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Brain plasticity in pregnancy and the postpartum period: links to maternal caregiving and mental health

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Abstract

Pregnancy and the postpartum period involve numerous physiological adaptations that enable the development and survival of the offspring. A distinct neural plasticity characterizes the female brain during this period, and dynamic structural and functional changes take place that accompany fundamental behavioral adaptations, stimulating the female to progress from an individual with self-directed needs to being responsible for the care of another life. While many animal studies detail these modifications, an emerging body of research reveals the existence of reproduction-related brain plasticity in human mothers too. Additionally, associations with aspects of maternal caregiving point to adaptive changes that benefit a woman's transition to motherhood. However, the dynamic changes that affect a woman's brain are not merely adaptive, and they likely confer a vulnerability for the development of mental disorders. Here, we review the changes in brain structure and function that a woman undergoes during the peripartum period, outlining associations between these neural alterations and different aspects of maternal care. We additionally discuss peripartum mood disorders and postpartum psychosis, and review the neuroimaging studies that investigate the neural bases of these conditions.
ORIGINAL ARTICLE
Brain plasticity in pregnancy and the postpartum period: links
to maternal caregiving and mental health
Erika Barba-Müller
1,2,3
&Sinéad Craddock
1,2
&Susanna Carmona
4,5,6
&Elseline Hoekzema
1,2
Received: 26 March 2018 / Accepted: 2 July 2018 / Published online: 14 July 2018
#The Author(s) 2018
Abstract
Pregnancy and the postpartum period involve numerous physiological adaptations that enable the development and
survival of the offspring. A distinct neural plasticity characterizes the female brain during this period, and dynamic
structural and functional changes take place that accompany fundamental behavioral adaptations, stimulating the female
to progress from an individual with self-directed needs to being responsible for the care of another life. While many
animal studies detail these modifications, an emerging body of research reveals the existence of reproduction-related
brain plasticity in human mothers too. Additionally, associations with aspects of maternal caregiving point to adaptive
changes that benefit a womans transition to motherhood. However, the dynamic changes that affect a womansbrainare
not merely adaptive, and they likely confer a vulnerability for the development of mental disorders. Here, we review the
changes in brain structure and function that a woman undergoes during the peripartum period, outlining associations
between these neural alterations and different aspects of maternal care. We additionally discuss peripartum mood
disorders and postpartum psychosis, and review the neuroimaging studies that investigate the neural bases of these
conditions.
Keywords Neuroplasticity .Perinatal mental health .Maternal behavior .Postpartum depression .Maternal attachment
Introduction
Becoming a mother brings about profound changes in the
female mammalian brain. Evidence from across the animal
kingdom indicates numerous functional and structural ad-
aptations in the female brain throughout pregnancy and the
postpartum period, which are driven by an interplay be-
tween endocrine and environmental factors (Brunton and
Russell 2008; Hillerer et al. 2014a;Kohletal.2016).
These reproduction-related changes take place in brain
structures that regulate maternal caregiving behaviors such
as licking and grooming of the young, with the medial
preoptic area (mPOA) as a core node in the induction of
these behaviors (Keyser-Marcus et al. 2001;Numan2007),
but they also occur in structures that are not directly asso-
ciated with this behavioral repertoire of caregiving activi-
ties, such as the hippocampal complex (Pawluski et al.
2016). At the cellular level, the events that take place are
also wide-ranging, including various forms of neural plas-
ticity such as neurogenesis, synaptic remodeling and
changes (increases and/or decreases) in dendritic mor-
phometry, spine density, and astrocytic density (Kinsley
et al. 2006; Leuner and Sabihi 2016; Salmaso et al.
2009). The resulting maternal network comprises multiple
cortical, limbic, and sensory systems that interact to sup-
port various forms of maternal behavior. Interestingly,
This article is part of the Topical Collection on Neurobiology of Maternal
Mental Illness
Guest Editor: Jodi Pawluski
*Elseline Hoekzema
e.a.hoekzema@fsw.leidenuniv.nl
1
Brain and Development Research Center, Leiden University,
Leiden, the Netherlands
2
Leiden Institute for Brain and Cognition, Leiden, the Netherlands
3
University Institute of Mental Health Vidal i Barraquer, Ramon Llull
University, Barcelona, Spain
4
Centro de Investigación Biomédica en Red de Salud Mental
(CIBERSAM), Madrid, Spain
5
Unidad de Medicina y Cirugía Experimental, Instituto de
Investigación Sanitaria Gregorio Marañón, Madrid, Spain
6
Faculty of Health Sciences, Universitat Oberta de Catalunya,
Barcelona, Spain
Archives of Women's Mental Health (2019) 22:289299
https://doi.org/10.1007/s00737-018-0889-z
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many of the regions of the maternal circuitry are rich in
receptors for oxytocina neuropeptide that plays a key
role in bondingand are considered central nodes of the
mammalian social behavior network (Kohl and Dulac
2018;Newman1999).
It is interesting to note that some of these structural
brain changes were replicated in virgin female rodents after
a hormonal treatment mimicking pregnancy based on ex-
ogenous steroid hormones, stressing the implication of the
hormonal surges of pregnancy in the observed gestational
brain changes (Keyser-Marcus et al. 2001; Kinsley et al.
2006). This is unsurprising, since sex steroid hormones are
powerful neurotrophic agents that regulate most major de-
velopmental events (Simerly 2002). Other hormones such
as prolactin, oxytocin, and glucocorticoids have also been
showntoplayakeyroleinshapingoractivatingthema-
ternal brain (Kim and Strathearn 2016;Slatteryand
Hillerer 2016). For instance, in pregnant mice, increases
in prolactin mediate the production of neural progenitors
in the forebrain subventricular zone, which later migrate to
produce new olfactory interneurons, likely facilitating the
recognition and rearing of the offspring (Shingo et al.
2003). Once endocrine factors have triggered the neural
circuits regulating maternal behavior, this behavior is
maintained by experiential factors, i.e., by exposure to off-
spring cues (Numan 2007).
Research investigating the human brain in relation to
pregnancy and the postpartum period pales in comparison
to animal research in this domain. However, emerging
magnetic resonance imaging (MRI) studies indicate that
the human brain also undergoes dramatic changes during
pregnancy and the postpartum period. Here, we review the
structural and functional brain changes that take place dur-
ing the gestational and postpartum period in women. First,
we review the very scarce research detailing changes in a
womans brain structure, proceeding to a more extensive
discussion of the studies investigating brain function in the
peripartum period. Furthermore, throughout these sections,
we highlight findings that link this neuroplasticity to as-
pects of maternal caregiving. Finally, we introduce the
main peripartum mental disorders, by briefly describing
the symptoms, incidence rates, and principal risk factors
associated with these conditions, followed by a discussion
of the neuroimaging findings that shed light on the neuro-
biology of these debilitating disorders.
Structural brain plasticity
Like other mammals, a woman experiences unparalleled
surges of sex steroid hormones during pregnancy (Casey
et al. 1993) and some authors have suggested the existence
of a structural brain plasticity inherent and specific to
human reproduction itself (Brunton and Russell 2008;
Kinsley and Amory-Meyer 2011;Swainetal.2014).
While this topic has scarcely been investigated, a few stud-
ies point to the occurrence of dynamic peripartum changes
in a womans brain structure. For instance, it was recently
found that first-time mothers undergo a symmetrical pat-
tern of extensive gray matter (GM) volume reductions
across pregnancy, primarily affecting the anterior and pos-
terior cortical midline and specific sections of the bilateral
lateral prefrontal and temporal cortex, which last for at
least 2 years postpartum (Hoekzema et al. 2017). The af-
fected areas were found to significantly overlap with the
Theory of Mind (ToM) network and with brain activations
in response to own-baby stimuli in the postpartum period.
It is noteworthy that these changes consist exclusively of
volume reductions and no increases were detected.
Accordingly, other studies have found a decrease in overall
brain size related to pregnancy in humans (Oatridge et al.
2002) and rodents (Hillerer et al. 2014b). Moreover, GM
volume reductions have been observed in response to in-
creases in endogenous or exogenous sex steroid hormones
outside of pregnancy, for instance during adolescence
(Peper et al. 2011) or hormonal treatment in gender dys-
phoric individuals (Zubiaurre-Elorza et al. 2014), which
supports the notion that hormones are the main mediators
of the morphometric brain changes that accompany
gestation.
Furthermore, there are indications that brain structure con-
tinues to develop in the postpartum period. Based on findings
from animal studies, we can speculate that, while hormonal
factors are paramount in driving neural adaptations during
pregnancy, direct interactions with the baby play a key role
in further postpartum brain changes. Infantsneeds are always
evolving throughout development and parents intuitively
adapt to those changes, incorporating new knowledge, abili-
ties and skills in their parental repertoire. This results in a
neural reorganization referred to as experience-dependent
plasticity (Nithianantharajah and Hannan 2006).
Kim et al. (2010) assessed morphological changes of the
mothers brain during the postpartum period. Results revealed
that from time 1 (24 weeks postpartum) to time 2 (3
4 months postpartum) mothers showed increases in GM vol-
ume in sections of the parietal lobe, prefrontal cortex, and
midbrain. In contrast to the observed structural brain changes
across pregnancy, no GM decreases were detected in the early
postpartum period. Although it is difficult to directly compare
these findings due to differences in study parameters (e.g.,
time period between scans, statistical thresholds, the number
of participants, and morphometric procedures), these findings
suggest that pregnancy and motherhood exert divergent
even opposingeffects on parts of a womans brain in terms
of the direction of GM volume change. While these findings
mostly concern distinct sections of the brainpotentially
290 E. Barba-Müller et al.
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reflecting a region-dependent sensitivity to reproduction-
related endocrine versus experiential factorsthere is some
overlap in the involved anatomical areas as well. These areas
of overlap primarily concern clusters located along the mid-
line of the brain, which were found to undergo increases dur-
ing the early postpartum period as well as volume losses
across pregnancy that remained stable for at least 2 years post-
partum. This might seem contradictory but could reflect, for
instance, a partial volume recovery within these regions fol-
lowing the strong volume reductions of pregnancy that had
already (partially) occurred prior to the post-pregnancy fol-
low-up scan.
Interestingly, a positive perception of the baby predicted
greater GM augmentations in the hypothalamus, substantia
nigra, and amygdala in the mothersbrains (Kim et al.
2010), pointing to a relation between the changes in maternal
brain structure and a mothers response to her baby.
Furthermore, there are indications that changes in a womans
brain structure across pregnancy are also linked to aspects of
maternal caregiving, that is, to the development of maternal
attachment. The brain changes that occur during pregnancy
were found to significantly predict the quality of mother-to-
infant attachment and the absence of hostility towards her
newborn (Hoekzema et al. 2017).
While more research on this topic is needed, these studies
assessing morphometric changes draw a first impression of
certainprimarily socialbrain areas that undergo decreases
in GM volume driven by hormone-derived plasticity in preg-
nancy, followed by GM volume increasesprimarily in net-
works involved in motivation, somatosensory information and
executive functionsmediated by experience-dependent
plasticity during the postpartum period. Furthermore, there
are indications that both gestational and postpartum changes
in brain structure are linked to aspects of maternal caregiving,
providing preliminary evidence for an adaptive purpose serv-
ing a womans transition to motherhood. Future longitudinal
studies collecting hormonal samples and detailed measures of
environmental changes during pregnancy and the postpartum
period are necessary to elucidate the mediators contributing to
the brain plasticity inherent to reproduction and to better track
the structural changes in a womans brain across this dynamic
period.
Functional brain plasticity
In contrast to the few studies examining structural brain
changes in human mothers, there are several studies that as-
sess brain activity in response to own-infant stimuli in com-
parison to other-infant stimuli using functional magnetic res-
onance imaging (fMRI) in the postpartum period. These stud-
ies allow us to identify regions of the brain involved in moth-
erhood by measuring activity in the mothersbrains in
response to their babiesauditory or visual stimuli. Taken
together, they contribute to our understanding of the neural
substrates that underlie the expression of maternal behavior
(Barrett and Fleming 2011; Kim et al. 2016;Moses-Kolkoet
al. 2014; Noriuchi et al. 2008; Swain et al. 2014; Young et al.
2017).
While numerous brain regions have been observed and
paradigms often differ across laboratories, certain networks
have been replicated acrossvarious studies that are considered
part of the maternal brain. These networks are not completely
independent, they share common brain regions and can be co-
activated.
When mothers are presented with stimuli of their own
child, areas of the reward system become activated. This is
unsurprising, since seeing a loved one is a rewarding experi-
ence, which is even stronger during early motherhood, when
her baby becomes a mothers most powerful appetitive stim-
ulus. Studies in female rodents show that mothers eagerly bar-
press for contact with pups (Lee et al. 2000) and find pup
suckling more rewarding than cocaine (Ferris 2005).
Therefore, this dopaminergic and oxytocinergic neuroendo-
crine system is also called the maternal motivation system,
which has been defined by animal studies. The core regions
of the maternal motivational system comprise the mPOA and
the bed nucleus of the stria terminalis, which project to the
ventral tegmental area and the retrorubral field and activate the
reward circuit by releasing dopamine into the nucleus accum-
bens (Numan 2007). In addition to the mesolimbic reward
pathway connecting the ventral tegmental area and nucleus
accumbens, many other subcortical and cortical structures
contribute to the processing of rewarding experiences,
forming a complex network that interfaces with cognitive
functions to affect motor planning, like the dorsal striatum,
substantia nigra, amygdala, hippocampus, and various pre-
frontal areas (Berridge and Kringelbach 2015; Haber and
Knutson 2010). In human mothers, many of these brain re-
gions have been observed to respond strongly when presented
with cues of their infants (Bartels and Zeki 2004; Lorberbaum
et al. 2002; Noriuchi et al. 2008), even more so if the baby is
smiling (Strathearn et al. 2008).
Another conclusion from fMRI studies on the human
maternal brain is the implication of two networks that are
frequently co-activated: the salience network and the emo-
tion regulation network (Seeley et al. 2007). The salience
network is activated in response to the most relevant stim-
uli resulting in a state of alert being fundamental, among
others, for threat detection. Maternal concerns focus on the
well-being of the infant where vigilant protectiveness and
harm-avoidant behaviors are essential. This network is
built around paralimbic structuresparticularly the dorsal
anterior cingulate and orbital frontoinsular corticesand
has a strong connectivity to subcortical and limbic struc-
tures (Seeley et al. 2007). With regard to the emotion
Brain plasticity in pregnancy and the postpartum period: links to maternal caregiving and mental health 291
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regulation network, a common challenge for parents is to
preserve their own regulated emotional state in front of
threats or while caring for their immature and deregulated
child. Children often arouse many emotions, since they
express their own emotions intensely and without control.
The mother, in order to help her infant to integrate his/her
emotional experience, must first effectively regulate her
own emotional arousal and coordinate it with thoughts,
actions, and interactions (Rutherford et al. 2015). In doing
so, prefrontal and cingulate control systems modulate ac-
tivity in emotion systems (Ochsner et al. 2012; Rutherford
et al. 2015). During fMRI tasks, these networks are active
in front of own-baby versus other-baby stimuli (Leibenluft
et al. 2004), particularly if the stimuli presents a negative
emotional cue, such as cries or distress (Lorberbaum et al.
2002;Noriuchietal.2008;Swainetal.2008).
Furthermore, fMRI studies that employ own-children cries
positively correlate a greater activity in frontal regions to a
better quality of attachment (Laurent and Ablow 2012a)
and to more sensitive behaviors with their infant (Musser
et al. 2012), and reduced activation in the anterior cingu-
late cortex and medial prefrontal cortex have been associ-
ated with greater cortisol reactivity to stress in primiparous
women (Laurent et al. 2011).
fMRI studies also strongly converge on the observation
that new mothers exhibit an activation of the empathy and
ToM net w orks (Gingnell et al. 2015; Leibenluft et al. 2004;
Lenzi et al. 2009). These networks, which are specialized in
social cognitive processing, encompass regions of the reward,
salience, and emotion regulation network. The anterior insula
and middle anterior cingulate cortex play a fundamental role
in empathy (Lamm et al. 2011), the capacity of sharing an-
others emotional state while being conscious that the other is
the source of that emotion (Kanske et al. 2015). ToM, often
also called Bmentalizing^or Bsocial intelligence,^is based on
the assumption that we possess a theory of mind that allows us
to have a reflective function concerning our mental states and
to attribute mental states to others, accepting that others can
have perspectives, beliefs, desires, and intentions different
from ones own (Premack and Woodruff 1978; Schaafsma et
al. 2015). The neural network underlying ToM includes mid-
line areas (medial prefrontal cortex, precuneus, and posterior
cingulate cortex) anterior temporal lobes, temporo-parietal
junction, and the inferior frontal gyri (Schurz et al. 2014).
Through empathy and perspective taking, the mother can
Bfeel^and infer what her baby, incapable to speak, is
experiencing and can consequently offer accurate care.
Interestingly, using quantitative analyses of overlap,
Hoekzema et al. (2017) confirmed a remarkable similarity
between the structural changes of pregnancy and the ToM
network, and found that only networks recruited by ToM tasks
displayed a greater-than-random overlap with the observed
morphological brain changes. Furthermore, it was observed
that the neural response of mothers to visual cues of their
babies corresponded to various regions that lost GM volume
across pregnancy, supporting the notion of a specialization of
the brainmore specifically, in the neural network subserving
social cognitionthat plays a role in a mothersresponseto
her infant (Hoekzema et al. 2017).
A meta-analysis has integrated the results of eight fMRI
studies assessing mothers while processing own versus un-
known infant stimuli (a total of 144 mothers, 27 with depres-
sive symptoms or a personality disorder) (Rocchetti et al.
2014). The results of this meta-analysis showed a greater ac-
tivation in the bilateral insula extending to the inferior frontal
gyrus, basal ganglia, and thalamus, confirming the implication
of these regions in the maternal circuitry.
A few recent studies show that the neurobiology of moth-
erhood represents a dynamic process: a longitudinal fMRI
study examining mothers in the early postpartum period
(within 48 h) and 1 month later using an emotional face-
matching task, showed that the reactivity in the insula, middle
frontal gyrus, and inferior frontal gyrus had incremented, sug-
gesting that the neurobiology of motherhood continues to
change throughout the postpartum period, perhaps in order
to follow the constant development of the offspring
(Gingnell et al. 2015). Parsons et al. (2017) revealed that as
the child grows, the mother shows greater activity in response
to general infant cues in key regions linked to caregiving,
more specifically in the amygdala and orbitofrontal cortex,
implicated in parental vigilance and the appraisal of
emotional expressions. In other words, a lengthier maternal
experience is associated with heightened, differential brain
reactivity that reflects a buildup of these capacities over
time. Montirosso et al. (2017) showed that giving birth to a
preterm baby that needs neonatal intensive care is accompa-
nied by a differential pattern of activity in areas subserving
emotion regulation and social cognition (a greater activation
in inferior frontal gyrus, supramarginal gyrus, and insula),
reflecting that the neurobiology of motherhood is dynamic
not only regarding the passage of time but also depending
on the environmental circumstances, facilitating a sensitive
adaptation to the infantsneeds.
Few studies have investigated brain activity during preg-
nancy, but they all indicate changes in the recruitment of neu-
ral resources in order to facilitate the processing of social
information: Raz (2014) show changes in the recruitment of
neural resources processing emotional stimuli, and Roos et al.
(2011) found that PFC activation in front of fear-relevant stim-
uli is associated with increased distress and anxiety, and in-
creased levels of cortisol and testosterone in pregnant but not
in control women. Other studies that do not assess brain ac-
tivity have found enhanced face recognition during pregnancy
particularly for own-race male faces (Anderson and
Rutherford 2011), enhanced ability to encode emotional faces
of threat or harm during late pregnancy (Pearson et al. 2009)
292 E. Barba-Müller et al.
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and an increase in ethnocentrism during the first trimester of
pregnancy (Navarrete et al. 2007). In accordance with these
findings, the notion of gestational adaptations in social cogni-
tion has been proposed from an evolutionary perspective
(Anderson and Rutherford 2012), where enhanced social cog-
nitive abilities and vigilance towards emotional signals would
facilitate efficiently establishing alliances and identifying
threats such as potential infections and aggressions from con-
specifics in order to protect the fetus.
It is worth mentioning that, while pregnancy and the asso-
ciated brain changes may help prepare a female for mother-
hood, this is not a requirement for mothering. For instance,
virgin female rats will start to exhibit maternal behavior to-
wards pups when exposed to pups consistently for a certain
period (Seip and Morrell 2008). Alloparenting can also hap-
pen in females that are taking care of their offspring and adopt
a parental role towards other unrelated infants (Schubert et al.
2009), as well as in males (Stiver and Alonzo 2011), and there
are even cases of interspecies nursing. Among humans, even
if mothers are often the primary caregiver, fathers, grandpar-
ents, other related kin and unrelated professionals can also
take good care of and genuinely attach to a child. Likewise,
the adoption of infants in humans illustrates that mother-child
behavior and attachment can occur successfully without being
preceded by endocrine priming. In fact, foster mothers show
an association between oxytocin levels, caregiving behaviors,
and brain activity in response to cues of the foster child (Bick
et al. 2013); findings that are similar to those observed in
biologically related mothers. Hence, pregnancy-related neuro-
endocrine changes cannot be necessary forneither guaran-
teethe emergence of a dedicated mother taking care of and
having a loving bond with her child.
In conclusion, it has been said that Bit is fortunate for their
survival that babies are so designed by Nature that they be-
guile and enslave mothers^(Bowlby 1958, p. 19). While it is
true that babies are captivating, it appears that Bnature,^in
addition to its charming baby design, also designed the
mothers brain for this evolutionary goal.
Peripartum mental disorders
Given the vast brain plasticity inherent to reproduction itself, it
is unsurprising that the transition to motherhood is a delicate
period accompanied by a higher risk of suffering mental dis-
turbance. At least one in 10 new mothers finds herself with a
surprising difficulty to take care of and enjoy her baby (Fisher
et al. 2012). She may be facing a postpartum disorder which, if
not treated, can have far-reaching consequences for both the
mother and the child (Davalos et al. 2012). The possible se-
verity of such consequences is demonstrated by records from
the UK that indicate suicide as the leading cause of maternal
death (Oates 2003).
Several types of mental problems can occur during the
perinatal period. The most common is postpartum depres-
sion (PPD), with an estimated 1120% of new mothers
suffering from minor and approximately 714% from ma-
jor depression (Almond 2009;Earls2010; Gavin et al.
2005). Symptomatology is dysphoric affect, a disposition
to feel guilty and/or ashamed, and impaired concentration.
Another frequent complication of childbearing is anxiety.
New mothers often experience some apprehension in re-
sponse to childbearing, which is adaptive (Winnicott
1975), but some mothers experience a concern that is ex-
cessive and cannot be controlled, causing levels of distress
and impairment. Anxiety disorders manifest in a wide
range: generalized anxiety disorder, obsessivecompulsive
disorder, panic disorder, and birth-related posttraumatic
stress disorder. In the postpartum, sometimes the severity
and symptoms do not rise to the level of an anxiety disor-
der diagnosis (e.g., hypervigilant concerns and attention
for the baby, extreme lability, constant worry) but never-
theless can cause significant distress and disturb mother-
infant interactions (Anniverno et al. 2013; Ross and
McLean 2006). Rates of postpartum anxiety (PPA) range
from 10 to 17% in primiparous women (Miller et al. 2006,
2013;Pauletal.2013). PPD is frequently comorbid with
PPA (OHara and Wisner 2014;Recketal.2008) and both
mood disorders can also be manifested during pregnancy
with an estimated prevalence of 15.6% (Fisher et al. 2012).
In fact, a recent review estimates that rates of antenatal
depression are higher than in the first year following child-
birth (Underwood et al. 2016) and that both PPD and PPA
are often a continuation of symptomatology already mani-
fested antenatally (Heron et al. 2004).
Puerperal psychosis (PPP) has a low incidence, but evolves
rapidly and can have tragic consequences. Several character-
istics of its diagnosis are debated (Higgins 2012), but based on
psychiatric income rates, it is estimated that the incidence
ranges between 0.89 and 2.6 in 1000 births (VanderKruik et
al. 2017), although others assure that the incidence is consid-
erably higher and that the women who come to be admitted
are only the most serious cases (Lucas 1994; Vesga-López et
al. 2008). Sometimes, the woman already manifested anxiety
or depression during pregnancy, but other times the psychosis
arrives suddenly. The person begins to experience restless-
ness, insomnia, irritability, and, in many cases, euphoria. As
the development is rapid, usually without prodrome, confu-
sional states appear abruptly, where places, people, objects,
and baby are perceived blurry, threatening, or bizarre. They
are accompanied by strange behavior, lability of mood, and
hallucinations and/or delusions about, for instance, the baby
being dead, very sick, deformed, or possessed (Higgins 2012;
Raphael-Leff 2014). There is an increased risk of filicide and
suicide, usually carried out in an unforeseen way and with
little planning (Brockington 2017).
Brain plasticity in pregnancy and the postpartum period: links to maternal caregiving and mental health 293
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As opposed to certain diseases with a clear biologically
defined underlying pathology, peripartum mental disorders
are determined by multiple factors and can therefore not be
fully understood without taking into account multiple biolog-
ical, psychological, and environmental influences, e.g., poor
social support (Collins et al. 2011; Leigh and Milgrom 2008),
stressful life events (Agrati and Lonstein 2016), a history of
mental illness (Fisher et al. 2012), hormonal fluctuations
(Altemus 2010;Seeman1997), and a genetic predisposition
(Agrati and Lonstein 2016; Caspi and Moffitt 2006).
Therefore, eventually, an interdisciplinary approach is re-
quired to fully understand the etiology of peripartum mental
disorders. Neuroscientific progress is considerably contribut-
ing to increasing our understanding of the neural mechanisms
underlying these mental disorders, which is expected to lead
to advances in prevention and treatment strategies.
Brain structure in peripartum mental disorders
The neurobiology of peripartum mental disorders remains to
be defined, but animal studies provide important indications.
In laboratory rodent models, a repeated exposure to stressors,
separation from pups, and the administration of hormones like
glucocorticoids can produce PPD- and PPA-like behaviors.
Furthermore, these models show brain alterations in
neurogenesis and cellular morphology (e.g., reduced spine
density, dendritic length, and branching) within key structures
of the maternal circuitry such as nucleus accumbens, prefron-
tal cortex, bed nucleus of the stria terminalis, midbrain
periaqueductal gray and hippocampus (Pawluski et al. 2017;
Pereira 2016).
Few human studies have assessed structural alterations
in puerperal clinical samples. A recent study utilized dif-
fusion tensor imaging in order to compare white matter
integrity between medication-free mothers with PPD and
healthy control mothers (Silver et al. 2018). Region of
interest analysis detected a white matter abnormality in
the left anterior limb of the internal capsule in PPD, sug-
gesting a disruption of fronto-subcortical circuits. In addi-
tion, correlation analyses relate disrupted interhemispheric
structural connectivity to elevated depression scores
(Silver et al. 2018). It is not clear if this disrupted structural
connectivity represents a structural risk factor for the de-
velopment of peripartum depression or is pathognomonic
of a PPD episode, but interestingly, Young et al. (2017),
based on a review of fMRI studies, conclude that there is
an association between more adaptive maternal behavior
and good regulation across prefrontal and subcortical
regions.
Regarding PPP, a computerized tomography study com-
pared mothers with PPP to patients (with psychoses or
bipolar disorders outside the postpartum period) and con-
trols (Lanczik et al. 1998). PPP mothers showed a volume
enlargement in the left ventricular area, planimetric
ventricular-to-brain ratio, and superior cerebellar cistern.
Another study examined whether mothers who develop a
PPP episode differ in brain cortical volume and morphol-
ogy (Fusté et al. 2017). They compared three groups of
mothers at the postpartum period: 11 mothers at risk that
developed a PPP episode; 15 mothers at risk that did not
develop a PPP episode; and 21 control mothers. Region of
interest analyses showed that mothers with an episode had
less volume in the ACC, left parahippocampal gyrus, and
left superior temporal gyrus in comparison to mothers at
risk without an episode. Subsequent analyses showed that
these differences might be driven by surface area changes
rather than changes in cortical thickness. In addition,
mothers at risk without an episode had larger left superior
and inferior frontal gyrus than the control group, proposing
a different cortical phenotype across the three groups.
Since there were between-group differences in terms of
duration of illness and interval between delivery and the
MRI acquisition, the results should be interpreted with
caution. Nevertheless, they provide information about al-
terations on brain morphology in relation to PPP.
Brain function in peripartum mental disorders
fMRI studies assessing samples with PPD or high levels of
anxiety have identified a different pattern of neural activation
in front of own-infant cry in comparison to control mothers,
suggesting reduced neural sensitivity. For instance, mothers
with PPD have shown weaker activation of reward and moti-
vation areas such as the thalamus, nucleus accumbens, and
caudate and key emotion regulation areas such as the lateral
orbitofrontal cortex (Laurent and Ablow 2012b). Kim et al.
(2015) found that higher levels of anxiety in relation to par-
enting correlated with reduced activation in the substantia
nigra, a region implicated in reward processing.
Results appear to be contradictory in relation to the in-
volvement of the amygdala: Some studies relate a more adap-
tive caregiving behavior to an increased activity while others
relate this to a decreased activity (Barrett et al. 2012;Laurent
and Ablow 2012a; Lenzi et al. 2016; Moses-Kolko et al. 2010;
Wonch et al . 2016). In relation to this, Young et al. (2017)
hypothesize that sensitive maternal care lies on a U-shaped
curve, where both hypo-reactivity and hyper-reactivity to in-
fant cues in the amygdala are problematic. Mothers suffering
from PPD or PPA may fall at either end of this curve and
therefore show disrupted maternal sensitivity.
Resting-state fMRI is another strategy that has been
used to investigate brain activity in peripartum mental dis-
orders. It explores spontaneous neural activity and allows
investigating the so-called Default Mode Network.
Interestingly, this network encompasses internally focused,
self-referential processing (Buckner et al. 2008;Northoff
294 E. Barba-Müller et al.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
et al. 2006;Wickeretal.2003)aswellasToMfunctions
(Mars et al. 2012; Uddin et al. 2007). This analogous in-
volvement of the same midline structures in both self- and
other-referential processing corresponds to the simulation
theory that says that we use our own mental state as a
model for inferring the mental states of others (Goldman
1992) and not by merely simulating being in the others
situation but by simulating Bbeing the other^with his or
her psychological traits (Gordon 1995). ToM, as indicated
above, is fundamental for a mother, since it enables her to
make sense of the observed behavior of her baby. Three
studies have shown abnormal neural activity in
medication-free mothers with PPD when compared to
HCM: Xiao-juan et al. (2011) showed that regional homo-
geneity was significantly increased in the posterior
cingulate and medial frontal and decreased in temporal
gyrus, Deligiannidis et al. (2013) showed that cortico-
cortical and cortico-limbic connectivity was significantly
blunted, and Chase et al. (2014) found a clear disruption of
PCC connectivity with the right amygdala.
Interestingly, when comparing PPD and PPA to the same
symptom profile at other times in life outside the postpartum
period (major depressive disorder (MDD) or general anxiety
disorder (GAD)), some neurobiological distinctions can be
discerned: Pawluski et al. (2017) noted that resting-state ac-
tivity and functional paradigms using emotional cues in indi-
viduals with MMD show a hyperactivity in medial affective
and limbic regions that is not present in women with PPD.
With regard to anxiety symptomatology, subjects with GAD
show a hyperactivity in the amygdala and insula in response to
emotional cues, as well as an increased connectivity between
these two areas. On the other hand, higher anxiety in postpar-
tum women is associated with a lower amygdala response to
emotional non-own-infant cues and lower connectivity be-
tween the amygdala and insula (Pawluski et al. 2017). Better
discerning the distinctions between these disorders occurring
during and outside of the perinatal period is important, not
only for increasing our understanding of the neurobiology of
these disorders but also to aid therapeutic development, since
a different neurobiological profile may require a distinct treat-
ment approach.
In summation, pregnancy and the postpartum period differ
significantly from other times in a womans life in terms of
developing a de novo mental disorder or experiencing a re-
lapse of a pre-existing disorder. The etiology of these disor-
ders is multifactorial, but progress in neurobiological research
is leading to significant clues. Animal models and neuroim-
aging studies in humans are starting to detect abnormalities in
structure, function, and connectivity in brain regions respon-
sible for ToM, self-regulation, and emotion in mothers with
perinatal disorders. Although there are similarities between
mood and psychotic disorders during the peripartum period
and those occurring in other times in life, significant
differences are also starting to emerge (Fusté et al. 2017;
Pawluski et al. 2017), which might eventually lead to im-
provements in the treatment and prevention of these disorders.
Conclusion
A compelling body of evidence in healthy women and other
female mammals confirms that, during pregnancy and the
postpartum period, hormones and sensory interactions with
the offspring relate to complex structural and functional
changes in the brain. This reproduction-related brain plasticity
embraces various areas implicated in maternal caregiving, pri-
marily regions involved in reward/motivation, salience/threat
detection, emotional regulation, and social cognition such as
the ability to empathize and infer the mental state of the baby.
These changes seem necessary and adaptive: since the surviv-
al of the young is dependent on the mothers efforts, her brain
seems to have evolved in ways that promote mother-infant
bonding and sensitive caregiving.
Although this maternal brain plasticity facilitates a higher
purposethe continuation of the speciesit is not necessarily
innocuous and predisposes the mother or mother-to-be to peri-
partum mental disorders. Irrespective of the clinical manifes-
tation of the disturbance, the suffering that accompanies a
peripartum disorder has important implications for the mother,
her partner, and her child. As briefly reviewed here, brain
research is offering growing scientific understanding
concerning the neural correlates of these disorders. Some
structural irregularities and differences in activation patterns
are starting to be identified, which will eventually lead to
improvements in prevention and treatment.
Since pregnancy and the postpartum period signify a period
of particular vulnerability for the mother as well as for the
newbornwho is highly susceptible to his/her mothersdis-
tress or well-beingthe antenatal period can be seen as a
unique opportunity to identify women at risk. Just as we take
care of the womens physical health during gestation and the
peripartum periodwith programmed obstetric visits and
skilled birth attendance, safeguarding many livestaking
care of a womans mental health during this time seems a
promising focus for scientific and clinical investment.
Funding information EH was supported by an Innovational Research
Incentives Scheme Grant (Veni, 451-14-036) and a NARSAD Young
Investigator Grant from the Brain & Behavior Research Foundation,
and SC was supported by a Miguel Servet Type 1 Grant (CP16/00096)
from the Instituto de Salud Carlos III.
Compliance with ethical standards
Conflicts of interest The authors declare that they have no conflicts of
interest.
Brain plasticity in pregnancy and the postpartum period: links to maternal caregiving and mental health 295
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Open Access This article is distributed under the terms of the Creative
Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give appro-
priate credit to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made.
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... Changes include increases in grey matter volume in sections of the midbrain prefrontal cortex, the superior temporal sulcus, medial and inferior frontal cortex, and bilateral prefrontal cortex [59][60][61][62]. These changes are accompanied by emergence of higher levels of hormones related to reward circuitry including oxytocin and estrogen [63][64][65] that serve to increase emotional availability and maternal attachment necessary for responsivity to infant cues [64,66,67]. ...
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Purpose of review To provide a narrative summary of the epidemiology of prenatal cannabis use, the known reasons for use, the effects of in utero cannabis exposure on offspring neurodevelopment and impact on mother-infant attachment. Recent findings Compelling evidence from human imaging studies suggest that in utero cannabis exposure disrupts early brain development and has long-term behavioral consequences for the offspring. Maternal postpartum cannabis use may diminish the maternal-infant bonding process and quality of caregiving. Summary The combination of increasing trends in prenatal cannabis use, low perceived risk, and increasing potency pose a serious challenge for the clinical and public health communities. Additional research is needed to understand the consequences of in utero exposure as well as postnatal maternal impacts that diminish the quality of caregiving. Most importantly, clinical cessation programs are needed to support women who enter pregnancy with cannabis dependency.
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Parenting is a multicomponent social behavior that is essential for the survival of offspring in many species. Despite extensive characterization of individual brain areas involved in parental care, we do not fully understand how discrete aspects of this behavior are orchestrated at the neural circuit level. Recent progress in identifying genetically specified neuronal populations critical for parenting, and the use of genetic and viral tools for circuit-cracking now allow us to deconstruct the underlying circuitry and, thus, to elucidate how different aspects of parental care are controlled. Here we review the latest advances, outline possible organizational principles of parental circuits and discuss future challenges.
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Diffusion tensor imaging (DTI) studies in depression show decreased structural connectivity in the left anterior limb of the internal capsule and the genu of the corpus callosum but no such studies exist in peripartum depression (PPD), which affects 1 in 8 women. We analyzed fractional anisotropy (FA) as a measure of white matter integrity of these two tracts using tract-based spatial statistics (TBSS). We then conducted an exploratory whole-brain analysis to identify additional regions implicated in PPD. Seventy-five pregnant, medication-free women were evaluated with the Edinburgh Postnatal Depression Scale (EPDS) and Structured Clinical Interview (SCID) for DSM-IV-TR in pregnancy and in the postpartum. Structural MRI and DTI sequences were acquired in forty-four women within 2-8 weeks postpartum. TBSS data were analyzed between healthy comparison postpartum women (HCW) and women who developed PPD to determine differences in white matter integrity within the left anterior limb of the internal capsule and the genu of the corpus callosum, then analyzed across participants to explore correlation between FA and the EPDS score. An exploratory whole-brain analysis was also conducted to identify other potential regions showing differences in white matter integrity between groups, as well as correlation between EPDS and FA across groups. All results were corrected for multiple comparisons and analyses conducted using FSL, p < 0.05, K > 10. In comparison to HCW, women with PPD had significantly lower FA in left anterior limb of the internal capsule (p = 0.010). FA was negatively correlated with EPDS scores in the left anterior limb of the internal capsule (p = 0.019). In the whole-brain analysis, FA in the right retrolenticular internal capsule (p = 0.03) and two clusters within the body of the corpus callosum (p = 0.044, p = 0.050) were negatively correlated with EPDS; there were no between-group differences in FA. Reduced FA in the left anterior limb of the internal capsule suggests disruption of fronto-subcortical circuits in PPD. A negative correlation between FA within the body of the corpus callosum and EPDS total score could additionally reflect disrupted interhemispheric structural connectivity in women with depressive symptoms.
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Postpartum psychosis (PP) is the most severe psychiatric disorder associated with childbirth. The risk of PP is very high in women with a history of bipolar affective disorder or schizoaffective disorder. However, the neurobiological basis of PP remains poorly understood and no study has evaluated brain structure in women at risk of, or with, PP. We performed a cross-sectional study of 256 women at risk of PP and 21 healthy controls (HC) in the same postpartum period. Among women at risk, 11 who developed a recent episode of PP (PPE) (n = 2 with lifetime bipolar disorder; n = 9 psychotic disorder not otherwise specified) and 15 at risk women who did not develop an episode of PP (NPPE) (n = 10 with lifetime bipolar disorder; n = 1 with schizoaffective disorder; n = 1 with a history of PP in first-degree family member; n = 3 with previous PP). We obtained T1-weighted MRI scans at 3T and examined regional gray matter volumes with voxel-based morphometry and cortical thickness and surface area with Freesurfer. Women with PPE showed smaller anterior cingulate gyrus, superior temporal gyrus and parahippocampal gyrus compared to NPPE women. These regions also showed decreased surface area. Moreover, the NPPE group showed a larger superior and inferior frontal gyrus volume than the HC. These results should be interpreted with caution, as there were between-group differences in terms of duration of illness and interval between delivery and MRI acquisition. Nevertheless, these are the first findings to suggest that MRI can provide information on brain morphology that characterize those women at risk of PP more likely to develop an episode after childbirth.
Article
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Background Mental health is a significant contributor to global burden of disease and the consequences of perinatal psychiatric morbidity can be substantial. We aimed to obtain global estimates of puerperal psychosis prevalence based on population-based samples and to understand how postpartum psychosis is assessed and captured among included studies. Methods In June 2014, we searched PubMed, CiNAHL, EMBASE, PsycINFO, Sociological Collections, and Global Index Medicus for publications since the year 1990. Criteria for inclusion in the systematic review were: use of primary data relevant to pre-defined mental health conditions, specified dates of data collection, limited to data from 1990 onwards, sample size >200 and a clear description of methodology. Data were extracted from published peer reviewed articles. ResultsThe search yielded 24,273 publications, of which six studies met the criteria. Five studies reported incidence of puerperal psychosis (ranging from 0.89 to 2.6 in 1000 women) and one reported prevalence of psychosis (5 in 1000). Due to the heterogeneity of methodologies used across studies in definitions and assessments used to identify cases, data was not pooled to calculate a global estimate of risk. Conclusions This review confirms the relatively low rate of puerperal psychosis; yet given the potential for serious consequences, this morbidity is significant from a global public health perspective. Further attention to consistent detection of puerperal psychosis can help provide appropriate treatment to prevent harmful consequences for both mother and baby.
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The transition to motherhood, and the resultant experience of caregiving, may change the way women respond to affective, infant signals in their environments. Nonhuman animal studies have robustly demonstrated that mothers process both infant and other salient signals differently from nonmothers. Here, we investigated how women with and without young infants respond to vocalisations from infants and adults (both crying and neutral). We examined mothers with infants ranging in age (1–14 months) to examine the effects of duration of maternal experience. Using functional magnetic resonance imaging, we found that mothers showed greater activity than nonmothers to vocalisations from adults or infants in a range of cortical regions implicated in the processing of affective auditory cues. This main effect of maternal status suggests a general difference in vocalisation processing across infant and adult sounds. We found that a longer duration of motherhood, and therefore more experience with an infant, was associated with greater infant-specific activity in key parental brain regions, including the orbitofrontal cortex and amygdala. We suggest that these incremental differences in neural activity in the maternal brain reflect the building of parental capacity over time. This is consistent with conceptualizations of caregiving as a dynamic, learning process in humans.
Article
OBJECTIVE: To review the evidence about the prevalence and determinants of non-psychotic common perinatal mental disorders (CPMDs) in World Bank categorized low- and lower-middle-income countries. METHODS: Major databases were searched systematically for English-language publications on the prevalence of non-psychotic CPMDs and on their risk factors and determinants. All study designs were included. FINDINGS: Thirteen papers covering 17 low- and lower-middle-income countries provided findings for pregnant women, and 34, for women who had just given birth. Data on disorders in the antenatal period were available for 9 (8%) countries, and on disorders in the postnatal period, for 17 (15%). Weighted mean prevalence was 15.6% (95% confidence interval, CI: 15.4-15.9) antenatally and 19.8% (19.5-20.0) postnatally. Risk factors were: socioeconomic disadvantage (odds ratio [OR] range: 2.1-13.2); unintended pregnancy (1.6-8.8); being younger (2.1-5.4); being unmarried (3.4-5.8); lacking intimate partner empathy and support (2.0-9.4); having hostile in-laws (2.1-4.4); experiencing intimate partner violence (2.11-6.75); having insufficient emotional and practical support (2.8-6.1); in some settings, giving birth to a female (1.8-2.6), and having a history of mental health problems (5.1-5.6). Protective factors were: having more education (relative risk: 0.5; P = 0.03); having a permanent job (OR: 0.64; 95% CI: 0.4-1.0); being of the ethnic majority (OR: 0.2; 95% CI: 0.1-0.8) and having a kind, trustworthy intimate partner (OR: 0.52; 95% CI: 0.3-0.9). CONCLUSION: CPMDs are more prevalent in low- and lower-middle-income countries, particularly among poorer women with gender-based risks or a psychiatric history.
Article
Objective: The birth of a preterm infant and Neonatal Intensive Care Unit hospitalization constitute a potentially traumatic experience for mothers. Although behavioral studies investigated the parenting stress in preterm mothers, no study focused on the underlying neural mechanisms. We examined the effect of preterm births in mothers, by comparing brain activation in mothers of preterm and full-term infants. Study design: We used functional magnetic resonance imaging to measure the cerebral response of 10 first-time mothers of preterm infants (gestational age <32 weeks and/or birth weight <1500) and 11 mothers of full-term infants, viewing happy-, neutral- and distress-face images of their own infant, along with a matched unknown infant. Results: While viewing own infant's face preterm mothers showed increased activation in emotional processing area (i.e., inferior frontal gyrus) and social cognition (i.e., supramarginal gyrus) and affiliative behavior (i.e., insula). Conclusion: Differential brain activation patterns in mothers appears to be a function of the atypical parenthood transition related to prematurity.Journal of Perinatology advance online publication, 2 February 2017; doi:10.1038/jp.2017.2.
Article
Ten to twenty percent of postpartum women experience anxiety or depressive disorders, which can have detrimental effects on the mother, child, and family. Little is known about the neural correlates of these affective disorders when they occur in mothers, but they do have unique neural profiles during the postpartum period compared with when they occur at other times in a woman's life. Given that the neural systems affected by postpartum anxiety and depression overlap and interact with the systems involved in maternal caregiving behaviors, mother-infant interactions are highly susceptible to disruption. Thus, there is an intricate interplay among maternal mental health, the mother-infant relationship, and the neurobiological mechanisms mediating them that needs to be the focus of future study.
Article
Pregnancy involves radical hormone surges and biological adaptations. However, the effects of pregnancy on the human brain are virtually unknown. Here we show, using a prospective ('pre'-'post' pregnancy) study involving first-time mothers and fathers and nulliparous control groups, that pregnancy renders substantial changes in brain structure, primarily reductions in gray matter (GM) volume in regions subserving social cognition. The changes were selective for the mothers and highly consistent, correctly classifying all women as having undergone pregnancy or not in-between sessions. Interestingly, the volume reductions showed a substantial overlap with brain regions responding to the women's babies postpartum. Furthermore, the GM volume changes of pregnancy predicted measures of postpartum maternal attachment, suggestive of an adaptive process serving the transition into motherhood. Another follow-up session showed that the GM reductions endured for at least 2 years post-pregnancy. Our data provide the first evidence that pregnancy confers long-lasting changes in a woman's brain.