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1.
Biol Psychiatry ; 95(1): 27-36, 2024 Jan 01.
Article in English | MEDLINE | ID: mdl-37393047

ABSTRACT

BACKGROUND: Maternal stress (MS) is a well-documented risk factor for impaired emotional development in offspring. Rodent models implicate the dentate gyrus (DG) of the hippocampus in the effects of MS on offspring depressive-like behaviors, but mechanisms in humans remain unclear. Here, we tested whether MS was associated with depressive symptoms and DG micro- and macrostructural alterations in offspring across 2 independent cohorts. METHODS: We analyzed DG diffusion tensor imaging-derived mean diffusivity (DG-MD) and volume in a three-generation family risk for depression study (TGS; n = 69, mean age = 35.0 years) and in the Adolescent Brain Cognitive Development (ABCD) Study (n = 5196, mean age = 9.9 years) using generalized estimating equation models and mediation analysis. MS was assessed by the Parenting Stress Index (TGS) and a measure compiled from the Adult Response Survey from the ABCD Study. The Patient Health Questionnaire-9 and rumination scales (TGS) and the Child Behavior Checklist (ABCD Study) measured offspring depressive symptoms at follow-up. The Schedule for Affective Disorders and Schizophrenia-Lifetime interview was used to assign depression diagnoses. RESULTS: Across cohorts, MS was associated with future symptoms and higher DG-MD (indicating disrupted microstructure) in offspring. Higher DG-MD was associated with higher symptom scores measured 5 years (in the TGS) and 1 year (in the ABCD Study) after magnetic resonance imaging. In the ABCD Study, DG-MD was increased in high-MS offspring who had depressive symptoms at follow-up, but not in offspring who remained resilient or whose mother had low MS. CONCLUSIONS: Converging results across 2 independent samples extend previous rodent studies and suggest a role for the DG in exposure to MS and offspring depression.


Subject(s)
Diffusion Tensor Imaging , Mothers , Adult , Female , Child , Adolescent , Humans , Diffusion Tensor Imaging/methods , Mothers/psychology , Hippocampus , Magnetic Resonance Imaging , Dentate Gyrus , Depression/etiology
2.
JAMA Psychiatry ; 81(4): 406-413, 2024 Apr 01.
Article in English | MEDLINE | ID: mdl-38150238

ABSTRACT

Importance: Knowledge about childhood resilience factors relevant in circumstances of marginalization and high numbers of adverse childhood experiences (ACEs) can improve interventions. Objective: To identify sociocultural resilience factors in childhood that are associated with better young adult mental health in the context of ACEs. Design, Setting, and Participants: This cohort study examined 4 waves of data from the Boricua Youth Study, which included Puerto Rican children from the South Bronx, New York, and San Juan, Puerto Rico. Participants were aged 5 to 17 years at waves 1 through 3 (2000-2003) and aged 15 to 29 years at wave 4 (2013-2017). Linear and logistic regression models tested the associations of 7 childhood resilience factors and their interaction with ACEs on young adult mental health outcomes. Data were analyzed from June 2021 to October 2023. Main Outcomes and Measures: Perceived stress, major depressive disorder and/or generalized anxiety disorder (MDD/GAD), and substance use disorder (SUD) in young adulthood. Results: Among a total 2004 participants, the mean (SD) age at wave 4 was 22.4 (2.9) years; 1024 participants (51.1%) were female, and 980 (48.9%) were male. Positive parent-child relationships and nonparental adult support during childhood were associated with both lower perceived stress (ß = -0.14; SE = 0.02; P < .001; ß = -0.08; SE = 0.03; P = .003, respectively) and lower odds of MDD/GAD (adjusted odds ratio [aOR], 0.84; 95% CI, 0.73 to 0.97; aOR = 0.81; 95% CI, 0.69 to 0.95, respectively) in young adulthood. Maternal warmth reported during childhood was also associated with lower young adult perceived stress (ß = -0.11; SE = 0.02; P < .001). None of the resilience factors were associated with SUD. The resilience factors familism, friendships, and family religiosity were not associated with any of the mental health outcomes. ACEs were associated with poorer mental health outcomes; however, none of the resilience factors exhibited interactions consistent with being protective for ACEs. Unexpectedly, higher family religiosity was associated with more perceived stress in the presence of higher ACEs. Conclusions and Relevance: The results of this study suggest that promoting positive relationships with adults during childhood may reduce later young adulthood stress and MDD/GAD. However, there is still a need to identify sociocultural childhood protective factors for ACEs. Caution should be taken in assuming what resilience factors are relevant for a given group, as higher family religiosity (one postulated resilience factor) was unexpectedly associated with a stronger, rather than a weaker, association between ACEs and perceived stress in young adulthood.


Subject(s)
Adverse Childhood Experiences , Depressive Disorder, Major , Resilience, Psychological , Substance-Related Disorders , Adolescent , Young Adult , Humans , Male , Female , Adult , Cohort Studies , Mental Health
3.
Psychol Med ; 53(6): 2476-2484, 2023 04.
Article in English | MEDLINE | ID: mdl-34743762

ABSTRACT

BACKGROUND: Prospective studies are needed to assess the influence of pre-pandemic risk factors on mental health outcomes following the COVID-19 pandemic. From direct interviews prior to (T1), and then in the same individuals after the pandemic onset (T2), we assessed the influence of personal psychiatric history on changes in symptoms and wellbeing. METHODS: Two hundred and four (19-69 years/117 female) individuals from a multigenerational family study were followed clinically up to T1. Psychiatric symptom changes (T1-to-T2), their association with lifetime psychiatric history (no, only-past, and recent psychiatric history), and pandemic-specific worries were investigated. RESULTS: At T2 relative to T1, participants with recent psychopathology (in the last 2 years) had significantly fewer depressive (mean, M = 41.7 v. 47.6) and traumatic symptoms (M = 6.6 v. 8.1, p < 0.001), while those with no and only-past psychiatric history had decreased wellbeing (M = 22.6 v. 25.0, p < 0.01). Three pandemic-related worry factors were identified: Illness/death, Financial, and Social isolation. Individuals with recent psychiatric history had greater Illness/death and Financial worries than the no/only-past groups, but these worries were unrelated to depression at T2. Among individuals with no/only-past history, Illness/death worries predicted increased T2 depression [B = 0.6(0.3), p < 0.05]. CONCLUSIONS: As recent psychiatric history was not associated with increased depression or anxiety during the pandemic, new groups of previously unaffected persons might contribute to the increased pandemic-related depression and anxiety rates reported. These individuals likely represent incident cases that are first detected in primary care and other non-specialty clinical settings. Such settings may be useful for monitoring future illness among newly at-risk individuals.


Subject(s)
COVID-19 , Mental Health , Female , Humans , COVID-19/epidemiology , Pandemics , Depression/diagnosis , SARS-CoV-2
4.
Harv Rev Psychiatry ; 30(3): 163-180, 2022.
Article in English | MEDLINE | ID: mdl-35576448

ABSTRACT

LEARNING OBJECTIVES: After participating in this activity, learners should be better able to:• Discuss whether prepubertal depression shows longitudinal continuity with depression in adulthood.• Summarize existing literature on adult emotional and functional outcomes of prepubertal depression and internalizing problems. BACKGROUND: Adolescent- and young adult-onset depression are common, recurrent, and can cause significant distress and psychosocial impairment across the life span, but recognition of prepubertal internalizing problems and depression, along with their prevalence, clinical course, and long-term outcomes, remains elusive. OBJECTIVE: To examine whether prepubertal depression, which can manifest differently from adult depression, shows longitudinal continuity with depression in adulthood, and to summarize existing literature on adult emotional and functional outcomes of prepubertal depression and internalizing problems. METHODS: A scoping review was conducted for peer-reviewed cohort articles published between 2000 and 2020 using PubMed and PsycINFO. From 4309 identified references, 17 articles were included. RESULTS: Prepubertal depression confers increased risk of recurrence of depression in adulthood, with similar findings for prepubertal internalizing problems. No studies found prepubertal depression or internalizing problems predicting adult substance abuse, and no studies asked about adult bipolar diagnoses. More research is needed to draw clear conclusions regarding their implications for other psychiatric, medical, or psychosocial outcomes. CONCLUSION: The reviewed studies provide limited evidence that prepubertal depression onset predicts adult depression. The small evidence base and heterogeneous methodological assessments may limit, however, the ability to draw meaningful conclusions about the long-term course of prepubertal-onset depression. Well-designed studies with longer follow-up and multiple assessments in adulthood are needed to clarify and assess the potential effects of prepubertal depression on adult health and functioning. This information will eventually become available as the samples in recently initiated longitudinal cohort studies of children mature further.


Subject(s)
Depression , Substance-Related Disorders , Adolescent , Adult , Child , Depression/epidemiology , Humans , Longitudinal Studies , Substance-Related Disorders/epidemiology , Young Adult
5.
Clin Child Fam Psychol Rev ; 25(1): 93-109, 2022 03.
Article in English | MEDLINE | ID: mdl-35122559

ABSTRACT

With the growing involvement of fathers in childrearing and the application of neuroscientific tools to research on parenting, there is a need to understand how a father's brain and neurohormonal systems accommodate the transition to parenthood and how such neurobiological changes impact children's mental health, sociality, and family functioning. In this paper, we present a theoretical model on the human father's brain and the neural adaptations that take place when fathers assume an involved role. The neurobiology of fatherhood shows great variability across individuals, societies, and cultures and is shaped to a great extent by bottom-up caregiving experiences and the amount of childrearing responsibilities. Mechanisms of mother-father coparental brain coordination and hormonal correlates of paternal behavior are detailed. Adaptations in the father's brain during pregnancy and across the postpartum year carry long-term implications for children's emotion regulation, stress management, and symptom formation. We propose a new conceptual model of HEALthy Father Brain that describes how a father's brain serves as a source of resilience in the context of family adversity and its capacity to "heal", protect, and foster social brain maturation and functionality in family members via paternal sensitivity, attunement, and support, which, in turn, promote child development and healthy family functioning. Father's brain provides a unique model on neural plasticity as sustained by committed acts of caregiving, thereby affording a novel perspective on the brain basis of human affiliation.


Subject(s)
Father-Child Relations , Fathers , Brain/physiology , Child , Fathers/psychology , Female , Humans , Male , Parenting/psychology , Paternal Behavior/physiology , Paternal Behavior/psychology , Pregnancy
6.
Neuropsychopharmacology ; 47(2): 531-542, 2022 01.
Article in English | MEDLINE | ID: mdl-34162998

ABSTRACT

Deficits in social cognition and functioning are common in major depressive disorder (MDD). Still, no study into the pathophysiology of MDD has examined the social cognition-related neural pathways through which familial risk for MDD leads to depression and interpersonal impairments. Using resting-state fMRI, we applied a graph theoretical analysis to quantify the influence of nodes within the fronto-temporo-parietal cortical social cognition network in 108 generation 2 and generation 3 offspring at high and low-risk for MDD, defined by the presence or absence, respectively, of moderate to severe MDD in generation 1. New MDD episodes, future depressive symptoms, and interpersonal impairments were tested for associations with social cognition nodal influence, using regression analyses applied in a generalized estimating equations approach. Increased familial risk was associated with reduced nodal influence within the network, and this predicted new depressive episodes, worsening depressive symptomatology, and interpersonal impairments, 5-8 years later. Findings remained significant after controlling for current depressive/anxiety symptoms and current/lifetime MDD and anxiety disorders. Path-analysis models indicate that increased familial risk impacted offspring's brain function in two ways. First, high familial risk was indirectly associated with future depression, both new MDD episodes and symptomatology, via reduced nodal influence of the right posterior superior temporal gyrus (pSTG). Second, high familial risk was indirectly associated with future interpersonal impairments via reduced nodal influence of right inferior frontal gyrus (IFG). Finally, reduced nodal influence was associated with high familial risk in (1) those who had never had MDD at the time of scanning and (2) a subsample (n = 52) rescanned 8 years later. Together, findings reveal a potential pathway for the intergenerational transmission of vulnerability via the aberrant social cognition network organization and suggest using the connectome of neural network related to social cognition to identify intervention and prevention targets for those particularly at risk.


Subject(s)
Depressive Disorder, Major , Brain/diagnostic imaging , Depression , Humans , Magnetic Resonance Imaging , Prospective Studies , Social Cognition
8.
Dev Psychopathol ; : 1-15, 2021 Jun 08.
Article in English | MEDLINE | ID: mdl-34099080

ABSTRACT

In this three-generation longitudinal study of familial depression, we investigated the continuity of parenting styles, and major depressive disorder (MDD), temperament, and social support during childrearing as potential mechanisms. Each generation independently completed the Parental Bonding Instrument (PBI), measuring individuals' experiences of care and overprotection received from parents during childhood. MDD was assessed prospectively, up to 38 years, using the semi-structured Schedule for Affective Disorders and Schizophrenia (SADS). Social support and temperament were assessed using the Social Adjustment Scale - Self-Report (SAS-SR) and Dimensions of Temperament Scales - Revised, respectively. We first assessed transmission of parenting styles in the generation 1 to generation 2 cycle (G1→G2), including 133 G1 and their 229 G2 children (367 pairs), and found continuity of both care and overprotection. G1 MDD accounted for the association between G1→G2 experiences of care, and G1 social support and temperament moderated the transmission of overprotection. The findings were largely similar when examining these psychosocial mechanisms in 111 G2 and their spouses (G2+S) and their 136 children (G3) (a total of 223 pairs). Finally, in a subsample of families with three successive generations (G1→G2→G3), G2 experiences of overprotection accounted for the association between G1→G3 experiences of overprotection. The results of this study highlight the roles of MDD, temperament, and social support in the intergenerational continuity of parenting, which should be considered in interventions to "break the cycle" of poor parenting practices across generations.

9.
J Nerv Ment Dis ; 209(5): 370-377, 2021 05 01.
Article in English | MEDLINE | ID: mdl-33835955

ABSTRACT

ABSTRACT: Recent studies have shown that religiosity (R) is associated with lower rates of depression, whereas spirituality (S) is associated with higher rates. Rumination has also been associated with higher rates of depression. Some have hypothesized that rumination mediates the differential association of religiosity and spirituality with depression. We empirically test this hypothesis in a longitudinal, multigenerational sample through associations between rumination and depression, R/S and depression, and R/S and rumination. Cross-sectionally, total rumination scores were predicted by spirituality (standardized ß = 0.13; 95% confidence interval [CI], 0.00-0.26), with subscale (reflection, depression, and brooding) standardized betas ranging from 0.11 to 0.15 (95% CI, -0.03 to -0.29). Cross-sectionally, rumination was not predicted by religiosity. Longitudinally, and consistent with previous findings, religiosity, but not spirituality, predicted reduced depressive symptoms (standardized ß = -0.3; 95% CI, -0.58 to -0.01). The association between spirituality and rumination was driven by millennials. Psychotherapies that target rumination for depression might therefore be especially effective in the millennial demographic.


Subject(s)
Cognitive Behavioral Therapy , Depression/therapy , Psychotherapy , Rumination, Cognitive , Spirituality , Adult , Cross-Sectional Studies , Female , Humans , Intergenerational Relations , Male
10.
Dev Psychobiol ; 63(5): 1482-1498, 2021 07.
Article in English | MEDLINE | ID: mdl-33432595

ABSTRACT

While early caregiving and child's temperamental dispositions work in concert to shape social-emotional outcomes, their unique and joint contribution to the maturation of the child's stress and immune systems remain unclear. We followed children longitudinally from infancy to preschool to address the buffering effect of early parenting on the link between temperamental dysregulation and hypothalamic-pituitary-adrenal (HPA)-immune axis in preschool-aged children. Participants included 47 typically developing children and their 94 parents in both mother-father and two-father families followed across the first 4-years of family formation. In infancy, we observed parent-infant synchrony and measured parental oxytocin; in preschool, we observed temperamental reactivity and self-regulation and assessed children's cortisol and secretory Immunoglobulin A (s-IgA), biomarkers of the stress and immune systems. Greater self-regulation and lower negative emotionality were associated with lower baseline s-IgA and cortisol, respectively. However, these links were defined by interactive effects so that preschoolers with low self-regulation displayed higher s-IgA levels only in cases of low parent-infant synchrony and negative emotionality linked with greater baseline cortisol levels only when parental oxytocin levels were low. Results emphasize the long-term stress-buffering role of the neurobiology of parental care, demonstrate comparable developmental paths for mothers and fathers, and delineate the complex developmental cascades to the maturation of children's stress-management systems.


Subject(s)
Pituitary-Adrenal System , Saliva , Child , Child, Preschool , Fathers/psychology , Female , Humans , Hypothalamo-Hypophyseal System , Infant , Male , Parenting/psychology
11.
Article in English | MEDLINE | ID: mdl-32855106

ABSTRACT

BACKGROUND: Offspring of individuals with major depressive disorder (MDD) are at increased risk for developing MDD themselves. Altered hippocampal, and specifically dentate gyrus (DG), structure and function may be involved in depression development. However, hippocampal abnormalities could also be a consequence of the disease. For the first time, we tested whether abnormal DG micro- and macrostructure were present in offspring of individuals with MDD and whether these abnormalities predicted future symptomatology. METHODS: We measured the mean diffusivity of gray matter, a measure of microstructure, via diffusion tensor imaging and volume of the DG via structural magnetic resonance imaging in 102 generation 2 and generation 3 offspring at high and low risk for depression, defined by the presence or absence, respectively, of moderate to severe MDD in generation 1. Prior, current, and future depressive symptoms were tested for association with hippocampal structure. RESULTS: DG mean diffusivity was higher in individuals at high risk for depression, regardless of a lifetime history of MDD. While DG mean diffusivity was not associated with past or current depressive symptoms, higher mean diffusivity predicted higher symptom scores 8 years later. DG microstructure partially mediated the association between risk and future symptoms. DG volume was smaller in high-risk generation 2 but not in high-risk generation 3. CONCLUSIONS: Together, these findings suggest that the DG has a role in the development of depression. Furthermore, DG microstructure, more than macrostructure, is a sensitive risk marker for depression and partially mediates future depressive symptoms.


Subject(s)
Depressive Disorder, Major , Dentate Gyrus , Depression , Diffusion Tensor Imaging , Genetic Predisposition to Disease , Humans
12.
Soc Cogn Affect Neurosci ; 15(8): 889-903, 2020 10 08.
Article in English | MEDLINE | ID: mdl-33031555

ABSTRACT

Social behavior is transmitted cross-generationally through coordinated behavior within attachment bonds. Parental depression and poor parental care are major risks for disruptions of such coordination and are associated with offspring's psychopathology and interpersonal dysfunction. Given the key role of the cortico-basal ganglia (CBG) circuits in social communication, we examined similarities (concordance) of parent-offspring CBG white matter (WM) connections and how parental history of major depressive disorder (MDD) and early parental care moderate these similarities. We imaged 44 parent-offspring dyads and investigated WM connections between basal-ganglia seeds and selected regions in temporal cortex using diffusion tensor imaging (DTI) tractography. We found significant concordance in parent-offspring strength of CBG WM connections, moderated by parental lifetime-MDD and care. The results showed diminished neural concordance among dyads with a depressed parent and that better parental care predicted greater concordance, which also provided a protective buffer against attenuated concordance among dyads with a depressed parent. Our findings provide the first neurobiological evidence of concordance between parents-offspring in WM tracts and that concordance is diminished in families where parents have lifetime-MDD. This disruption may be a risk factor for intergenerational transmission of psychopathology. Findings emphasize the long-term role of early caregiving in shaping the neural concordance among at-risk and affected dyads.


Subject(s)
Basal Ganglia/diagnostic imaging , Cerebral Cortex/diagnostic imaging , Child of Impaired Parents , Depressive Disorder, Major/psychology , Parent-Child Relations , White Matter/diagnostic imaging , Adolescent , Adult , Child , Depressive Disorder, Major/diagnostic imaging , Diffusion Tensor Imaging , Female , Humans , Male , Middle Aged , Neural Pathways/diagnostic imaging , Risk Factors , Young Adult
13.
Front Genet ; 11: 724, 2020.
Article in English | MEDLINE | ID: mdl-32765586

ABSTRACT

Attention-deficit hyperactivity disorder (ADHD) is among the most commonly diagnosed psychiatric disorders of childhood. The dopaminergic system has been shown to have substantial effects on its etiology, with both functional Catechol-O-methyltransferase (COMT) Val158Met genotype and early-life environmental adversity involved in the risk of inattention and hyperactivity/impulsivity symptoms. In this prospective longitudinal study, we examined for the first time the impact of proximal and distal early-life family adversity and COMT Val158Met polymorphism gene - both the direct and the interactive effects, on children's ADHD symptoms across childhood. Data came from the Family Life Project, a prospective longitudinal study of 1,292 children and families in high poverty from birth to 11 years. In infancy, data regarding socioeconomic (SES)-risk-factors, observed-caregiving behaviors, and DNA genotyping were collected. In early and middle childhood teachers rated the occurrence and severity of the child's ADHD symptoms. Multilevel growth curve models revealed independent effects of COMT, early-life SES-risk and negative caregiving on ADHD symptoms in early and middle childhood. Significant gene-environment interactions were found, indicating that overall, carriers of at least one COMT158Met allele were more sensitive to early-life adversity, showing higher inattention and hyperactivity/impulsivity symptoms severity in childhood when exposed to high SES-risk factors in infancy, compared to Val-Val carriers. Findings provide new insights into the complex etiology of ADHD and underline the need for further investigation of the neuronal mechanisms underlying gene-environment interactions. Findings might have implications for prevention and intervention strategies with a focus on early-life family relationships in genetically at-risk children.

14.
Int J Psychophysiol ; 136: 39-48, 2019 02.
Article in English | MEDLINE | ID: mdl-29486216

ABSTRACT

Interoception, the perception and interpretation of one's own bodily signals, is a key aspect of human caregiving that impacts infant health and well-being across life. Interoception relies on limbic structures, mainly the amygdala, and the agranular visceromotor cortex, particularly the anterior insula (AI), that integrate with the oxytocin (OT) system to support interoceptive sensitivity. Here, we used functional magnetic resonance imaging (fMRI) to examine whether interoception sensitivity in the parent's brain during the first months of parenting combines with sensitive parenting and OT-system functionality to predict children's somatic symptoms six years later. We followed 45 primary-caregiving first-time mothers and fathers and their infants across the first six years of parenting. In infancy (Time 1), parents' brain response to infant stimuli was imaged, salivary OT measured, and parent-infant interactions coded for parent sensitivity. In preschool (Time 2), parent and child's OT and parent sensitivity were measured again. At six years (Time 3), parents reported on children's somatic symptoms. Greater activation of the parent's AI bilaterally when his/her child was an infant predicted lower child somatic problems at six years. Parent sensitivity partially mediated the links between parental AI activation and child somatic symptoms. In addition, greater parental bilateral amygdala activity predicted higher child OT levels at 3 years and parental OT moderated the relations between preschoolers' OT and later somatic symptoms. Our findings chart two independent cross-generational pathways from interoception sensitivity in the parent's brain and child somatization. The first defines an evolutionary-ancient path including the amygdala and the OT system that support mammalian attention to arousal modulations in response to social cues; the second, via the AI, implicates higher-order interoceptive representations of bodily responses and affective states that underpins human embodiment.


Subject(s)
Amygdala/physiology , Cerebral Cortex/physiology , Interoception/physiology , Maternal Behavior/physiology , Medically Unexplained Symptoms , Oxytocin/metabolism , Parent-Child Relations , Paternal Behavior/physiology , Adult , Amygdala/diagnostic imaging , Cerebral Cortex/diagnostic imaging , Child , Child, Preschool , Female , Follow-Up Studies , Humans , Infant , Magnetic Resonance Imaging , Male , Parenting , Saliva
15.
Physiol Behav ; 193(Pt A): 25-34, 2018 09 01.
Article in English | MEDLINE | ID: mdl-29730038

ABSTRACT

Allomothering, the caregiving to offspring by adults other than the biological mother including fathers and other group members, has characterized human societies throughout hominin evolution. Allomothering is common across the animal kingdom and carries long-term fitness benefits to offspring. Guided by our biobehavioral synchrony conceptual frame, we present research from our lab and others addressing the behavioral, hormonal, and neural systems that underpin human allomaternal care by fathers and studies on the coparental bond. Several important aspects of human allomothering are discussed: (i) father-child synchrony, (ii) longitudinal effects of fathering and coparenting on child outcomes (iii) cultural variability in paternal care, (iv) the role of oxytocin, vasopressin, prolactin, and testosterone in the formation and maintenance of human fathering, (v) evolutionary changes in fathers' brains within the parent-offspring interface and their contribution to children's long-term social adaptation, and (vi) the neural correlates of human coparenting. Based on our findings we propose that in the course of hominin evolution fathers' neuroendocrine systems, brain functionality and integrity, and behavioral responses to infant cues have undergone profound natural selection to accommodate the great variability in the paternal role across time and place, culminating in the contemporary cooperative, highly involved coparent observed in modern societies of the developed world.


Subject(s)
Brain/physiology , Child Development/physiology , Parenting , Paternal Behavior/physiology , Social Behavior , Animals , Child , Female , Humans , Male , Maternal Behavior/physiology , Maternal Behavior/psychology , Neurosecretory Systems/metabolism , Paternal Behavior/psychology
16.
Neuropsychologia ; 116(Pt A): 75-85, 2018 07 31.
Article in English | MEDLINE | ID: mdl-28412510

ABSTRACT

Parental empathy is a key component of sensitive parenting that supports children's social adaptation throughout life. Consistent with a two dissociable network perspective on empathy, we measured within- and between-network integrity of two empathy-related networks in the parental brain as predictors of children's social outcomes across the first six years of life. We focused on two empathy networks; embodied simulation, which supports parents' capacity to resonate with infant state and emotions and implicates cingulo-insulary structures, and mentalizing, which underpins parents' theory-of-mind and mental attributions via prefrontal-temporo-parietal circuit. We followed 87 first-time parents across the first six years of family formation, including heterosexual and homosexual parents. In infancy, parents' brain response to own versus unfamiliar infant stimuli was imaged; in preschool, children's cortisol production and emotion regulation were assessed; and at six years, children's behavior problems were reported. Parents' intra- and inter- network integrity increased when viewing their own infant compared to unfamiliar infant, suggesting that attachment stimuli increase network coherence in the parental brain. Functional connectivity within the parent's embodied simulation network in infancy predicted lower child cortisol production while inter-network connectivity among the embodied simulation and mentalizing networks was associated with more advanced child emotion regulation skills in preschool and lower internalizing problems at six years. Children's emotion regulation capacities mediated the link between inter-network integrity in the parental brain and internalizing symptoms. Our findings, the first to demonstrate that integrity of empathy-related networks in the parental brain shape children's long-term stress reactivity and emotional adaptation, highlight the brain component of the parental empathy attribute, suggest that increased coherence within the "parental caregiving network" marks a key feature of parent-infant attachment, and contribute to discussion on biobehavioral mechanisms underpinning the cross-generation transmission of human stress reactivity and sociality.


Subject(s)
Adaptation, Psychological/physiology , Cerebral Cortex/physiology , Empathy , Parent-Child Relations , Parenting , Stress, Psychological/physiopathology , Cerebral Cortex/diagnostic imaging , Female , Humans , Hydrocortisone/metabolism , Image Processing, Computer-Assisted , Infant , Magnetic Resonance Imaging , Male , Neural Pathways/diagnostic imaging , Oxygen/blood , Saliva/chemistry , Self Report , Theory of Mind
17.
Neuropsychopharmacology ; 42(12): 2301-2313, 2017 Nov.
Article in English | MEDLINE | ID: mdl-28401924

ABSTRACT

Alloparental care, the cooperative care of offspring by group members other than the biological mother, has been widely practiced since early hominin evolution to increase infant survival and thriving. The coparental bond-a relationship of solidarity and commitment between two adults who join their effort to care for children-is a central contributor to children's well-being and sociality; yet, the neural basis of coparenting has not been studied in humans. Here, we followed 84 first-time co-parents (42 couples) across the first 6 years of family formation, including opposite-sex and same-sex couples, measured brain response to coparental stimuli, observed collaborative and undermining coparental behaviors in infancy and preschool, assayed oxytocin (OT) and vasopressin (AVP), and measured coparenting and child behavior problems at 6 years. Across family types, coparental stimuli activated the striatum, specifically the ventral striatum and caudate, striatal nodes implicated in motivational goal-directed social behavior. Psychophysiological interaction analysis indicated that both nodes were functionally coupled with the vmPFC in support of the human coparental bond and this connectivity was stronger as collaborative coparental behavior increased. Furthermore, caudate functional connectivity patterns differentiated distinct corticostriatal pathways associated with two stable coparental behavioral styles; stronger caudate-vmPFC connectivity was associated with more collaborative coparenting and was linked to OT, whereas a stronger caudate-dACC connectivity was associated with increase in undermining coparenting and was related to AVP. Finally, dyadic path-analysis model indicated that the parental caudate-vmPFC connectivity in infancy predicted lower child externalizing symptoms at 6 years as mediated by collaborative coparenting in preschool. Findings indicate that the coparental bond is underpinned by striatal activations and corticostriatal connectivity similar to other human affiliative bonds; highlight specific corticostriatal pathways as defining distinct coparental orientations that underpin family life; chart brain-hormone-behavior constellations for the mature, child-orientated coparental bond; and demonstrate the flexibility of this bond across family constellations and its unique contribution to child well-being.


Subject(s)
Cerebral Cortex/diagnostic imaging , Child Welfare/psychology , Corpus Striatum/diagnostic imaging , Family/psychology , Object Attachment , Parenting/psychology , Adult , Child , Child Welfare/trends , Child, Preschool , Female , Humans , Infant , Longitudinal Studies , Magnetic Resonance Imaging/trends , Male , Neural Pathways/diagnostic imaging , Parent-Child Relations , Parenting/trends , Spouses/psychology
18.
Soc Cogn Affect Neurosci ; 11(11): 1707-1718, 2016 11.
Article in English | MEDLINE | ID: mdl-27369068

ABSTRACT

The cross-generational transmission of mammalian sociality, initiated by the parent's postpartum brain plasticity and species-typical behavior that buttress offspring's socialization, has not been studied in humans. In this longitudinal study, we measured brain response of 45 primary-caregiving parents to their infant's stimuli, observed parent-infant interactions, and assayed parental oxytocin (OT). Intra- and inter-network connectivity were computed in three main networks of the human parental brain: core limbic, embodied simulation and mentalizing. During preschool, two key child social competencies were observed: emotion regulation and socialization. Parent's network integrity in infancy predicted preschoolers' social outcomes, with subcortical and cortical network integrity foreshadowing simple evolutionary-based regulatory tactics vs complex self-regulatory strategies and advanced socialization. Parent-infant synchrony mediated the links between connectivity of the parent's embodied simulation network and preschoolers' ability to use cognitive/executive emotion regulation strategies, highlighting the inherently dyadic nature of this network and its long-term effects on tuning young to social life. Parent's inter-network core limbic-embodied simulation connectivity predicted children's OT as moderated by parental OT. Findings challenge solipsistic neuroscience perspectives by demonstrating how the parent-offspring interface enables the brain of one human to profoundly impact long-term adaptation of another.


Subject(s)
Brain/physiology , Nerve Net/physiology , Neuronal Plasticity/physiology , Oxytocin/blood , Parent-Child Relations , Self-Control/psychology , Social Skills , Socialization , Theory of Mind/physiology , Brain Mapping , Child , Child, Preschool , Emotional Intelligence , Female , Humans , Infant , Infant, Newborn , Male
19.
Proc Natl Acad Sci U S A ; 111(27): 9792-7, 2014 Jul 08.
Article in English | MEDLINE | ID: mdl-24912146

ABSTRACT

Although contemporary socio-cultural changes dramatically increased fathers' involvement in childrearing, little is known about the brain basis of human fatherhood, its comparability with the maternal brain, and its sensitivity to caregiving experiences. We measured parental brain response to infant stimuli using functional MRI, oxytocin, and parenting behavior in three groups of parents (n = 89) raising their firstborn infant: heterosexual primary-caregiving mothers (PC-Mothers), heterosexual secondary-caregiving fathers (SC-Fathers), and primary-caregiving homosexual fathers (PC-Fathers) rearing infants without maternal involvement. Results revealed that parenting implemented a global "parental caregiving" neural network, mainly consistent across parents, which integrated functioning of two systems: the emotional processing network including subcortical and paralimbic structures associated with vigilance, salience, reward, and motivation, and mentalizing network involving frontopolar-medial-prefrontal and temporo-parietal circuits implicated in social understanding and cognitive empathy. These networks work in concert to imbue infant care with emotional salience, attune with the infant state, and plan adequate parenting. PC-Mothers showed greater activation in emotion processing structures, correlated with oxytocin and parent-infant synchrony, whereas SC-Fathers displayed greater activation in cortical circuits, associated with oxytocin and parenting. PC-Fathers exhibited high amygdala activation similar to PC-Mothers, alongside high activation of superior temporal sulcus (STS) comparable to SC-Fathers, and functional connectivity between amygdala and STS. Among all fathers, time spent in direct childcare was linked with the degree of amygdala-STS connectivity. Findings underscore the common neural basis of maternal and paternal care, chart brain-hormone-behavior pathways that support parenthood, and specify mechanisms of brain malleability with caregiving experiences in human fathers.


Subject(s)
Brain/physiology , Father-Child Relations , Fathers , Emotions , Humans , Male , Sexual Behavior
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