Although maternal separation and neonatal paternal deprivation (PD) have been found to exert a profound and persistent effects on the physiological and behavioural development of offspring, whether preweaning PD (PPD; from PND 10 to 21) affects maternal and parental responses to pups and the underlying neuroendocrine mechanism are under-investigated. Using monogamous mandarin voles (Microtus mandarinus), the present study found that PPD increased the latency to approach a pup-containing ball, decreased the total durations of sniffing and contacting a pup-containing ball and walking and increased the total duration of inactivity in both sexes. Moreover, PPD decreased serum oxytocin levels and increased corticosterone levels, but only in females. Furthermore, in both males and females, PPD decreased the expression of oxytocin receptor mRNA and protein in the medial preoptic area (MPOA), nucleus accumbens (NAcc) and medial prefrontal cortex (mPFC), but increased it in the medial amygdala (MeA) and decreased the expression of oestrogen receptor mRNA and protein in the MPOA. PPD increased the expression of dopamine type I receptor in the NAcc, but decreased it in the mPFC. PPD decreased dopamine type II receptor (D2R) in the NAcc both in males and females, but increased D2R in the mPFC in females and decreased D2R protein expression in males. Moreover, PPD decreased vasopressin 1A receptor (V1AR) in the MPOA, MeA and mPFC, but only in males. Our results suggest that the reduction of parental responses to pups induced by PPD may be associated with the sex-specific alteration of several neuroendocrine parameters in relevant brain regions.

1.
Rilling
JK
,
Young
LJ
.
The biology of mammalian parenting and its effect on offspring social development
.
Science
.
2014
Aug
;
345
(
6198
):
771
6
.
[PubMed]
0036-8075
2.
Jia
R
,
Tai
F
,
An
S
,
Zhang
X
,
Broders
H
.
Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in mandarin voles
.
Behav Processes
.
2009
Nov
;
82
(
3
):
271
8
.
[PubMed]
0376-6357
3.
Barnow
S
,
Lucht
M
,
Freyberger
HJ
.
Influence of punishment, emotional rejection, child abuse, and broken home on aggression in adolescence: an examination of aggressive adolescents in Germany
.
Psychopathology
.
2001
Jul-Aug
;
34
(
4
):
167
73
.
[PubMed]
0254-4962
4.
Heim
C
,
Nemeroff
CB
.
The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies
.
Biol Psychiatry
.
2001
Jun
;
49
(
12
):
1023
39
.
[PubMed]
0006-3223
5.
Heim
C
,
Newport
DJ
,
Mletzko
T
,
Miller
AH
,
Nemeroff
CB
.
The link between childhood trauma and depression: insights from HPA axis studies in humans
.
Psychoneuroendocrinology
.
2008
Jul
;
33
(
6
):
693
710
.
[PubMed]
0306-4530
6.
Parker
G
.
Parental deprivation and depression in a non-clinical group
.
Aust N Z J Psychiatry
.
1979
Mar
;
13
(
1
):
51
6
.
[PubMed]
0004-8674
7.
Kleiman
DG
,
Malcolm
JR
.
The evolution of male parental investment in mammals
.
New York
:
Plenum Press
;
1981
.
8.
Wang
ZX
,
Novak
MA
.
Alloparental care and the influence of father presence on juvenile prairie voles (Microtus ochrogaster)
.
Anim Behav
.
1994
;
47
(
2
):
281
8
. 0003-3472
9.
Chang
L
,
Schwartz
D
,
Dodge
KA
,
McBride-Chang
C
.
Harsh parenting in relation to child emotion regulation and aggression
.
J Fam Psychol
.
2003
Dec
;
17
(
4
):
598
606
.
[PubMed]
0893-3200
10.
Ember
CR
,
Ember
M
.
War, socialization, and interpersonal violence: a cross-cultural study
.
J Conflict Resolut
.
1994
;
38
(
4
):
620
46
. 0022-0027
11.
Flinn
MV
,
England
BG
.
Social economics of childhood glucocorticoid stress response and health
.
Am J Phys Anthropol
.
1997
Jan
;
102
(
1
):
33
53
.
[PubMed]
0002-9483
12.
Ahern
TH
,
Young
LJ
.
The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (microtus ochrogaster)
.
Front Behav Neurosci
.
2009
Aug
;
3
:
17
.
[PubMed]
1662-5153
13.
Cao
Y
,
Wu
R
,
Tai
F
,
Zhang
X
,
Yu
P
,
An
X
, et al
Neonatal paternal deprivation impairs social recognition and alters levels of oxytocin and estrogen receptor α mRNA expression in the MeA and NAcc, and serum oxytocin in mandarin voles
.
Horm Behav
.
2014
Jan
;
65
(
1
):
57
65
.
[PubMed]
0018-506X
14.
Jia
R
,
Tai
F
,
An
S
,
Zhang
X
.
Neonatal paternal deprivation or early deprivation reduces adult parental behavior and central estrogen receptor α expression in mandarin voles (Microtus mandarinus)
.
Behav Brain Res
.
2011
Oct
;
224
(
2
):
279
89
.
[PubMed]
0166-4328
15.
Yu
P
,
An
S
,
Tai
F
,
Zhang
X
,
He
F
,
Wang
J
, et al
The effects of neonatal paternal deprivation on pair bonding, NAcc dopamine receptor mRNA expression and serum corticosterone in mandarin voles
.
Horm Behav
.
2012
May
;
61
(
5
):
669
77
.
[PubMed]
0018-506X
16.
Yu
P
,
Zhang
H
,
Li
X
,
He
F
,
Tai
F
.
Early bi-parental separation or neonatal paternal deprivation in mandarin voles reduces adult offspring paternal behavior and alters serum corticosterone levels and neurochemistry
.
Horm Behav
.
2015
Jul
;
73
:
8
14
.
[PubMed]
0018-506X
17.
Wang
B
,
Li
L
,
He
Z
,
Wang
L
,
Zhang
S
,
Qiao
H
, et al
Effects of reproductive experience on paternal behavior, levels of testosterone, prolactin in serum and dendritic spines in medial prefrontal cortex of mandarin voles
.
Integr Zool
.
2018
Nov
;
13
(
6
):
711
22
.
[PubMed]
1749-4869
18.
Yuan
W
,
He
Z
,
Hou
W
,
Wang
L
,
Li
L
,
Zhang
J
, et al
Role of oxytocin in the medial preoptic area (MPOA) in the modulation of paternal behavior in mandarin voles
.
Horm Behav
.
2019
Apr
;
110
:
46
55
.
[PubMed]
0018-506X
19.
He
Z
,
Zhang
S
,
Yu
C
,
Li
Y
,
Jia
R
,
Tai
F
.
Emotional attachment of pre-weaning pups to mothers and fathers in mandarin voles
.
Behav Processes
.
2017
Feb
;
135
:
87
94
.
[PubMed]
0376-6357
20.
Grossmann
K
,
Grossmann
KE
,
Fremmer-Bombik
E
,
Kindler
H
,
Scheuerer-Englisch
H
,
Zimmermann
AP
.
The uniqueness of the child–father attachment relationship: fathers’ sensitive and challenging play as a pivotal variable in a 16-year longitudinal study
.
Soc Dev
.
2002
;
11
(
3
):
301
37
. 0961-205X
21.
Sobrinho
LG
,
Duarte
JS
,
Paiva
I
,
Gomes
L
,
Vicente
V
,
Aguiar
P
.
Paternal deprivation prior to adolescence and vulnerability to pituitary adenomas
.
Pituitary
.
2012
Jun
;
15
(
2
):
251
7
.
[PubMed]
1386-341X
22.
Galbally
M
,
Lewis
AJ
,
Ijzendoorn
M
,
Permezel
M
.
The role of oxytocin in mother-infant relations: a systematic review of human studies
.
Harv Rev Psychiatry
.
2011
Jan-Feb
;
19
(
1
):
1
14
.
[PubMed]
1067-3229
23.
Kim
S
,
Fonagy
P
,
Koos
O
,
Dorsett
K
,
Strathearn
L
.
Maternal oxytocin response predicts mother-to-infant gaze
.
Brain Res
.
2014
Sep
;
1580
:
133
42
.
[PubMed]
0006-8993
24.
Fahrbach
SE
,
Morrell
JI
,
Pfaff
DW
.
Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats
.
Horm Behav
.
1984
Sep
;
18
(
3
):
267
86
.
[PubMed]
0018-506X
25.
Pedersen
CA
,
Caldwell
JD
,
Walker
C
,
Ayers
G
,
Mason
GA
.
Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas
.
Behav Neurosci
.
1994
Dec
;
108
(
6
):
1163
71
.
[PubMed]
0735-7044
26.
Williams
JR
,
Insel
TR
,
Harbaugh
CR
,
Carter
CS
.
Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster)
.
J Neuroendocrinol
.
1994
Jun
;
6
(
3
):
247
50
.
[PubMed]
0953-8194
27.
Song
Z
,
Tai
F
,
Yu
C
,
Wu
R
,
Zhang
X
,
Broders
H
, et al
Sexual or paternal experiences alter alloparental behavior and the central expression of ERalpha and OT in male mandarin voles (Microtus mandarinus)
.
Behav Brain Res
.
2010
Dec
;
214
(
2
):
290
300
.
[PubMed]
0166-4328
28.
de Jong
TR
,
Chauke
M
,
Harris
BN
,
Saltzman
W
.
From here to paternity: neural correlates of the onset of paternal behavior in California mice (Peromyscus californicus)
.
Horm Behav
.
2009
Aug
;
56
(
2
):
220
31
.
[PubMed]
0018-506X
29.
Lambert
KG
,
Franssen
CL
,
Bardi
M
,
Hampton
JE
,
Hainley
L
,
Karsner
S
, et al
Characteristic neurobiological patterns differentiate paternal responsiveness in two Peromyscus species
.
Brain Behav Evol
.
2011
;
77
(
3
):
159
75
.
[PubMed]
1421-9743
30.
Kenkel
WM
,
Paredes
J
,
Yee
JR
,
Pournajafi-Nazarloo
H
,
Bales
KL
,
Carter
CS
.
Neuroendocrine and behavioural responses to exposure to an infant in male prairie voles
.
J Neuroendocrinol
.
2012
Jun
;
24
(
6
):
874
86
.
[PubMed]
0953-8194
31.
Kenkel
WM
,
Suboc
G
,
Carter
CS
.
Autonomic, behavioral and neuroendocrine correlates of paternal behavior in male prairie voles
.
Physiol Behav
.
2014
Apr
;
128
:
252
9
.
[PubMed]
0031-9384
32.
Okabe
S
,
Tsuneoka
Y
,
Takahashi
A
,
Ooyama
R
,
Watarai
A
,
Maeda
S
, et al
Pup exposure facilitates retrieving behavior via the oxytocin neural system in female mice
.
Psychoneuroendocrinology
.
2017
May
;
79
:
20
30
.
[PubMed]
0306-4530
33.
Sabihi
S
,
Dong
SM
,
Durosko
NE
,
Leuner
B
.
Oxytocin in the medial prefrontal cortex regulates maternal care, maternal aggression and anxiety during the postpartum period
.
Front Behav Neurosci
.
2014
Aug
;
8
:
258
.
[PubMed]
1662-5153
34.
Champagne
F
,
Diorio
J
,
Sharma
S
,
Meaney
MJ
.
Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors
.
Proc Natl Acad Sci USA
.
2001
Oct
;
98
(
22
):
12736
41
.
[PubMed]
0027-8424
35.
Numan
M
,
Stolzenberg
DS
.
Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats
.
Front Neuroendocrinol
.
2009
Jan
;
30
(
1
):
46
64
.
[PubMed]
0091-3022
36.
Li
Y
,
Lian
Z
,
Wang
B
,
Tai
F
,
Wu
R
,
Hao
P
, et al
Natural variation in paternal behavior is associated with central estrogen receptor alpha and oxytocin levels
.
J Comp Physiol A Neuroethol Sens Neural Behav Physiol
.
2015
Mar
;
201
(
3
):
285
93
.
[PubMed]
0340-7594
37.
Martínez
A
,
Arteaga-Silva
M
,
Bonilla-Jaime
H
,
Cárdenas
M
,
Rojas-Castañeda
J
,
Vigueras-Villaseñor
R
, et al;
Martínez
.
Arteaga-Silva M, Bonilla-Jaime H, Cárdenas M, Rojas-Castañeda J, Vigueras-Villaseñor R, Limón-Morales O, Luis J: paternal behavior in the Mongolian gerbil, and its regulation by social factors, T, ERα, and AR
.
Physiol Behav
.
2019
;
199
:
351
8
. 0031-9384
38.
Rodgers
AB
,
Morgan
CP
,
Bronson
SL
,
Revello
S
,
Bale
TL
.
Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation
.
J Neurosci
.
2013
May
;
33
(
21
):
9003
12
.
[PubMed]
0270-6474
39.
Maniam
J
,
Antoniadis
C
,
Morris
MJ
.
Early-Life Stress, HPA Axis Adaptation, and Mechanisms Contributing to Later Health Outcomes
.
Front Endocrinol (Lausanne)
.
2014
May
;
5
:
73
.
[PubMed]
1664-2392
40.
Young
LJ
,
Wang
Z
.
The neurobiology of pair bonding
.
Nat Neurosci
.
2004
Oct
;
7
(
10
):
1048
54
.
[PubMed]
1097-6256
41.
Freeman
SM
,
Young
LJ
.
Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: translational Implications
.
J Neuroendocrinol
.
2016
Apr
;
28
(
4
):
28
.
[PubMed]
0953-8194
42.
Yuan
W
,
Yang
XP
,
Yu
P
,
Jia
R
,
Tai
FD
,
Wei
B
, et al
Different behavioral, neural and neuropeptide responses of fathers to their own and to alien pups in mandarin voles
.
J Comp Physiol A Neuroethol Sens Neural Behav Physiol
.
2018
Mar
;
204
(
3
):
257
69
.
[PubMed]
0340-7594
43.
Wang
B
,
Wang
L
,
Wang
K
,
Tai
F
.
The effects of fathering experience on paternal behaviors and levels of central expression of oxytocin and dopamine-2 type receptors in mandarin voles
.
Physiol Behav
.
2018
Sep
;
193
Pt A
:
35
42
.
[PubMed]
0031-9384
44.
Aragona
BJ
,
Liu
Y
,
Curtis
JT
,
Stephan
FK
,
Wang
Z
.
A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles
.
J Neurosci
.
2003
Apr
;
23
(
8
):
3483
90
.
[PubMed]
0270-6474
45.
Aragona
BJ
,
Liu
Y
,
Yu
YJ
,
Curtis
JT
,
Detwiler
JM
,
Insel
TR
, et al
Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds
.
Nat Neurosci
.
2006
Jan
;
9
(
1
):
133
9
.
[PubMed]
1097-6256
46.
Newman
SW
.
The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network
.
Ann N Y Acad Sci
.
1999
Jun
;
877
1 ADVANCING FRO
:
242
57
.
[PubMed]
0077-8923
47.
Duvarci
S
,
Pare
D
.
Amygdala microcircuits controlling learned fear
.
Neuron
.
2014
Jun
;
82
(
5
):
966
80
.
[PubMed]
0896-6273
48.
Lehman
MN
,
Winans
SS
,
Powers
JB
.
Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior
.
Science
.
1980
Oct
;
210
(
4469
):
557
60
.
[PubMed]
0036-8075
49.
Paré
D
,
Quirk
GJ
,
Ledoux
JE
.
New vistas on amygdala networks in conditioned fear
.
J Neurophysiol
.
2004
Jul
;
92
(
1
):
1
9
.
[PubMed]
0022-3077
50.
Fleming
AS
,
Vaccarino
F
,
Luebke
C
.
Amygdaloid inhibition of maternal behavior in the nulliparous female rat
.
Physiol Behav
.
1980
Nov
;
25
(
5
):
731
43
.
[PubMed]
0031-9384
51.
Numan
M
,
Numan
MJ
,
English
JB
.
Excitotoxic amino acid injections into the medial amygdala facilitate maternal behavior in virgin female rats
.
Horm Behav
.
1993
Mar
;
27
(
1
):
56
81
.
[PubMed]
0018-506X
52.
Tai
F
,
Wang
T
,
Zhao
Y
.
Mating system of mandarin vole (Microtus mandarinus)
.
Shou Lei Xue Bao
.
2001
;
47
:
266
73
.1000-1050
53.
Tai
F
,
Wang
T
.
Social organization of mandarin voles in burrow system
.
Shou Lei Xue Bao
.
2001
;
21
:
50
6
.1000-1050
54.
de Jong
TR
,
Measor
KR
,
Chauke
M
,
Harris
BN
,
Saltzman
W
.
Brief pup exposure induces Fos expression in the lateral habenula and serotonergic caudal dorsal raphe nucleus of paternally experienced male California mice (Peromyscus californicus)
.
Neuroscience
.
2010
Sep
;
169
(
3
):
1094
104
.
[PubMed]
0306-4522
55.
Wang
B
,
Li
Y
,
Wu
R
,
Zhang
S
,
Tai
F
.
Behavioral responses to pups in males with different reproductive experiences are associated with changes in central OT, TH and OTR, D1R, D2R mRNA expression in mandarin voles
.
Horm Behav
.
2015
Jan
;
67
:
73
82
.
[PubMed]
0018-506X
56.
Lambert
KG
,
Franssen
CL
,
Hampton
JE
,
Rzucidlo
AM
,
Hyer
MM
,
True
M
, et al
Modeling paternal attentiveness: distressed pups evoke differential neurobiological and behavioral responses in paternal and nonpaternal mice
.
Neuroscience
.
2013
Mar
;
234
:
1
12
.
[PubMed]
0306-4522
57.
Blumstein
DT
,
Daniel
JC
:
Quantifying behavior the JWatcher way.
2007
58.
Paxinos
G
,
Franklin
KB
.
The Mouse Brain in Stereotaxic Coordintes
.
Academic Press
;
2001
.
59.
Priego
T
,
Sánchez
J
,
Picó
C
,
Palou
A
.
Sex-differential expression of metabolism-related genes in response to a high-fat diet
.
Obesity (Silver Spring)
.
2008
Apr
;
16
(
4
):
819
26
.
[PubMed]
1930-7381
60.
Pfaffl
MW
.
A new mathematical model for relative quantification in real-time RT-PCR
.
Nucleic Acids Res
.
2001
May
;
29
(
9
):
e45
.
[PubMed]
0305-1048
61.
Sarkadi
A
,
Kristiansson
R
,
Oberklaid
F
,
Bremberg
S
.
Fathers’ involvement and children’s developmental outcomes: a systematic review of longitudinal studies
.
Acta Paediatr
.
2008
Feb
;
97
(
2
):
153
8
.
[PubMed]
0803-5253
62.
Côté
SM
,
Vaillancourt
T
,
Barker
ED
,
Nagin
D
,
Tremblay
RE
.
The joint development of physical and indirect aggression: predictors of continuity and change during childhood
.
Dev Psychopathol
.
2007
;
19
(
1
):
37
55
.
[PubMed]
0954-5794
63.
Champagne
FA
,
Curley
JP
.
How social experiences influence the brain
.
Curr Opin Neurobiol
.
2005
Dec
;
15
(
6
):
704
9
.
[PubMed]
0959-4388
64.
Veenema
AH
,
Neumann
ID
.
Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats
.
Psychoneuroendocrinology
.
2009
Apr
;
34
(
3
):
463
7
.
[PubMed]
0306-4530
65.
He
Z
,
Guo
Q
,
Yang
Y
,
Wang
L
,
Zhang
S
,
Yuan
W
, et al
Pre-weaning paternal deprivation impairs social recognition and alters hippocampal neurogenesis and spine density in adult mandarin voles
.
Neurobiol Learn Mem
.
2018
Nov
;
155
:
452
62
.
[PubMed]
1074-7427
66.
Hulshof
HJ
,
Novati
A
,
Sgoifo
A
,
Luiten
PG
,
den Boer
JA
,
Meerlo
P
.
Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effect on stress sensitivity and anxiety in adult Wistar rats
.
Behav Brain Res
.
2011
Jan
;
216
(
2
):
552
60
.
[PubMed]
0166-4328
67.
Feldman
R
,
Zagoory-Sharon
O
,
Weisman
O
,
Schneiderman
I
,
Gordon
I
,
Maoz
R
, et al
Sensitive parenting is associated with plasma oxytocin and polymorphisms in the OXTR and CD38 genes
.
Biol Psychiatry
.
2012
Aug
;
72
(
3
):
175
81
.
[PubMed]
0006-3223
68.
Taylor
JH
,
French
JA
.
Oxytocin and vasopressin enhance responsiveness to infant stimuli in adult marmosets
.
Horm Behav
.
2015
Sep
;
75
:
154
9
.
[PubMed]
0018-506X
69.
Wu
R
,
Song
Z
,
Wang
S
,
Shui
L
,
Tai
F
,
Qiao
X
, et al
Early paternal deprivation alters levels of hippocampal brain-derived neurotrophic factor and glucocorticoid receptor and serum corticosterone and adrenocorticotropin in a sex-specific way in socially monogamous mandarin voles
.
Neuroendocrinology
.
2014
;
100
(
2-3
):
119
28
.
[PubMed]
0028-3835
70.
Bosch
OJ
,
Neumann
ID
.
Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action
.
Horm Behav
.
2012
Mar
;
61
(
3
):
293
303
.
[PubMed]
0018-506X
71.
Ross
HE
,
Young
LJ
.
Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior
.
Front Neuroendocrinol
.
2009
Oct
;
30
(
4
):
534
47
.
[PubMed]
0091-3022
72.
Donaldson
ZR
,
Young
LJ
.
Oxytocin, vasopressin, and the neurogenetics of sociality
.
Science
.
2008
Nov
;
322
(
5903
):
900
4
.
[PubMed]
0036-8075
73.
Gimpl
G
,
Fahrenholz
F
.
The oxytocin receptor system: structure, function, and regulation
.
Physiol Rev
.
2001
Apr
;
81
(
2
):
629
83
.
[PubMed]
0031-9333
74.
Numan
M
.
Medial preoptic area and maternal behavior in the female rat
.
J Comp Physiol Psychol
.
1974
Oct
;
87
(
4
):
746
59
.
[PubMed]
0021-9940
75.
Olazábal
DE
.
Comparative analysis of oxytocin receptor density in the nucleus accumbens: an adaptation for female and male alloparental care?
J Physiol Paris
.
2014
Apr-Jun
;
108
(
2-3
):
213
20
.
[PubMed]
0928-4257
76.
Keebaugh
AC
,
Barrett
CE
,
Laprairie
JL
,
Jenkins
JJ
,
Young
LJ
.
RNAi knockdown of oxytocin receptor in the nucleus accumbens inhibits social attachment and parental care in monogamous female prairie voles
.
Soc Neurosci
.
2015
;
10
(
5
):
561
70
.
[PubMed]
1747-0919
77.
Lee
AW
,
Brown
RE
.
Medial preoptic lesions disrupt parental behavior in both male and female California mice (Peromyscus californicus)
.
Behav Neurosci
.
2002
Dec
;
116
(
6
):
968
75
.
[PubMed]
0735-7044
78.
Wang
Z
,
Yu
G
,
Cascio
C
,
Liu
Y
,
Gingrich
B
,
Insel
TR
.
Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles (Microtus ochrogaster): a mechanism for pair bonding?
Behav Neurosci
.
1999
Jun
;
113
(
3
):
602
11
.
[PubMed]
0735-7044
79.
Stolzenberg
DS
,
Zhang
KY
,
Luskin
K
,
Ranker
L
,
Bress
J
,
Numan
M
.
Dopamine D(1) receptor activation of adenylyl cyclase, not phospholipase C, in the nucleus accumbens promotes maternal behavior onset in rats
.
Horm Behav
.
2010
Jan
;
57
(
1
):
96
104
.
[PubMed]
0018-506X
80.
Baskerville
TA
,
Douglas
AJ
.
Dopamine and oxytocin interactions underlying behaviors: potential contributions to behavioral disorders
.
CNS Neurosci Ther
.
2010
Jun
;
16
(
3
):
e92
123
.
[PubMed]
1755-5930
81.
Nie
L
,
Di
T
,
Li
Y
,
Cheng
P
,
Li
M
,
Gao
J
.
Blockade of serotonin 5-HT2A receptors potentiates dopamine D2 activation-induced disruption of pup retrieval on an elevated plus maze, but has no effect on D2 blockade-induced one
.
Pharmacol Biochem Behav
.
2018
Aug
;
171
:
74
84
.
[PubMed]
0091-3057
82.
Tseng
KY
,
O’Donnell
P
.
Dopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms
.
J Neurosci
.
2004
Jun
;
24
(
22
):
5131
9
.
[PubMed]
0270-6474
83.
Floresco
SB
.
Prefrontal dopamine and behavioral flexibility: shifting from an “inverted-U” toward a family of functions
.
Front Neurosci
.
2013
Apr
;
7
:
62
.
[PubMed]
1662-4548
84.
Williams
GV
,
Castner
SA
.
Under the curve: critical issues for elucidating D1 receptor function in working memory
.
Neuroscience
.
2006
Apr
;
139
(
1
):
263
76
.
[PubMed]
0306-4522
85.
Takahashi
H
,
Yamada
M
,
Suhara
T
.
Functional significance of central D1 receptors in cognition: beyond working memory
.
J Cereb Blood Flow Metab
.
2012
Jul
;
32
(
7
):
1248
58
.
[PubMed]
0271-678X
86.
Di Cara
B
,
Panayi
F
,
Gobert
A
,
Dekeyne
A
,
Sicard
D
,
De Groote
L
, et al
Activation of dopamine D1 receptors enhances cholinergic transmission and social cognition: a parallel dialysis and behavioural study in rats
.
Int J Neuropsychopharmacol
.
2007
Jun
;
10
(
3
):
383
99
.
[PubMed]
1461-1457
87.
Loiseau
F
,
Millan
MJ
.
Blockade of dopamine D(3) receptors in frontal cortex, but not in sub-cortical structures, enhances social recognition in rats: similar actions of D(1) receptor agonists, but not of D(2) antagonists
.
Eur Neuropsychopharmacol
.
2009
Jan
;
19
(
1
):
23
33
.
[PubMed]
0924-977X
88.
Han
X
,
Li
N
,
Xue
X
,
Shao
F
,
Wang
W
.
Early social isolation disrupts latent inhibition and increases dopamine D2 receptor expression in the medial prefrontal cortex and nucleus accumbens of adult rats
.
Brain Res
.
2012
Apr
;
1447
:
38
43
.
[PubMed]
0006-8993
89.
Sun
WL
,
Festa
ED
,
Jenab
S
,
Quinones-Jenab
V
: Sex differences in dopamine D2-like receptor-mediated G-protein activation in the medial prefrontal cortex after cocaine. Ethn Dis
2010
;20:S1-88-91.
90.
Fodor
A
,
Barsvari
B
,
Aliczki
M
,
Balogh
Z
,
Zelena
D
,
Goldberg
SR
, et al
The effects of vasopressin deficiency on aggression and impulsiveness in male and female rats
.
Psychoneuroendocrinology
.
2014
Sep
;
47
:
141
50
.
[PubMed]
0306-4530
91.
Bielsky
IF
,
Hu
SB
,
Szegda
KL
,
Westphal
H
,
Young
LJ
.
Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice
.
Neuropsychopharmacology
.
2004
Mar
;
29
(
3
):
483
93
.
[PubMed]
0893-133X
92.
Bayerl
DS
,
Hönig
JN
,
Bosch
OJ
.
Vasopressin V1a, but not V1b, receptors within the PVN of lactating rats mediate maternal care and anxiety-related behaviour
.
Behav Brain Res
.
2016
May
;
305
:
18
22
.
[PubMed]
0166-4328
93.
Bamshad
M
,
Novak
MA
,
De Vries
GJ
.
Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster and meadow voles, Microtus pennsylvanicus
.
J Neuroendocrinol
.
1993
Jun
;
5
(
3
):
247
55
.
[PubMed]
0953-8194
94.
Freeman
SM
,
Inoue
K
,
Smith
AL
,
Goodman
MM
,
Young
LJ
.
The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta)
.
Psychoneuroendocrinology
.
2014
Jul
;
45
:
128
41
.
[PubMed]
0306-4530
95.
Yohn
CN
,
Leithead
AB
,
Becker
EA
.
Increased vasopressin expression in the BNST accompanies paternally induced territoriality in male and female California mouse offspring
.
Horm Behav
.
2017
Jul
;
93
:
9
17
.
[PubMed]
0018-506X
96.
Paul
MJ
,
Terranova
JI
,
Probst
CK
,
Murray
EK
,
Ismail
NI
,
de Vries
GJ
.
Sexually dimorphic role for vasopressin in the development of social play
.
Front Behav Neurosci
.
2014
Feb
;
8
:
58
.
[PubMed]
1662-5153
97.
Bosch
OJ
.
Maternal aggression in rodents: brain oxytocin and vasopressin mediate pup defence
.
Philos Trans R Soc Lond B Biol Sci
.
2013
Oct
;
368
(
1631
):
20130085
.
[PubMed]
0962-8436
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