Brain Structure and Function

, Volume 222, Issue 2, pp 895–921

Tuning the brain for motherhood: prolactin-like central signalling in virgin, pregnant, and lactating female mice

  • Hugo Salais-López
  • Enrique Lanuza
  • Carmen Agustín-Pavón
  • Fernando Martínez-García
Original Article

DOI: 10.1007/s00429-016-1254-5

Cite this article as:
Salais-López, H., Lanuza, E., Agustín-Pavón, C. et al. Brain Struct Funct (2017) 222: 895. doi:10.1007/s00429-016-1254-5

Abstract

Prolactin is fundamental for the expression of maternal behaviour. In virgin female rats, prolactin administered upon steroid hormone priming accelerates the onset of maternal care. By contrast, the role of prolactin in mice maternal behaviour remains unclear. This study aims at characterizing central prolactin activity patterns in female mice and their variation through pregnancy and lactation. This was revealed by immunoreactivity of phosphorylated (active) signal transducer and activator of transcription 5 (pSTAT5-ir), a key molecule in the signalling cascade of prolactin receptors. We also evaluated non-hypophyseal lactogenic activity during pregnancy by administering bromocriptine, which suppresses hypophyseal prolactin release. Late-pregnant and lactating females showed significantly increased pSTAT5-ir resulting in a widespread pattern of immunostaining with minor variations between pregnant and lactating animals, which comprises nuclei of the sociosexual and maternal brain, including telencephalic (septum, nucleus of the stria terminalis, and amygdala), hypothalamic (preoptic, paraventricular, supraoptic, and ventromedial), and midbrain (periaqueductal grey) regions. During late pregnancy, this pattern was not affected by the administration of bromocriptine, suggesting it to be elicited mostly by non-hypophyseal lactogenic agents, likely placental lactogens. Virgin females displayed, instead, a variable pattern of pSTAT5-ir restricted to a subset of the brain nuclei labelled in pregnant and lactating mice. A hormonal substitution experiment confirmed that estradiol and progesterone contribute to the variability found in virgin females. Our results reflect how the shaping of the maternal brain takes place prior to parturition and suggest that lactogenic agents are important candidates in the development of maternal behaviours already during pregnancy.

Keywords

Maternal care Maternal aggression Placental lactogens pSTAT5 CD1 mice Sociosexual brain 

Abbreviations

10N

Dorsal motor nucleus of vagus

12N

Hypoglossal nucleus

3V

Third ventricle

AAD

Anterior amygdaloid area, dorsal part

AAV

Anterior amygdaloid area, ventral part

AC

Anterior commissural nucleus

aca

Anterior commissure, anterior part

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

AHC

Anterior hypothalamic area, central part

AHiAL

Amygdalohippocampal area, anterolateral part

AHiPM

Amygdalohippocampal area, posteromedial part

AHP

Anterior hypothalamic area, posterior part

AP

Area postrema

APT

Anterior pretectal nucleus

Aq

Aqueduct (Sylvius)

Arc

Arcuate hypothalamic nucleus

AVPe

Anteroventral periventricular nucleus

BAC

Bed nucleus of the anterior commissure

Bar

Barrington’s nucleus

BIC

Nucleus of the brachium of the inferior colliculus

bic

Brachium of the inferior colliculus

BLA

Basolateral amygdaloid nucleus, anterior part

BLP

Basolateral amygdaloid nucleus, posterior part

BLV

Basolateral amygdaloid nucleus, ventral part

BMA

Basomedial amygdaloid nucleus, anterior part

BMP

Basomedial amygdaloid nucleus, posterior part

bp

Brachium pontis

BSTIA

Bed nucleus of the stria terminalis, intra-amygdaloid division

BSTLD

Bed nucleus of the stria terminalis, lateral division, dorsal 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

BSTMV

Bed nucleus of the stria terminalis, medial division, ventral 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

cc

Corpus callosum

CC

Central canal

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, anterodorsal part

CeMPV

Central amygdaloid nucleus, medial division, posteroventral part

cg

Cingulum

CI

Caudal interstitial nucleus of the medial longitudinal fasciculum

Cir

Circular nucleus

CLi

Caudal linear nucleus of the raphe

CP

Choroid plexus

cp

Cerebral peduncle, basal part

CPu

Caudate putamen (striatum)

Cu

Cuneate nucleus

CxA

Cortex-amygdala transition zone

D3V

Dorsal third ventricle

Den

Dorsal endopiriform nucleus

Dk

Nucleus of Darkschewitsch

DLG

Dorsal lateral geniculate nucleus

DLPAG

Dorsolateral periaqueductal grey

DM

Dorsomedial hypothalamic nucleus

DMPAG

Dorsomedial periaqueductal grey

DMTg

Dorsomedial tegmental area

DP

Dorsal peduncular cortex

DpG

Deep grey layer of the superior colliculus

DpMe

Deep mesencephalic nucleus

DPO

Dorsal periolivary region

DpWh

Deep white layer of the superior colliculus

DR

Dorsal raphe nucleus

DTgC

Dorsal tegmental nucleus, central part

DTT

Dorsal taenia tecta

eml

External medullary lamina

EW

Edinger–Westphal nucleus

f

Fornix

fi

Fimbria of the hippocampus

fmi

Forceps minor of the corpus callosum

fr

Fasciculus retroflexus

HDB

Nucleus of the horizontal limb of the diagonal band

I

Intercalated nuclei of the amygdala

ic

Internal capsule

IF

Interfascicular nucleus

IGL

Intergeniculate leaf

IL

Infralimbic cortex

InC

Interstitial nucleus of Cajal

InCO

Intercollicular nucleus

InG

Intermediate grey layer of the superior colliculus

InWh

Intermediate white layer of the superior colliculus

IP

Interpeduncular nucleus

IPAC

Interstitial nucleus of the posterior limb of the anterior commissure

IRt

Intermediate reticular nucleus

La

Lateral amygdaloid nucleus

LA

Lateroanterior hypothalamic nucleus

LC

Locus coeruleus

Ld

Lambdoid septal zone

LD

Laterodorsal thalamic nucleus

LDTg

Laterodorsal tegmental nucleus

LGP

Lateral globus pallidus

LH

Lateral hypothalamic area

LHb

Lateral habenular nucleus

ll

Lateral lemiscus

lo

Lateral olfactory tract

LOT

Nucleus of the lateral olfactory tract

LP

Lateral posterior thalamic nucleus

LPAG

Lateral periaqueductal grey

LPBC

Lateral parabrachial nucleus, central part

LPBD

Lateral parabrachial nucleus, dorsal part

LPBE

Lateral parabrachial nucleus, external part

LPBI

Lateral parabrachial nucleus, internal part

LPBV

Lateral parabrachial nucleus, ventral part

LPMR

Lateral posterior thalamic nucleus, mediorostral part

LPO

Lateral preoptic area

LRt

Lateral reticular nucleus

LSD

Lateral septal nucleus, dorsal part

LSI

Lateral septal nucleus, intermediate part

LSO

Lateral superior olive

LSV

Lateral septal nucleus, ventral part

LV

Lateral ventricle

MCLH

Magnocellular nucleus of the lateral hypothalamus

mcp

Middle cerebellar peduncle

MCPC

Magnocellular precommissural nucleus

MCPO

Magnocellular preoptic nucleus

MdD

Medullary reticular nucleus, dorsal part

MdV

Medullary reticular nucleus, ventral part

ME

Median eminence

MeA

Medial amygdaloid nucleus, anterior part

MePD

Medial amygdaloid nucleus, posterodorsal part

MePV

Medial amygdaloid nucleus, posteroventral part

MGD

Medial geniculate nucleus, dorsal part

MGM

Medial geniculate nucleus, medial part

MGP

Medial globus pallidus

MGV

Medial geniculate nucleus, ventral part

MHb

Medial habenular nucleus

ml

Medial lemniscus

mlf

Medial longitudinal fasciculus

MnPO

Median preoptic nucleus

MnR

Median raphe nucleus

MPA

Medial preoptic area

MPB

Medial parabrachial nucleus

MPBE

Medial parabrachial nucleus, external part

MPO

Medial preoptic nucleus

MS

Medial septal nucleus

mt

Mammilothalamic tract

MTu

Medial tuberal nucleus

MZMGV

Marginal zone of the medial geniculate

ns

Nigrostriatal bundle

opt

Optic tract

OPT

Olivary pretectal nucleus

OT

Nucleus of the optic tract

ox

Optic chiasm

PAG

Periaqueductal grey

PaLM

Paraventricular nucleus, lateral magnocellular part

PaMM

Paraventricular nucleus, medial magnocellular part

PaPO

Paraventricular nucleus, posterior part

PaV

Paraventricular nucleus, ventral part

PCom

Nucleus of the posterior commissure

Pe

Periventricular hypothalamic nucleus

PeF

Perifornical nucleus

PF

Parafascicular thalamic nucleus

PH

Posterior hypothalamic area

PIL

Posterior-intralaminar thalamic nucleus

Pir

Piriform cortex

PLCo

Posterolateral cortical amygdaloid nucleus

PM

Paramedian lobule

PMD

Premammillary nucleus, dorsal part

PMV

Premammillary nucleus, ventral part

PnC

Pontine reticular nucleus, caudal part

PnO

Pontine reticular nucleus, oral part

PnR

Pontine raphe nucleus

PnV

Pontine reticular nucleus, ventral part

PoT

Posterior thalamic nuclear group, triangular part

PP

Peripeduncular nucleus

PPT

Posterior pretectal nucleus

PPTg

Pedunculopontine tegmental nucleus

Pr5

Principal sensory trigeminal nucleus

PSTh

Parasubthalamic nucleus

PV

Paraventricular thalamic nucleus

PVA

Paraventricular thalamic nucleus, anterior part

py

Pyramidal tract

R

Red nucleus

RCh

Retrochiasmatic area

Re

Reuniens thalamic nucleus

RMg

Raphe magnus nucleus

Rob

Raphe obscurus nucleus

rs

Rubrospinal tract

Rt

Reticular thalamic nucleus

s5

Sensory root of the trigeminal nerve

SCh

Suprachiasmatic nucleus

SCO

Subcommissural organ

scp

Superior cerebellar peduncle

SFi

Septofimbrial nucleus

SFO

Subfornical organ

SG

Suprageniculate thalamic nucleus

SHi

Septohippocampal nucleus

SI

Substantia innominata

SLEA

Sublenticular extended amygdala

sm

Stria medullaris of the thalamus

SN

Substantia nigra

SNC

Substantia nigra, pars compacta

SNR

Substantia nigra, reticular part

SO

Supraoptic nucleus

sol

Solitary tract

Sol

Nucleus of the solitary tract

SolC

Nucleus of the solitary tract, commissural part

SolDL

Nucleus of the solitary tract, dorsolateral part

SolG

Nucleus of the solitary tract, gelatinous part

SolM

Nucleus of the solitary tract, medial part

SolV

Nucleus of the solitary tract, ventral part

Sp5

Spinal trigeminal nucleus

Spa

Subparaventricular zone of the hypothalamus

SPFPC

Subparafascicular thalamic nucleus, parvicellular part

SPO

Superior paraolivary nucleus

st

Stria terminalis

STh

Subthalamic nucleus

str

Superior thalamic radiation

SubB

Subbrachial nucleus

SubCD

Subcoeruleus nucleus, dorsal part

SubCV

Subcoeruleus nucleus, ventral part

SubG

Subgeniculate nucleus

SubI

Subincertal nucleus

SuMM

Supramammillary nucleus, medial part

TC

Tuber cinereum

Te

Terete hypothalamic nucleus

Tu

Olfactory tubercle

VEn

Ventral endopiriform nucleus

VLG

Ventral lateral geniculate nucleus

VLGMC

Ventral lateral geniculate nucleus, magnocellular part

VLGPC

Ventral lateral geniculate nucleus, parvicellular part

VLPAG

Ventrolateral periaqueductal grey

VLPO

Ventrolateral preoptic 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

VRe

Ventral reuniens thalamic nucleus

vsc

Ventral spinocerebellar tract

VTA

Ventral tegmental area

ZI

Zona incerta

ZID

Zona incerta, dorsal part

ZIV

Zona incerta, ventral part

Supplementary material

429_2016_1254_MOESM1_ESM.pdf (718 kb)
Supplementary material 1 (PDF 718 kb)

Funding information

Funder NameGrant NumberFunding Note
Spanish Ministry of Science-FEDER
  • BFU2013-47688-P
Secretaría de Estado de Investigación, Desarrollo e Innovación
  • BFU2013-47688-P
Junta de Comunidades de Castilla la Mancha
  • PEIC-2014-006-P
Ministerio de Educación, Cultura y Deporte
  • FPU12/05472

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Hugo Salais-López
    • 1
  • Enrique Lanuza
    • 2
  • Carmen Agustín-Pavón
    • 1
  • Fernando Martínez-García
    • 1
  1. 1.Unitat Predepartamental de Medicina, Facultat de Ciències de la SalutUniversitat Jaume ICastelló de la PlanaSpain
  2. 2.Departaments de Biologia Cel·lular i Biologia Funcional, Facultat de Ciències BiològiquesUniversitat de ValènciaBurjassotSpain

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