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Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice

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Abstract

Oxytocin (OT) and vasopressin (AVP) play a major role in social behaviours. Mice have become the species of choice for neurobiology of social behaviour due to identification of mouse pheromones and the advantage of genetically modified mice. However, neuroanatomical data on nonapeptidergic systems in mice are fragmentary, especially concerning the central distribution of OT. Therefore, we analyse the immunoreactivity for OT and its neurophysin in the brain of male and female mice (strain CD1). Further, we combine immunofluorescent detection of OT and AVP to locate cells co-expressing both peptides and their putative axonal processes. The results indicate that OT is present in cells of the neurosecretory paraventricular (Pa) and supraoptic hypothalamic nuclei (SON). From the anterior SON, OTergic cells extend into the medial amygdala, where a sparse cell population occupies its ventral anterior and posterior divisions. Co-expression of OT and AVP in these nuclei is rare. Moreover, a remarkable OTergic cell group is found near the ventral bed nucleus of the stria terminalis (BST), distributed between the anterodorsal preoptic nucleus and the nucleus of anterior commissure (ADP/AC). This cell group, the rostral edge of the Pa and the periventricular hypothalamus display frequent OT + AVP double labelling, with a general dominance of OT over AVP immunoreactivity. Fibres with similar immunoreactivity profile innervate the accumbens shell and core, central amygdala and portions of the intervening BST. These data, together with data in the literature on rats, suggest that the projections of ADP/AC nonapeptidergic cells onto these brain centres could promote pup-motivated behaviours and inhibit pup avoidance during motherhood.

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Abbreviations

10N:

Dorsal motor nucleus of the vagus

12N:

Hypoglossal nucleus

3V:

Third ventricle

4n:

Trochlear nerve or its root

4V:

4th ventricle

A1:

A1 noradrenaline cells

AC:

Anterior commissural nucleus

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

AHP:

Anterior hypothalamic area, posterior part

AIP:

Agranular insular cortex, posterior part

AM:

Anteromedial thalamic nucleus

Amb:

Ambiguus nucleus

AN:

Accessory nuclei

AP:

Area postrema

APir:

Amygdalopiriform transition area

Aq:

Aqueduct (Sylvius)

Arc:

Arcuate hypothalamic nucleus

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

Bar:

Barrington’s nucleus

BLA:

Basolateral amygdaloid nucleus, anterior

BLV:

Basolateral amygdaloid nucleus, ventral

BMA:

Basomedial amygdaloid nucleus, anterior

BST:

Bed nucleus of the stria terminalis

BSTA:

Bed nucleus of the stria terminalis, anterior part

BSTIA:

Bed nucleus of the stria terminalis, intraamygdaloid division

BSTLD:

Bed nucleus of the stria terminalis, lateral division, dorsal 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

cc:

Corpus callosum

CC:

Central canal

Ce:

Central amygdaloid nucleus

CeC:

Central amygdaloid nucleus, capsular part

CeL:

Central amygdaloid nucleus, lateral division

CeM:

Central amygdaloid nucleus, medial division

CeMAD:

Central amygdaloid nucleus, medial division, anterodorsal part

CeMAV:

Central amygdaloid nucleus, medial division, anteroventral part

CGPn:

Central grey of the pons

Cl:

Claustrum

CL:

Centrolateral thalamic nucleus

CM:

Central medial thalamic nucleus

cp:

Cerebral peduncle, basal part

CPu:

Caudate putamen (striatum)

cst:

Commissural stria terminalis

Cu:

Cuneate nucleus

CxA:

Cortex–amygdala transition zone

D3V:

Dorsal third ventricle

DEn:

Dorsal endopiriform nucleus

DG:

Dentate gyrus

DLPAG:

Dorsolateral periaqueductal grey

DM:

Dorsomedial hypothalamic nucleus

DMPAG:

Dorsomedial periaqueductal grey

DMTg:

Dorsomedial tegmental nucleus

DP:

Dorsal peduncular cortex

DpMe:

Deep mesencephalic nucleus

DRC:

Dorsal raphe nucleus, caudal part

DRI:

Dorsal raphe nucleus, interfascicular part

DTg:

Dorsal tegmental nucleus

DTgP:

Dorsal tegmental nucleus, pericentral part

DTM:

Dorsal tuberomammillary nucleus

DTT:

Dorsal tenia tecta

ECu:

External cuneate nucleus

EW:

Edinger–Westphal nucleus

f:

Fornix

F:

Nucleus of the fields of Forel

FG:

Fluorogold

fi:

Fimbria of the hippocampus

fmi:

Forceps minor of the corpus callosum

fr:

Fasciculus retroflexus

GrDG:

Granular layer of the dentate gyrus

Gus:

Gustatory thalamic nucleus

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

ICjvm:

Islands of Calleja, ventromedial island

icp:

Inferior cerebellar peduncle

IG:

Indusium griseum

IL:

Infralimbic cortex

IM:

Intercalated amygdaloid nucleus, main part

In:

Intercalated nucleus of the medulla

IO:

Inferior olive

IOD:

Inferior olive, dorsal nucleus

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

IRt:

Intermediate reticular nucleus

KF:

Kölliker-Fuse nucleus

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

LC:

Locus coeruleus

LDTg:

Laterodorsal tegmental nucleus

LDTgV:

Laterodorsal tegmental nucleus, ventral part

LEnt:

Lateral entorhinal cortex

LGP:

Lateral globus pallidus

LH:

Lateral hypothalamic area

LHb:

Lateral habenular nucleus

lo:

Lateral olfactory tract

LPBE:

Lateral parabrachial nucleus, external part

LPBS:

Lateral parabrachial nucleus, superior part

LPBV:

Lateral parabrachial nucleus, ventral part

LPMR:

Lateral posterior thalamic nucleus, mediodorsal part

LPO:

Lateral preoptic area

LRt:

Lateral reticular nucleus

LS:

Lateral septum

LSD:

Lateral septal nucleus, dorsal part

LSI:

Lateral septal nucleus, intermediate part

LSV:

Lateral septal nucleus, ventral part

LV:

Lateral ventricle

maopt:

Medial accessory optic tract

MCLH:

Magnocellular nucleus of the lateral hypothalamus

MCPO:

Magnocellular preoptic nucleus

MD:

Mediodorsal thalamic nucleus

MdD:

Medullary reticular nucleus, dorsal part

MdV:

Medullary reticular nucleus, ventral part

Me:

Medial amygdaloid nucleus

Me5:

Mesencephalic trigeminal 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)

MHb:

Medial habenular nucleus

ml:

Medial lemniscus

mlf:

Medial longitudinal fasciculus

MnPO:

Median preoptic nucleus

MPA:

Medial preoptic area

MPB:

Medial parabrachial nucleus

MPO:

Medial preoptic nucleus

MPOL:

Medial preoptic nucleus, lateral part

MPOM:

Medial preoptic nucleus, medial part

MS:

Medial septal nucleus

mt:

Mammillothalamic tract

mtg:

Mammillotegmental tract

MTu:

Medial tuberal nucleus

MVe:

Medial vestibular nucleus

mvStP:

Medioventral striato-pallidum

NADPHd:

Nicotinamide adenine dinucleotide phosphate diaphorase

ns:

Nigrostriatal bundle

O:

Nucleus O

opt:

Optic tract

OT:

Oxytocin

OT-ir:

Oxytocin-like immunoreactive (referring to immunostaining using antibodies raised against oxytocin or against its specific neurophysin)

OTR:

Oxytocin receptor

PaAP:

Paraventricular hypothalamic nucleus, anterior parvicellular

PAG:

Periaqueductal grey

PaL:

Paraventricular hypothalamic nucleus, lateral part

PaM:

Paraventricular hypothalamic nucleus, medial part

PaPo:

Paraventricular hypothalamic nucleus, posterior part

PaV:

Paraventricular hypothalamic nucleus, ventral part

PB:

Phosphate buffer

PBS:

Phosphate-buffered saline

PC:

Paracentral thalamic nucleus

Pc:

Posterior commissure

PCom:

Nucleus of the posterior commissure

Pe:

Periventricular hypothalamic nucleus

PeF:

Perifornical nucleus

PF:

Parafascicular thalamic nucleus

PH:

Posterior hypothalamic area

Pir:

Piriform cortex

PLCo:

Posterolateral cortical amygdaloid nucleus

PMCo:

Posteromedial cortical amygdaloid nucleus

PMD:

Premammillary nucleus, dorsal part

PMn:

Paramedian reticular nucleus

PMnR:

Paramedian raphe nucleus

PMV:

Premammillary nucleus, ventral part

PnC:

Pontine reticular nucleus, caudal part

PO:

Periolivary region

Pr5:

Principal sensory trigeminal nucleus

PRh:

Perirhinal cortex

PrL:

Prelimbic cortex

PSTh:

Parasubthalamic nucleus

PT:

Paratenial thalamic nucleus

PV:

Paraventricular 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

RI:

Rostral interstitial nucleus of the medial longitudinal fasciculus

RLi:

Rostral linear nucleus of the raphe

RMg:

Raphe magnus nucleus

RPF:

Retroparafascicular nucleus

RRF:

Retrorubral field

rs:

Rubrospinal tract

Rt:

Reticular thalamic nucleus

SCh:

Suprachiasmatic nucleus

SCO:

Subcommissural organ

scp:

Superior cerebellar peduncle

SFi:

Septofimbrial nucleus

SFO:

Subfornical organ

Shi:

Septohippocampal nucleus

SHy:

Septohypothalamic nucleus

SI:

Substantia innominata

SL:

Semilunar nucleus

SLu:

Stratum lucidum, hippocampus

SM:

Nucleus of the stria medullaris

sm:

Stria medullaris of the thalamus

SN:

Substantia nigra

Sol:

Nucleus of the solitary tract

sol:

Solitary tract

SON:

Supraoptic nucleus

SOR:

Supraoptic nucleus, retrochiasmatic part

sp5:

Spinal trigeminal tract

st:

Stria terminalis

StA:

Striatal part of the preoptic area

Su3:

Supraoculomotor periaqueductal grey

Su5:

Supratrigeminal nucleus

SubB:

Subbrachial nucleus

SubC:

Subcoeruleus nucleus

TBS:

TRIS-buffered saline

TC:

Tuber cinereum area

Te:

Terete hypothalamic nucleus

Tu:

Olfactory tubercle

Unc:

Uncinate fasciculus

V1aR:

Arginine vasopressin receptor type 1a

V1bR:

Arginine vasopressin receptor type 1b

VA:

Ventral anterior thalamic nucleus

VDB:

Nucleus of the vertical limb of the diagonal band

VEn:

Ventral endopiriform nucleus

VLPO:

Ventrolateral preoptic nucleus

VM:

Ventromedial thalamic nucleus

VMH:

Ventromedial hypothalamic nucleus

VMHC:

Ventromedial hypothalamic nucleus, central part

VMHDM:

Ventromedial hypothalamic nucleus, dorsomedial part

VMHVL:

Ventromedial hypothalamic nucleus, ventrolateral part

VMPO:

Ventromedial preoptic nucleus

VOLT:

Vascular organ of the lamina terminalis

VP:

Ventral pallidum

vsc:

Ventral spinocerebellar tract

VTA:

Ventral tegmental area

VTg:

Ventral tegmental nucleus

VTM:

Ventral tuberomammillary nucleus

VTT:

Ventral tenia tecta

Xi:

Xiphoid thalamic nucleus

ZI:

Zona incerta

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Acknowledgments

This work was funded by the Spanish Ministry of Science—FEDER (BFU2013-47688-P), the Junta de Comunidades de Castilla-La Mancha/FEDER (PEIC11-0045-4490) and the Universitat Jaume I. This work is part of the doctoral thesis of Marcos Otero-García, granted by the FPU (Formación de Profesorado Universitario) programme of the Spanish Ministry of Education and Science. The authors gratefully acknowledge Dr. Harold Gainer for his generous gift of antibodies.

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  1. Lab. of Functional Neuroanatomy (NeuroFun), Unitat Predepartamental de Medicina, Facultat de Ciències de la Salut, Universitat Jaume I, Av. de Vicent Sos Baynat, s/n, 12071, Castelló de la Plana, Spain

    Carmen Agustín-Pavón & Fernando Martínez-García

  2. Departaments de Biologia Cel·lular i de Biologia Funcional, Facultat de Ciències Biològiques, Universitat de València, València, Spain

    Marcos Otero-García & Enrique Lanuza

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  1. Marcos Otero-García
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  4. Fernando Martínez-García
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Otero-García, M., Agustín-Pavón, C., Lanuza, E. et al. Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice. Brain Struct Funct 221, 3445–3473 (2016). https://doi.org/10.1007/s00429-015-1111-y

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