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Extending the socio-sexual brain: arginine-vasopressin immunoreactive circuits in the telencephalon of mice

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Abstract

Quantitative analysis of the immunoreactivity for arginine-vasopressin (AVP-ir) in the telencephalon of male (intact and castrated) and female CD1 mice allows us to precisely locate two sexually dimorphic (more abundant in intact than castrated males and females) AVP-ir cell groups in the posterior bed nucleus of the stria terminalis (BST) and the amygdala. Chemoarchitecture (NADPH diaphorase) reveals that the intraamygdaloid AVP-ir cells are located in the intra-amygdaloid BST (BSTIA) rather than the medial amygdala (Me), as previously thought. Then, we have used for the first time tract tracing (combined with AVP immunofluorescence) and fiber-sparing lesions of the BST to analyze the projections of the telencephalic AVP-ir cell groups. The results demonstrate that the posterior BST originates the sexually dimorphic innervation of the lateral septum, the posterodorsal Me and a substance P-negative area in the medioventral striato-pallidum (mvStP).The BSTIA may also contribute to some of these terminal fields. Our material also reveals non-dimorphic AVP-ir processes in two locations of the amygdala. First, the ventral Me shows dendrite-like AVP-ir processes apparently belonging supraoptic neurons, whose possible functions are discussed. Second, the Ce shows sparse, thick AVP-ir axons with high individual variability in density and distribution, whose possible influence on stress coping in relation to the affiliative or agonistic behaviors mediated by the Me are discussed. Finally, we propose that the region of the mvStP showing sexually dimorphic AVP-ir innervation is part of the brain network for socio-sexual behavior, in which it would mediate motivational aspects of chemosensory-guided social interactions.

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Abbreviations

3V:

Third ventricle

AA:

Anterior amygdaloid area

AAD:

Anterior amygdaloid area, dorsal part

AAV:

Anterior amygdaloid area, ventral part

AC:

Anterior commissural nucleus

aca:

Anterior commissure, anterior part

Acb:

Accumbens nucleus

AcbC:

Accumbens nucleus, core

AcbSh:

Accumbens nucleus, shell

ACo:

Anterior cortical amygdaloid nucleus

acp:

Anterior commissure, posterior part

AD:

Anterodorsal thalamic nucleus

ADP:

Anterodorsal preoptic nucleus

AHA:

Anterior hypothalamic area, anterior part

AHiAL:

Amygdalohippocampal area, anterolateral part

AHiMP:

Amygdalohippocampal area, medial posterior part

AIP:

Agranular insular cortex, posterior part

AM:

Anteromedial thalamic nucleus

AOM:

Anterior olfactory nucleus, medial part

AOP:

Anterior olfactory nucleus, posterior part

APir:

Amygdalopiriform transition area

AStr:

Amygdalostriatal transition area

AV:

Anteroventral thalamic nucleus

AVP:

Arginine-vasopressin

AVPe:

Anteroventral periventricular nucleus

AVP-ir:

Arginine-vasopressin immunoreactive

AVV:

Anteroventral thalamic nucleus, ventral part

BAC:

Bed nucleus of the anterior commissure

BAOT:

Bed nucleus of the accessory olfactory tract

BLA:

Basolateral amygdaloid nucleus, anterior

BLP:

Basolateral amygdaloid nucleus, posterior

BLV:

Basolateral amygdaloid nucleus, ventral

BMA:

Basomedial amygdaloid nucleus, anterior

BMP:

Basomedial amygdaloid nucleus, posterior

BST:

Bed nucleus of the stria terminalis

BSTIA:

Bed nucleus of the stria terminalis, intraamygdaloid division

BSTLD:

Bed nucleus of the stria terminalis, lateral division, dorsal part

BSTLI:

Bed nucleus of the stria terminalis, lateral division, intermediate part

BSTLJ:

Bed nucleus of the stria terminalis, lateral division, juxtacapsular part

BSTLP:

Bed nucleus of the stria terminalis, lateral division, posterior part

BSTLV:

Bed nucleus of the stria terminalis, lateral division, ventral part

BSTMA:

Bed nucleus of the stria terminalis, medial division, anterior part

BSTMP:

Bed nucleus of the stria terminalis, medial division, posterior part

BSTMPI:

Bed nucleus of the stria terminalis, medial division, posterointermediate part

BSTMPL:

Bed nucleus of the stria terminalis, medial division, posterolateral part

BSTMPM:

Bed nucleus of the stria terminalis, medial division, posteromedial part

BSTMV:

Bed nucleus of the stria terminalis, medial division, ventral part

BSTS:

Bed nucleus of the stria terminalis, supracapsular part

CA1:

Field CA1 of hippocampus

CA2:

Field CA2 of hippocampus

CA3:

Field CA3 of hippocampus

cc:

Corpus callosum

Ce:

Central amygdaloid nucleus

CeC:

Central amygdaloid nucleus, capsular part

CeL:

Central amygdaloid nucleus, lateral division

CeM:

Central amygdaloid nucleus, medial division

CeMPV:

Central amygdaloid nucleus, medial division, posteroventral part

Cg1:

Cingulate cortex, area 1

Cg2:

Cingulate cortex, area 2

Cl:

Claustrum

CM:

Central medial thalamic nucleus

CPu:

Caudate putamen (striatum)

CxA:

Cortex-amygdala transition zone

D3V:

Dorsal third ventricle

DEn:

Dorsal endopiriform nucleus

DG:

Dentate gyrus

DP:

Dorsal peduncular cortex

DTT:

Dorsal tenia tecta

f:

Fornix

FG:

Fluorogold

fi:

Fimbria of the hippocampus

fmi:

Forceps minor of the corpus callosum

GrDG:

Granular layer of the dentate gyrus

HDB:

Nucleus of the horizontal limb of the diagonal band

I:

Intercalated nuclei of the amygdala

IAD:

Interanterodorsal thalamic nucleus

ic:

Internal capsule

ICj:

Islands of Calleja

ICjM:

Islands of Calleja, major island

IG:

Indusium griseum

IL:

Infralimbic cortex

IM:

Intercalated amygdaloid nucleus, main part

IPAC:

Interstitial nucleus of the posterior limb of the anterior commissure

IPACL:

Lateral interstitial nucleus of the posterior limb of the anterior commissure

IPACM:

Medial interstitial nucleus of the posterior limb of the anterior commissure

La:

Lateral amygdaloid nucleus

LA:

Lateroanterior hypothalamic nucleus

LaDL:

Lateral amygdaloid nucleus, dorsolateral part

LaVL:

Lateral amygdaloid nucleus, ventrolateral part

LaVM:

Lateral amygdaloid nucleus, ventromedial part

LEnt:

Lateral entorhinal cortex

LGP:

Lateral globus pallidus

LH:

Lateral hypothalamic area

lo:

Lateral olfactory tract

LOT:

Nucleus of the lateral olfactory tract

LOT 1:

Nucleus of the lateral olfactory tract, layer 1

LOT 2:

Nucleus of the lateral olfactory tract, layer 2

LOT 3:

Nucleus of the lateral olfactory tract, layer 3

LPO:

Lateral preoptic area

LS:

Lateral septum

LSD:

Lateral septal nucleus, dorsal part

LSI:

Lateral septal nucleus, intermediate part

LSV:

Lateral septal nucleus, ventral part

LV:

Lateral ventricle

M1:

Primary motor cortex

M2:

Secondary motor cortex

MCPO:

Magnocellular preoptic nucleus

MD:

Mediodorsal thalamic nucleus

Me:

Medial amygdaloid nucleus

MeA:

Medial amygdaloid nucleus, anterior part

MeAD:

Medial amygdaloid nucleus, anterior dorsal part

MeAV:

Medial amygdaloid nucleus, anteroventral part

MePD:

Medial amygdaloid nucleus, posterodorsal part

MePV:

Medial amygdaloid nucleus, posteroventral part

mfb:

Medial forebrain bundle

MGP:

Medial globus pallidus (entopeduncular nucleus)

MnPO:

Median preoptic nucleus

MO:

Medial orbital cortex

MPA:

Medial preoptic area

MPO:

Medial preoptic nucleus

MPOM:

Medial preoptic nucleus, medial part

MS:

Medial septal nucleus

mvStP:

Medioventral striato-pallidum

NADPHd:

Nicotinamide adenine dinucleotide phosphate diaphorase

opt:

Optic tract

Or:

Oriens layer of the hippocampus

PaAP:

Paraventricular hypothalamic nucleus, anterior parvicellular part

PB:

Phosphate buffer

PBS:

Phosphate buffered saline

Pir:

Piriform cortex

PLCo:

Posterolateral cortical amygdaloid nucleus

PMCo:

Posteromedial cortical amygdaloid nucleus

PRh:

Perirhinal cortex

PrL:

Prelimbic cortex

PT:

Paratenial thalamic nucleus

PVA:

Paraventricular thalamic nucleus, anterior part

Py:

Pyramidal cell layer of the hippocampus

Rad:

Stratum radiatum of the hippocampus

Re:

Reuniens thalamic nucleus

Rt:

Reticular thalamic nucleus

SCh:

Suprachiasmatic nucleus

SFi:

Septofimbrial nucleus

SFO:

Subfornical organ

SHi:

Septohippocampal nucleus

SHy:

Septohypothalamic nucleus

SI:

Substantia innominata

SLu:

Stratum lucidum, hippocampus

SM:

Nucleus of the stria medullaris

sm:

Stria medullaris of the thalamus

SO:

Supraoptic nucleus

SP:

Substance P

st:

Stria terminalis

StA:

Strial part of the preoptic area

TBS:

TRIS buffered saline

Tu:

Olfactory tubercle

V1aR:

Arginine-vasopressin receptor type 1a

V1bR:

Arginine-vasopressin receptor type 1b

VA:

Ventral anterior thalamic nucleus

VEn:

Ventral endopiriform nucleus

VDB:

Ventral diagonal band

VLPO:

Ventrolateral preoptic nucleus

VMPO:

Ventromedial preoptic nucleus

VO:

Ventral orbital cortex

VOLT:

Vascular organ of the lamina terminalis

VP:

Ventral pallidum

VTT:

Ventral tenia tecta

Xi:

Xiphoid thalamic nucleus

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Acknowledgments

This work has been funded by the Spanish Ministry of Science-FEDER (BFU2007-67912/BFI and BFU2010-16656/BFI), the Generalitat Valenciana (ACOMP/2010/127) and the Junta de Comunidades de Castilla-La Mancha/FEDER (PEIC11-0045-4490). This paper is part of the Doctoral Thesis of Marcos Otero-Garcia. The authors are indebted to Adoración Hernandez-Martinez for her invaluable help throughout the experimental work.

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The authors declare that they have no conflict of interest.

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Correspondence to Fernando Martínez-García.

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Otero-Garcia, M., Martin-Sanchez, A., Fortes-Marco, L. et al. Extending the socio-sexual brain: arginine-vasopressin immunoreactive circuits in the telencephalon of mice. Brain Struct Funct 219, 1055–1081 (2014). https://doi.org/10.1007/s00429-013-0553-3

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