the medial CEA (CEAm) and the anterior ventrolateral BST (BSTvl) of adult male rats. The anatomical distribution of tracer-labeled neurons was mapped throughout the brain. Regions with overlapping populations of CEAm- and BSTvl-projecting neurons were further examined for the presence of double-labeled neurons. Although most regions with input to the mCEA also projected to the BSTvl, and vice versa, cortical and sensory system-related regions projected more robustly to the CEAm, while motor system-related regions primarily innervated the BSTvl. The incidence of double-labeled neurons with collateralized axonal inputs to the CEAm and BSTvl was relatively small (~2 to 13%) and varied across regions, suggesting regional differences in the degree of coordinated CEAm and BSTvl input. The demonstrated similarities and differences in inputs to CEAm and BSTvl provide new anatomical insights into the functional organization of these limbic forebrain regions.

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Abbreviations

ACBsh:

Nucleus accumbens, shell division

aco:

Anterior commissure

AI:

Agranular insular cortex

amc:

Amygdalar capsule

AP:

Area postrema

AStr:

Amygdala-striatal transition area

Aud:

Auditory thalamus

BLAp:

Basolateral amygdalar nucleus, posterior part

BMA:

Basomedial amygdalar nucleus

BST:

Bed nucleus of stria terminalis

pBST:

Posterior subnuclei group of the bed nucleus of stria terminalis

BSTvl:

Ventrolateral subnuclei group of the bed nucleus of stria terminalis

CA1:

Field CA1, Ammon’s horn

cc:

Corpus callosum

CEA:

Central amygdalar nucleus

CEAm:

Central amygdalar nucleus, medial part

CEAl:

Central amygdalar nucleus, lateral part

CLI:

Central linear nucleus raphé

cpd:

Cerebral peduncle

DI:

Dysgranular insular cortex

DMX:

Dorsal motor nucleus of the vagus

DR:

Dorsal nucleus raphé

dscp:

Superior cerebellar peduncle decussation

ec:

External capsule

fx:

Fornix

ILA:

Infralimbic area

IMD:

Intermediodorsal nucleus thalamus

IPAC:

Interstitial nucleus of the posterior limb of the anterior commissure

LHA:

Lateral hypothalamic area

LS:

Lateral septal nucleus

mcp:

Middle cerebellar peduncle

MD:

Mediodorsal nucleus thalamus

ml:

Medial lemniscus

mlf:

Medial longitudinal fascicle

mPFC:

Medial prefrontal cortex

MPO:

Medial preoptic area

MTN:

Midline thalamic nuclei

NLOT:

Nucleus of the lateral olfactory tract

NTS:

Nucleus of the solitary tract

och:

Optic chiasm

opt:

Optic tract

PA:

Posterior amygdalar nucleus

PAGvl:

Periaqueductal gray, ventrolateral division

PB:

Parabrachial nucleus

PBle:

Parabrachial nucleus, external lateral part

PBlv:

Parabrachial nucleus, ventral lateral part

PBm:

Parabrachial nucleus, medial part

PBw:

Parabrachial nucleus, waist part

PL:

Prelimbic area

PPN:

Pedunculopontine nucleus

PSTN:

Parasubthalamic nucleus

PVN:

Paraventricular hypothalamic nucleus

PVT:

Paraventricular thalamic nucleus

py:

Pyramid

scp:

Superior cerebellar peduncle

SI:

Substantia innominata

sm:

Stria medullaris

SNc:

Substantia nigra, compact part

SNr:

Substantia nigra, reticular part

SPFpm:

Subparafascicular nucleus thalamus, parvicellular part, medial division

st:

Stria terminalis

STN:

Subthalamic nucleus

TR:

Postpiriform transition area

V4:

Fourth ventricle

VLM:

Ventrolateral medulla

VP:

Ventral pallidum

VPMpc:

Ventral posteromedial nucleus thalamus, parvicellular part

VTA:

Ventral tegmental area

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Acknowledgments

We thank Vicki Maldovan and Li Cai for their expert technical assistance in this study. This research was supported by grants from the National Institutes of Health (MH59911 and DK063922). Research supported by NIH grant MH59911 to L.R. and NIH grant DK063922 to M.B.

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  1. Department of Neuroscience, University of Pittsburgh, A210 Langley Hall, Pittsburgh, PA, 15260, USA

    Michael S. Bienkowski & Linda Rinaman

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  1. Michael S. Bienkowski
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Correspondence to Linda Rinaman.

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Bienkowski, M.S., Rinaman, L. Common and distinct neural inputs to the medial central nucleus of the amygdala and anterior ventrolateral bed nucleus of stria terminalis in rats. Brain Struct Funct 218, 187–208 (2013). https://doi.org/10.1007/s00429-012-0393-6

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