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Abstract

PAWLUSKI, J.L., Hoekzema, E., Leuner, B,. and Lonstein, J.S. Less can be more: Fine tuning the maternal brain. NEUROSCI BIOBEHAV REV (129) XXX-XXX, 2022. Plasticity in the female brain across the lifespan has recently become a growing field of scientific inquiry. This has led to the understanding that the transition to motherhood is marked by some of the most significant changes in brain plasticity in the adult female brain. Perhaps unexpectedly, plasticity occurring in the maternal brain often involves a decrease in brain volume, neurogenesis and glial cell density that presumably optimizes caregiving and other postpartum behaviors. This review summarizes what we know of the ‘fine-tuning’ of the female brain that accompanies motherhood and highlights the implications of these changes for maternal neurobehavioral health. The first part of the review summarizes structural and functional brain changes in humans during pregnancy and postpartum period with the remainder of the review focusing on neural and glial plasticity during the peripartum period in animal models. The aim of this review is to provide a clear understanding of when ‘less is more’ in maternal brain plasticity and where future research can focus to improve our understanding of the unique brain plasticity occurring during matrescence.

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... Maternal behaviour is one of the most important social behaviours, and its expression requires many genetic and physiological changes in the brain of females [1][2][3] . These changes enable dams to cope with the new situation and improve the likelihood of offspring survival. ...
... These changes enable dams to cope with the new situation and improve the likelihood of offspring survival. Thus, reproductive fitness and maternal behaviour are closely related [1][2][3][4] . ...
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Virgin female laboratory mice readily express maternal care when co-housed with dams and pups. However, pup-sensitized virgins fail to express maternal aggression on a single session of testing. To study whether repeated testing would affect the onset and dynamics of maternal aggression we tested dams and their accompanying virgins from postpartum day 4 to 6. Repeated testing led to escalated aggression towards male intruders in dams, but virgins never developed aggression. In dams, inhibition of the medial amygdala using DREADD (designer receptors exclusively activated by designer drugs) vectors carrying the hM4Di receptor blocked the expected increase in maternal aggression on the second testing day. Our data support that the onset of maternal aggression is linked to physiological changes occurring during motherhood, and that medial amygdala, a key centre integrating vomeronasal, olfactory and hormonal information, enables the expression of escalated aggression induced by repeated testing.
... Various adaptive changes, from the molecular to behavioral level, are well documented in laboratory animals, including increased chronic basal hypercorticism, decreased hypothalamic pituitary adrenal (HPA) axis responsiveness to stressors, decreased corticotropin-releasing hormone (CRH, a stress hormone) mRNA and hypothalamic paraventricular nucleus (PVN) binding, increased oxytocin and receptor mRNA expression in the PVN, increased adult neuroplasticity (e.g., adult neurogenesis), reduced sensorimotor gating (an attentional filtering function) as measured in prepulse inhibition (PPI), reduced acoustic startle response, increased pup-directed maternal responses (pup retrieval and nursing), increased maternal aggression, decreased anxiety, and enhanced memory function (Byrnes et al., 2007;Hård & Hansen, 1985;Hillerer et al., 2012;Kask et al., 2008;Kinsley & Lambert, 2008). Magnetic resonance imaging (MRI) studies on the brains of human mothers have also documented structural and functional changes in certain corticolimbic circuits involved in emotional processing, volitional attention and executive function, reward and motivation, and sensorimotor functions (Kim et al., 2010Pawluski et al., 2021). These areas include the prefrontal cortex (PFC), cingulate cortex, parietal cortex, amygdala, striatum, hypothalamus, and substantia nigra (SN). ...
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The postpartum period is associated with structural and functional plasticity in brain regions involved in parenting. While one study identified an increase in gray matter volume during the first 4 months among new mothers, little is known regarding the relationship between cortical thickness across postpartum months and perceived adjustment to parenthood. In this study of 39 socioeconomically diverse first-time new mothers, we examined the relations among postpartum months, cortical thickness, and parental self-efficacy. We identified a positive association between postpartum months and cortical thickness in the prefrontal cortex including the superior frontal gyrus extending into the medial frontal and orbitofrontal gyri, in the lateral occipital gyrus extending into the inferior parietal and fusiform gyri, as well as in the caudal middle frontal and precentral gyri. The relationship between cortical thickness and parental self-efficacy was specific to the prefrontal regions. These findings contribute to our understanding of the maternal brain in the first 6 months postpartum and provide evidence of a relationship between brain structure and perceived adjustment to parenthood.
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There is widespread consensus that distributed circuits across prefrontal and anterior cingulate cortex (PFC/ACC) are critical for reward‐based decision making. The circuit specialisations of these areas in primates were likely shaped by their foraging niche, in which decision making is typically sequential, attention‐guided and temporally extended. Here, I argue that in humans and other primates, PFC/ACC circuits are functionally specialised in two ways. First, microcircuits found across PFC/ACC are highly recurrent in nature and have synaptic properties that support persistent activity across temporally extended cognitive tasks. These properties provide the basis of a computational account of time‐varying neural activity within PFC/ACC as a decision is being made. Second, the macrocircuit connections (to other brain areas) differs between distinct PFC/ACC cytoarchitectonic subregions. This variation in macrocircuit connections explains why PFC/ACC subregions make unique contributions to reward‐based decision tasks, and how these contributions are shaped by attention. They predict dissociable neural representations to emerge in orbitofrontal, anterior cingulate and dorsolateral prefrontal cortex during sequential attention‐guided choice, as recently confirmed in neurophysiological recordings.
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Phenotypic plasticity allows organisms to respond to changing environments throughout their lifetime, but these changes are rarely reversible. Exceptions occur in relatively long-lived vertebrate species that exhibit seasonal plasticity in brain size, although similar changes have not been identified in short-lived species, such as insects. Here, we investigate brain plasticity in reproductive workers of the ant Harpegnathos saltator . Unlike most ant species, workers of H. saltator are capable of sexual reproduction, and they compete in a dominance tournament to establish a group of reproductive workers, termed ‘gamergates'. We demonstrated that, compared to foragers, gamergates exhibited a 19% reduction in brain volume in addition to significant differences in behaviour, ovarian status, venom production, cuticular hydrocarbon profile, and expression profiles of related genes. In experimentally manipulated gamergates, 6–8 weeks after being reverted back to non-reproductive status their phenotypes shifted to the forager phenotype across all traits we measured, including brain volume, a trait in which changes were previously shown to be irreversible in honeybees and Drosophila . Brain plasticity in H. saltator is therefore more similar to that found in some long-lived vertebrates that display reversible changes in brain volume throughout their lifetimes.
Article
Despite continual debate for the past 30 years about the function of anterior cingulate cortex (ACC), its key contribution to neurocognition remains unknown. However, recent computational modeling work has provided insight into this question. Here we review computational models that illustrate three core principles of ACC function, related to hierarchy, world models, and cost. We also discuss four constraints on the neural implementation of these principles, related to modularity, binding, encoding, and learning and regulation. These observations suggest a role for ACC in hierarchical model-based hierarchical reinforcement learning (HMB-HRL), which instantiates a mechanism motivating the execution of high-level plans.
Article
Mother-infant bonding develops rapidly following parturition and is accompanied by changes in sensory perception and behavior. Here, we study how ultrasonic vocalizations (USVs) are represented in the brain of mothers. Using a mouse line that allows temporally controlled genetic access to active neurons, we find that the temporal association cortex (TeA) in mothers exhibits robust USV responses. Rabies tracing from USV-responsive neurons reveals extensive subcortical and cortical inputs into TeA. A particularly dominant cortical source of inputs is the primary auditory cortex (A1), suggesting strong A1-to-TeA connectivity. Chemogenetic silencing of USV-responsive neurons in TeA impairs auditory-driven maternal preference in a pup-retrieval assay. Furthermore, dense extracellular recordings from awake mice reveal changes of both single-neuron and population responses to USVs in TeA, improving discriminability of pup calls in mothers compared with naive females. These data indicate that TeA plays a key role in encoding and perceiving pup cries during motherhood.
Article
Background: Pregnancy constitutes a significant period in the lives of women, after which they often experience numerous crucial physiological and psychological changes. Functional neuroimaging studies have shown longitudinal changes in functional brain activity in mothers responding to infant-related stimuli. However, the structural changes that occur in the brains of mothers after delivery remain to be explored. Objective: We aimed to evaluate the structural changes in mothers during the postpartum phase. Methods: We recruited 35 primiparous mothers and 26 nonmothers to participate in this voxel- and surface-based morphometry study, and 22 mothers were scanned twice with a follow-up of approximately 2 years. Results: Compared to nonmothers, mothers exhibited reduced gray matter (GM) volumes and increased white matter (WM) volumes in regions associated with empathy and reward networks (supplementary motor area, precuneus, inferior parietal lobe, insula, and striatum), decreased cortical thickness in the precentral gyrus and increased gyrification index in the orbitofrontal cortex. Furthermore, mothers showed longitudinal changes in the GM and WM volumes and cortical thickness of several of these regions (including the superior and medial frontal gyrus, insula, limbic lobe, superior and middle temporal gyrus, and precentral gyrus), which have been associated with maternal networks during the postpartum period. Additionally, the changes in GM and WM volumes were related to changes in empathetic abilities in mothers. Conclusion: These results suggest that the brains of mothers exhibit adaptive structural dynamic plasticity. These findings provide a neuroanatomical basis for understanding how mothers process emotional sensory information during the postpartum period.
Article
Cortical neuronal circuits along the sensorimotor pathways are shaped by experience during critical periods of heightened plasticity in early postnatal development. After closure of critical periods, measured histologically by the formation and maintenance of extracellular matrix structures called perineuronal nets (PNNs), the adult mouse brain exhibits restricted plasticity and maturity. Mature PNNs are typically considered to be stable structures that restrict synaptic plasticity on cortical parvalbumin+ GABAergic neurons. Changes in environment (i.e. novel behavioral training) or social contexts (i.e. motherhood) are known to elicit synaptic plasticity in relevant neural circuitry. However, little is known about concomitant changes in the PNNs surrounding the cortical parvalbumin+ GABAergic neurons. Here, we show novel changes in PNN density in the primary somatosensory cortex (SS1) of adult female mice after maternal experience (called Surrogate, Sur), using systematic microscopy analysis of a whole brain region. On average, PNNs were increased in the right barrel field and decreased in the left forelimb regions. Individual mice had left hemisphere dominance in PNN density. Using adult female mice deficient in methyl-CpG-binding protein 2 (MECP2), an epigenetic regulator involved in regulating experience-dependent plasticity, we found that MECP2 is critical for this precise and dynamic expression of PNN. Adult naïve Mecp2-heterozygous females (Het) had increased PNN density in specific subregions in both hemispheres before maternal experience, compared to wildtype (WT) littermate controls. The laterality in PNN expression seen in naïve Het was lost after maternal experience in Surrogate Het mice, suggesting possible intact mechanisms for plasticity. Together, our results identify subregion and hemisphere-specific alterations in PNN expression in adult females, suggesting extracellular matrix plasticity as a possible neurobiological mechanism for adult behaviors in rodents.Significance Statement Perineuronal nets (PNNs) are extracellular matrix structures that surround cortical parvalbumin+ fast spiking GABAergic interneurons and synapses. They have long been considered stable structures that restrict synaptic plasticity. Removal of PNNs by enzymes reactivates plasticity in the rodent visual and auditory cortices and in the amygdala. However, it is currently unknown if PNNs in adult brains undergo changes in expression under normal physiological conditions, similar to synaptic plasticity mechanisms. If they do, PNNs may not be very stable structures as they are perceived. We provide evidence that mature PNNs in the adult mouse primary somatosensory cortex show dynamic expression changes in a hemisphere-specific, subregion-specific manner after maternal experience and are regulated by methyl-CpG-binding protein 2 (MECP2).
Article
Traditionally sex hormones have been associated with reproductive and developmental processes only. Since the 1950s we know that hormones can have organizational effects on the developing brain and initiate hormonal transition periods such as puberty. However, recent evidence shows that sex hormones additionally structure the brain during important hormonal transition periods across a woman's life including short-term fluctuations. during the menstrual cycle. However, a comprehensive review focusing on structural changes during all hormonal transition phases of women is still missing. Therefore, in this review structural changes across hormonal transition periods (i.e. puberty, menstrual cycle, oral contraceptive intake, pregnancy and menopause) were investigated in a structured way and correlations with sex hormones evaluated. Results show an overall reduction in gray matter and region-specific decreases in prefrontal, parietal and middle temporal areas during puberty. Across the menstrual cycle gray matter plasticity in the hippocampus, the amygdala as well as temporal- and parietal regions were most consistently reported. Studies reporting on pre- and post-pregnancy measurements revealed volume reductions in midline structures as well as prefrontal- and temporal cortices. During perimenopause, the decline in sex hormones was paralleled with a reduction in hippocampal and parietal cortex volume. Brain volume changes were significantly correlated with estradiol, testosterone and progesterone levels in some studies but directionality remains inconclusive between studies. These results indicate that sex hormones play an important role in shaping women's brain structure during different transition periods and are not restricted to specific developmental periods.
Article
Objective: Pregnancy causes many changes in our body and some of them may affect our ability of learning and memory. We examined the cerebral cortical volume of brain during pregnancy and measured changes in the brain electrical activity and cerebral blood flow. Method: 35 women (20 normal full-term primigravida and 15 non-pregnant women) received the Electroencephalography (EEG) and Transcranial Doppler ultrasonography (TCD). 8 non-pregnant women and 9 primigravida after vaginal delivery underwent brain magnetic resonance imaging (MRI) voluntarily within 24 h. Results: Compared with the non-pregnant, changes were shown by EEG through electrodes of T5, Pz, Cz, T6, F3 and F8. The results displayed increased activity in the central parietal area of pregnant women, while that in the temporoparietal junction decreased. The result of TCD revealed that pulsation index (PI) values of left and right internal and external carotid arteries were asymmetrical, but they all decreased in pregnancy. Atrophy of cortical volume had been found in many brain functional areas of pregnant women. The percentage of atrophy varied between 6.76% and 13.17%. Conclusion: Atrophy of cerebral cortex, changes in cerebral blood flow and neuron electrophysiology may be the physiological basis of the emotional, cognitive changes in pregnant women.
Article
Pregnancy results in obvious physiological changes to the female body, but data as to what happens to the maternal brain after giving birth are sparse as well as inconsistent. The overall goal of this study is to determine the nature of cerebral change in the postpartum period. For this purpose, we analyzed T1-weighted brain images of 14 healthy women (age range: 25-38 years) at two time points, specifically within 1-2 days of childbirth (immediate postpartum) and at 4-6 weeks after childbirth (late postpartum). When comparing voxel-wise gray matter between these two time points, there was no evidence of any significant decrease. Instead, we detected a pronounced gray matter increase involving both cortical and subcortical regions, such as the pre- and postcentral gyrus, the frontal and central operculum, the inferior frontal gyrus, the precuneus, and the middle occipital gyrus, as well as the thalamus and caudate. These structural changes occurring within only 4-6 weeks after delivery are reflective of a high degree of neuroplasticity and massive adaptations in the maternal brain. They may suggest a restoration of brain tissue following pregnancy and/or a substantial brain reorganization, possibly to accommodate a multi-faceted repertoire of complex behaviors associated with being a mother.
Article
This selective review first describes the involvement of the maternal hypothalamic-pituitary-adrenal (HPA) axis during pregnancy and the postpartum period, and the relation between peripartum HPA axis function and maternal behavior, stress reactivity and emotional dysregulation in human mothers. To provide experimental background to this correlational work, where helpful, animal studies are also described. It then explores the association between HPA axis function in mothers and their infants, under ongoing non-stressful conditions and during stressful challenges, the moderating role of mothers' sensitivity and behavior in the mother-child co-regulation and the effects of more traumatic risk factors on these relations. The overarching theme being explored is that the HPA axis - albeit a system designed to function during periods of high stress and challenge - also functions to promote adaptation to more normative processes, shown in the new mother who experiences both high cortisol and enhanced attraction and attention to and recognition of, their infants and their cues. Hence the same HPA system shows positive relations with behavior at some time points and inverse ones at others. However, the literature is not uniform and results vary widely depending on the number, timing, place, and type of samplings and assessments, and, of course, the population being studied and, in the present context, the state, the stage, and the stress levels of mother and infant.
Article
One of the most frequently prescribed selective serotonin reuptake inhibitor medications (SSRIs) for peripartum mood and anxiety disorders is sertraline (Zoloft®). Sertraline can help alleviate mood and anxiety symptoms in many women but it is not known how sertraline, or SSRIs in general, affect the neurobiology of the brain particularly when pregnant. The aim of this study was to investigate how sertraline affects plasticity in the hippocampus, a brain area integral in depression and SSRI efficacy (particularly in males), during late pregnancy and whether these effects differ from the effects of sertraline in non-pregnant females. To do this pregnant and age-matched non-pregnant female Sprague-Dawley rats were used. For the last half of pregnancy (10 days), and at matched points in non-pregnant females, rats were given sertraline (2.5 mg/kg/day or 10 mg/kg/day) or vehicle (0 mg/kg/day). Brains were used to investigate effects on the serotonergic system in the hippocampus and prefrontal cortex, and measures of neuroplasticity in the hippocampus. Results show that pregnant females have significantly higher serum levels of sertraline compared to non-pregnant females but that rates of serotonin turnover in the hippocampus and PFC are similar between pregnant and non-pregnant females. Sertraline increased synaptophysin density in the dentate gyrus and CA3 and was associated with a decrease in cell proliferation in dentate gyrus of non-pregnant, but not pregnant, females. During late pregnancy the hippocampus showed significant reductions in neurogenesis and increases in synaptophysin density. This research highlights the need to consider the unique effect of reproductive state on neuropharmacological effects of SSRIs.
Article
There has been interest in the function of adult neurogenesis since its discovery, by Joseph Altman, nearly 60 years ago. While controversy curtailed follow up studies, in the 1990s a second wave of research validated many of Altman's original claims and revealed that factors such as stress and environmental stimulation altered the production of new neurons in the hippocampus. However, only with the advent of tools for manipulating neurogenesis did it become possible to perform causal tests of the function of newborn neurons. Here, we identify approximately 100 studies in which adult neurogenesis was manipulated to study its function. A majority of these studies demonstrate functions for adult neurogenesis in classic hippocampal behaviors such as context learning and spatial memory, as well as emotional behaviors related to stress, anxiety and depression. However, a closer look reveals a number of other, arguably understudied, functions in decision making, temporal association memory, and addiction. In this special issue, we present 16 new studies and review articles that continue to address and clarify the function of adult neurogenesis in behaviors as diverse as memory formation and consolidation, pattern separation and discrimination behaviors, addiction, and attention. Reviews of stem cell dynamics and regenerative properties provide insights into the mechanisms by which neurogenesis may be controlled to offset age- and disease-related brain injury. Finally, translation-oriented reviews identify next steps for minimizing the gap between discoveries made in animals and applications for human health. The articles in this issue synthesize and extend what we have learned in the last half century of functional neurogenesis research and identify themes that will define its future.
Article
Maternal bonding early postpartum lays an important foundation for child development. Changing brain structure and function during pregnancy and postpartum may underscore maternal bonding. We employed connectome-based predictive modeling (CPM) to measure brain functional connectivity and predict self-reported maternal bonding in mothers at 2 and 8 months postpartum. At 2 months, CPM predicted maternal anxiety in the bonding relationship: Greater integration between cerebellar and motor-sensory-auditory networks and between frontoparietal and motor-sensory-auditory networks were associated with more maternal anxiety toward their infant. Furthermore, greater segregation between the cerebellar and frontoparietal, and within the motor-sensory-auditory networks, was associated with more maternal anxiety regarding their infant. We did not observe CPM prediction of maternal bonding impairments or rejection/anger toward the infant. Finally, considering 2 and 8 months of data, changes in network connectivity were associated with changes in maternal anxiety in the bonding relationship. Our results suggest that changing connectivity among maternal brain networks may provide insight into the mother-infant bond, specifically in the context of anxiety and the representation of the infant in the mother's mind. These findings provide an opportunity to mechanistically investigate approaches to enhance the connectivity of these networks to optimize the representational and behavioral quality of the caregiving relationship.
Article
In mothers, offspring cues are associated with a powerful reinforcing value that motivates maternal care. Animal studies show that this is mediated by dopamine release into the nucleus accumbens, a core component of the brain's reward system located in the ventral striatum (VStr). The VStr is also known to respond to infant signals in human mothers. However, it is unknown whether pregnancy modifies the anatomy or functionality of this structure, and whether such modifications underlie its strong reactivity to offspring cues. Therefore, we analyzed structural and functional neuroimaging data from a unique pre-conception prospective cohort study involving first-time mothers investigated before and after their pregnancy as well as nulliparous control women scanned at similar time intervals. First, we delineated the anatomy of the VStr in each subject's neuroanatomical space and examined whether there are volumetric changes in this structure across sessions. Then, we tested if these changes could predict the mothers' brain responses to visual stimuli of their infants. We found decreases in the right VStr and a trend for left VStr reductions in the women who were pregnant between sessions compared to the women who were not. Furthermore, VStr volume reductions across pregnancy were associated with infant-related VStr responses in the postpartum period, with stronger volume decreases predicting stronger functional activation to offspring cues. These findings provide the first indications that the transition to motherhood renders anatomical adaptations in the VStr that promote the strong responsiveness of a mother's reward circuit to cues of her infant.
Article
Maternal brain adaptations have been found across pregnancy and postpartum, but little is known about the long-term effects of parity on the maternal brain. Using neuroimaging and machine learning, we investigated structural brain characteristics in 12,021 middle-aged women from the UK Biobank, demonstrating that parous women showed less evidence of brain aging compared to their nulliparous peers. The relationship between childbirths and a “younger-looking” brain could not be explained by common genetic variation or relevant confounders. Although prospective longitudinal studies are needed, the results suggest that parity may involve neural changes that could influence women’s brain aging later in life.
Article
New neurons are continuously added in the dentate gyrus of the hippocampus, the olfactory bulb and the hypothalamus of mammalian brain. In sheep, while the control of adult neurogenesis by the social environment or the photoperiod has been the subject of several studies, its regulation by intrinsic factors, like hormones or neurotransmitters is less documented. We addressed this question by investigating the effects of central oxytocin administration on hippocampal, olfactory and hypothalamic neurogenesis. Endogenous markers, Ki67, Sox2 and DCX were used to assess cell proliferation, progenitor cells density and cell survival respectively in non-gestant ewes receiving a steroid treatment followed by intracerebroventricular injections of either oxytocin or saline. The results showed that oxytocin treatment significantly decreases the density of neuroblasts in the olfactory bulb, increases the density of neuroblasts in the ventromedian nucleus of the hypothalamus while no change is observed in both ventral and dorsal dentate gyrus. In addition, no change in the density of progenitor cells is found in the three neurogenic niches. These findings show for the first time that in females, oxytocin can regulate adult neurogenesis by acting on neuroblasts but not on progenitor cells and that this regulation is region specific.
Article
Mothers' sensitive responses to their infants have evolutionary importance and are likely hardwired into the maternal brain. Mood disorders are associated with aberrant neural processing of emotion in regions overlapping with 'maternal sensitivity networks' which could compromise maternal processing of infant signals. This systematic review aimed to integrate findings from studies of neural responses to infant stimuli in healthy mothers and in mothers with mood disorders. We included original studies using functional brain imaging and electrophysiological techniques. The databases psycINFO and PubMed were searched for eligible articles until January 2019. Twenty-seven studies met the inclusion criteria, none of which investigated mothers with bipolar disorder or remitted unipolar disorder. Studies were characterized by large methodological heterogeneity. The most consistent findings were that healthy mothers exhibit stronger and faster neural responses to infant stimuli than non-mothers in key emotional processing regions including the amygdala, insula and orbitofrontal cortex, which is accentuated for own infants. Motherswith acute depression display blunted neural responses within these regions which correlates with greater depression severity.
Article
This study investigated cognitive, neural and endocrine function during late pregnancy. One of the first to examine brain ERPs in pregnant women, the study is unique in its focus on response inhibition function. In the study, cognitive function was evaluated by a digit-symbol coding test, an arithmetic ability test, and a visual stop-signal task which places enhanced demands on impulse control and response inhibition, considered a hallmark of executive function. Brain activity was measured by scalp-recorded Event-Related Potentials (ERPs) during the stop-signal task. HPA axis reactivity was assessed by measuring salivary cortisol levels before and after experimental sessions. Test performance, ERPs and cortisol reactivity were compared across groups of 23 women in their third trimester of pregnancy and 22 non-pregnant controls. Pregnant women scored lower than the control group on the digit-symbol coding test. On the stop-signal task, both groups had similar error rates, but pregnant women had longer response times to Go trials. On the Stop condition of the task in which a response must be inhibited, pregnant women demonstrated significantly better performance. At the electro-physiological level, in response to Go stimuli pregnant women exhibited greater amplitude of P2 than controls. In response to Stop-signals, pregnant women had lesser amplitudes of P1 and N2 and greater amplitude of P3. Cortisol reactivity to the test session was significantly more pronounced in non-pregnant women with significant correlations found between cortisol reactivity and behavioral responses. The results suggest that response patterns of women in late pregnancy are less impulsive and more cautious and controlled.
Article
Background/aims: Human pregnancy goes along with decreasing gray matter volume in the brain of the mother. Whether these reductions remain for years or renormalize shortly after delivery is unclear. The present study used a longitudinal control group design to investigate postpartal neural plasticity. Methods: 24 healthy young women were assessed with cognitive and hormonal measures in late pregnancy and underwent a brain scan within the first two months after delivery (TP1). They were compared to 24 naturally cycling women. A follow-up cognitive and imaging measurement was performed three months after the first scan in both groups (TP2, 4-5 months postpartally in the mothers). Results: Compared to the control group, widespread gray matter volume increases from the first to second scan were observed in the new mothers (TP2 > TP1, whole-brain analysis). These were especially pronounced in frontal and cerebellar regions. The time by group interaction pattern of gray matter indicated a postpartal renormalization process, most likely following pregnancy-related decreases. Age was negatively correlated to postpartal gray matter increase in most of the regions. Despite pronounced changes in brain structure, the two groups did not reliably differ in cognitive performance. Conclusion: The results reveal the potential for plasticity in the adult female brain following pregnancy. They support the assumption that the volume reductions during pregnancy renormalize at least partly in the early postpartal phase. The course of renormalization seems to differ between participants of different ages. Future studies are needed to further investigate inter-individual variability and the time course of postpartal neural change.
Article
In the postpartum period, the maternal brain experiences both structural and functional plasticity. While we have a growing understanding of the human maternal brain's responses to infant stimuli, little is known about the intrinsic connectivity among those regions during the postpartum months. Resting‐state functional connectivity (rsFC) provides a measure of the functional architecture of the brain based upon intrinsic functional connectivity i.e. the temporal correlation in blood oxygenation level dependent signal when the brain is not engaged in a specific task. In this study, we used resting‐state fMRI to examine how later postpartum months are associated with rsFC and maternal behaviors. We recruited a sample of forty‐seven socioeconomically diverse first‐time mothers with singleton pregnancies. As the amygdala has been shown to play a critical role in maternal behaviors in the postpartum period, it was chosen as the seed for a seed‐based correlation analysis. For the left amygdala, later postpartum months were associated with greater connectivity with the anterior cingulate gyrus, left nucleus accumbens, right caudate, and left cerebellum (p < 0.05, FDR corrected). Further, in an exploratory analysis, we observed indications that rsFC between the left amygdala and left nucleus accumbens was positively associated with maternal structuring during a mother child‐interaction. In addition, later postpartum months were associated with greater connectivity between the right amygdala and the bilateral caudate and right putamen. Overall, we provide evidence of relationships between postpartum months and rsFC in the regions involved in salience detection and regions involved in maternal motivation. Greater connectivity between the amygdala and nucleus accumbens may play a role in positive maternal behaviors. This article is protected by copyright. All rights reserved.
Article
In a minority of mammalian species, mothers depend on others to help raise their offspring. New research is investigating the neuroendocrine mechanisms supporting this allomaternal behavior. Several hormones have been implicated in allomaternal caregiving; however, the role of specific hormones is variable across species, perhaps because allomothering independently evolved multiple times. Brain regions involved in maternal behavior in non-human animals, such as the medial preoptic area, are also critically involved in allomaternal behavior. Allomaternal experience modulates hormonal systems, neural plasticity, and behavioral reactivity. In humans, fatherhood-induced decreases in testosterone and increases in oxytocin may support sensitive caregiving. Fathers and mothers activate similar neural systems when exposed to child stimuli, and this can be considered a global “parental caregiving” network. Finally, early work on caregiving by non-kin (e.g., foster parents) suggests reliance on similar mechanisms as biologically-related parents. This article is part of the ‘Parental Brain and Behavior’ Special Issue.
Article
In recent decades, human sociocultural changes have increased the numbers of fathers that are involved in direct caregiving in Western societies. This trend has led to a resurgence of interest in understanding the mechanisms and effects of paternal care. Across the animal kingdom, paternal caregiving has been found to be a highly malleable phenomenon, presenting with great variability among and within species. The emergence of paternal behaviour in a male animal has been shown to be accompanied by substantial neural plasticity and to be shaped by previous and current caregiving experiences, maternal and infant stimuli and ecological conditions. Recent research has allowed us to gain a better understanding of the neural basis of mammalian paternal care, the genomic and circuit-level mechanisms underlying paternal behaviour and the ways in which the subcortical structures that support maternal caregiving have evolved into a global network of parental care. In addition, the behavioural, neural and molecular consequences of paternal caregiving for offspring are becoming increasingly apparent. Future cross-species research on the effects of absence of the father and the transmission of paternal influences across generations may allow research on the neuroscience of fatherhood to impact society at large in a number of important ways.
Article
The maternal brain displays considerable plasticity, and motherhood is associated with changes in affective and cognitive function. Motherhood can alter the trajectory of brain aging, including modifications to neuroplasticity and cognition. Here, we investigated the short- and long-term effects of motherhood on hippocampal neurogenesis, microglial density and morphology, and circulating cytokines, domains known to be altered with age and implicated in cognition and mood. Female rats were bred then euthanized during gestation or at various postpartum time points, culminating in middle age, and nulliparous rats served as age-matched controls. Hippocampal neurogenesis was significantly suppressed during gestation and the postpartum period. Interestingly, neurogenesis declined significantly in middle-aged nulliparous rats but increased in primiparous rats across the same period. Transient postpartum adaptations to the neuroimmune environment of the hippocampus were evidenced, as Iba-1-immunoreactive microglia assumed a deramified morphology followed by increased density. Intriguingly, aging-related changes in circulating cytokines were dependent on parity. These adaptations in neurogenic and immune processes may have ramifications for maternal mood and cognition across the peripartum period and beyond.
Article
Mapping the impact of pregnancy on the human brain is essential for understanding the neurobiology of maternal caregiving. Recently, we found that pregnancy leads to a long‐lasting reduction in cerebral gray matter volume. However, the morphometric features behind the volumetric reductions remain unexplored. Furthermore, the similarity between these reductions and those occurring during adolescence, another hormonally similar transitional period of life, still needs to be investigated. Here, we used surface‐based methods to analyze the longitudinal magnetic resonance imaging data of a group of 25 first‐time mothers (before and after pregnancy) and compare them to those of a group of 25 female adolescents (during 2 years of pubertal development). For both first‐time mothers and adolescent girls, a monthly rate of volumetric reductions of 0.09 mm³ was observed. In both cases, these reductions were accompanied by decreases in cortical thickness, surface area, local gyrification index, sulcal depth, and sulcal length, as well as increases in sulcal width. In fact, the changes associated with pregnancy did not differ from those that characterize the transition during adolescence in any of these measures. Our findings are consistent with the notion that the brain morphometric changes associated with pregnancy and adolescence reflect similar hormonally primed biological processes.
Article
Prior reproductive experience, or parity, may contribute to differential neural responses to infant stimuli during pregnancy. We examined the P300 elicited by viewing infant and adult faces, as well as houses, in women pregnant with their first child and compared their neural responses to women who had at least one child prior to their current pregnancy. We found the P300 amplitude was larger in women pregnant with their first child as compared to pregnant women who had previously had children. This larger P300 response was observed in response to all visual stimuli and was not specific to infant faces. Taken together, these findings indicate increased sensitivity toward social and non-social stimuli in pregnancy and indicate the importance of measuring parity in social neuroscience studies of pregnancy and motherhood.