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In contrast, the STS is a central region of the mentalizing network, playing a vital role in social cognition, biological motion, social goal interpretation, prediction making, and updating regarding others' behavior 28 , Thus, in addition to much commonality, somewhat different pathways seem to underpin maternal and paternal caregiving. The first, an evolutionary ancient path, operates via immediate fight-or-flight responses, danger signals, and motivational salience; the latter relies on later-evolving structures and implements circuits affording third person perspective and future planning 14 , These different pathways were demonstrated by the structural model, which showed that STS in all fathers had a direct path to parent—infant synchrony, as well as a mediated path via increases in oxytocin.

The comparable amygdala response in mothers and primary-caregiving fathers indicates the potential to activate the evolutionary ancient pathway when fathers raise infants without mothers, demonstrating amygdala sensitivity to the primary-caregiving role. These findings are consistent with animal studies showing influences on c-fos expressions in the amygdala in sexually naive male prairie voles following pup exposure Although functional amygdala—STS connectivity was observed only in primary-caregiving fathers, among all fathers, the overlap between the two structures correlated with the father's direct caregiving experiences.

These findings coincide with biparental animals' greater integration of multiple brain networks 7. Both the amygdala and STS are key structures of the social brain circuitry 15 , 31 , The STS plays a key role in social perception 33 , and STS projections to the amygdala determine its role in mentalizing and social perception processes 28 , The STS sends feed-forward projections to the amygdala and receives feedback projections from it 29 , with the amygdala fine-tuning neural response to affect-laden stimuli Stronger amygdala—STS connectivity has been linked with better social cue detection 32 , and amygdala-damaged patients revealed lower STS response to affective facial expressions Individuals with larger, more complex social networks showed stronger amygdala—STS connectivity, suggesting greater adeptness at initiating and maintaining social bonds Our findings suggest that this interconnected social perception network, indexed by amygdala—STS connectivity, may underpin a flexible and generalized form of nurturance that is not dependent on pregnancy and childbirth but on caregiving experiences.

Results of the current structural model indicate that the primary-caregiving role directly affected amygdala response in mothers and fathers, but amygdala effects on behavior were observed only in mothers. In contrast, the STS, which activated all fathers' responses to infant cues, had both a direct effect on synchrony and mediated effects via oxytocin, which has been repeatedly shown to support the development of synchronous parenting 5 , 20 , Oxytocin administration has been shown to increase STS response to tasks that require mentalizing Thus, our model charts two pathways of brain—hormone—behavior in first-time parents: one mediated by the amygdala for mothers and the other by the STS for fathers.

In addition, the model charts both direct and oxytocin-mediated paths between STS and synchrony in fathers. The interconnectedness between the amygdala and STS suggests that these two paths are interrelated and open to bidirectional effects. This assumption is consistent with recent imaging studies, which showed no differences in response to the attachment target between homosexual and heterosexual men 37 , and with our finding that homosexual and heterosexual fathers did not differ in their masculinity and femininity scores.

Findings for all fathers that degree of amygdala—STS connectivity was associated with the amount of direct childcare responsibility further supports the hypothesis that our results describe human fathers' brain adaptation to caregiving activities. However, it must be remembered that only a handful of studies examined the brain basis of human fatherhood, and research in this area requires much further investment.

Future research should continue to explore similarities and differences in the maternal and paternal brain; describe how mothers' and fathers' brains evolved to complement each other in the joint effort of raising young infants; and test how the forces that redefine the human family function to reorganize the human social brain. Current sociocultural and technological advances are already assembling new families, workplaces, and social networks.

Such novel social bonds will likely create a new interplay between the consistencies of the human social brain and the malleabilities resulting from unique contextual requirements, role definitions, cultural beliefs, and individual life histories. Much further research and conceptual effort is required to understand how these profound and rapid social changes shape brain, behavior, social relationships, the capacity for nurturance, and the larger social climate in which we live.

A total of 89 first-time parents raising their infant within partnered relationships participated [mean age, Data of two fathers one in SC-Fathers and one in PC-Fathers group were excluded from brain analyses due to strong movement artifacts. Participants were compensated for their time and gave written informed consent. The study included two sessions with each family.

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In the first session, families were visited at home between and PM to control for diurnal variability in oxytocin. After familiarization, salivary samples were collected for oxytocin, and each parent was interviewed and completed self-report measures. Next, each parent was videotaped interacting with the infant.

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Experimenters ascertained that infants were calm during videotaping; when infants were fussy, visits were rescheduled. Finally, we videotaped a 2-min segment of each parent alone and the infant alone during solitary activity in the same natural ecology.

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Parent—infant interaction videos were coded offline for parent—infant synchrony. In the second session, several days after the home visit, each parent underwent functional brain scanning. Saliva samples were collected twice—at baseline and following parent—infant interactions—by sallivette Sarstedt. Recent studies across several laboratories showed that salivary oxytocin measured by immunoassay is a reliable biomarker, stable over time, and correlates with oxytocin-related processes like breastfeeding.

Measurements were performed in duplicate and calculated using MatLab-7 according to relevant standard curves. The average of the two assessments was used.

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  • This global rating system for adult—child interactions includes 42 scales, which aggregate into theoretically meaningful constructs. The CIB is well-validated showing good psychometric properties We used the eight-scale CIB parent—infant synchrony construct to index the central behavioral expression of attuned human caregiving. Coding was conducted by trained raters who were blind to parent group. Imaging was performed on a GE-3T Sigma Horizon echo-speed scanner with a resonant gradient echoplanar imaging system. After standard preprocessing SI Materials and Methods , statistical maps were prepared for each participant using a general linear model GLM , in which the various blocks were defined as district predictors.

    Single-participant analysis was followed by multiparticipant analysis computed with random effects using a gray matter mask. To account for hemodynamic responses, predictors were convolved with a 6-s hemodynamic response filter for all participants. ROI analysis was conducted on the brain areas identified by the whole-brain GLM conjunction analysis and previous research as components of the parental caregiving neural network Table S4.

    Specifically, for each region, a box-shaped volume of five voxel diameter was placed around the peak of activation SI Materials and Methods. To analyze functional connectivity between amygdala and STS, we defined ROIs functionally and anatomically using the WFU Pick Atlas Tool 40 , placing a box-shaped volume of five voxel diameter around the activation peak. The signal was extracted from all ROIs, and a set of all pairwise Pearson correlation values was calculated for each participant and condition, incorporating a hemodynamic delay of two repetition times.

    After Fisher Z transformation, two-tailed t statistics were computed to compare conditions. Author contributions: E.

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    Skip to main content. Eyal Abraham. Significance Brain, oxytocin, and parenting behavior were measured in primary-caregiving mothers, secondary-caregiving fathers, and primary-caregiving homosexual fathers raising infants without maternal involvement. 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. Results Coinciding with ethological perspectives, we first examined differences in parenting behavior.

    Discussion The current study provides compelling evidence for brain malleability with caregiving experiences in human fathers and describes one mechanism underpinning this malleability. Materials and Methods Participants. Parenting Behavior. Interregional Functional Connectivity Analysis.

    The authors declare no conflict of interest. See Commentary on page Freely available online through the PNAS open access option. Psychol Bull 1 : 55 — Wynne-Edwards KE Hormonal changes in mammalian fathers. Horm Behav 40 2 : — Biol Psychiatry 68 4 : — Attach Hum Dev 15 4 : — Lambert KG , et al. Brain Behav Evol 77 3 : — Nat Neurosci 9 9 : — Nat Rev Neurosci 2 2 : — Endocrinology 5 : — Atzil S , Hendler T , Feldman R Specifying the neurobiological basis of human attachment: Brain, hormones, and behavior in synchronous and intrusive mothers.

    Neuropsychopharmacology 36 13 : — Biol Psychiatry 56 4 : — Barrett J , Fleming AS Annual Research Review: All mothers are not created equal: neural and psychobiological perspectives on mothering and the importance of individual differences. J Child Psychol Psychiatry 52 4 : — Behav Brain Sci 35 3 : — Neuron 50 4 : — Soc Cogn Affect Neurosci doi: OpenUrl CrossRef. Biol Psychol 91 2 : — Carter CS Oxytocin pathways and the evolution of human behavior.

    Annu Rev Psychol 65 : 17 — Feldman R Oxytocin and social affiliation in humans. Horm Behav 61 3 : — Feldman R , et al. Biol Psychiatry 72 3 : — Neuroscience 4 : — Behav Neurosci 5 : — Bem SL The measurement of psychological androgyny. J Consult Clin Psychol 42 2 : — Fleming AS , Korsmit M Plasticity in the maternal circuit: Effects of maternal experience on Fos-Lir in hypothalamic, limbic, and cortical structures in the postpartum rat. Behav Neurosci 3 : — J Cogn Neurosci 20 12 : — Trends Cogn Sci 4 7 : — Nature : — J Neurosci 32 42 : — Pelphrey KA , Morris JP , McCarthy G Grasping the intentions of others: The perceived intentionality of an action influences activity in the superior temporal sulcus during social perception.

    J Cogn Neurosci 16 10 : — Nat Neurosci 7 11 : — Gordon I , et al. Zeki S , Romaya JP The brain reaction to viewing faces of opposite- and same-sex romantic partners. The birdsong example demonstrates how hormones can affect behavior, but as noted, the reciprocal relation also occurs; that is, behavior can affect hormone concentrations. For example, the sight of a territorial intruder may elevate blood testosterone concentrations in resident male birds and thereby stimulate singing or fighting behavior.

    Similarly, male mice or rhesus monkeys that lose a fight decrease circulating testosterone concentrations for several days or even weeks afterward. Comparable results have also been reported in humans. Testosterone concentrations are affected not only in humans involved in physical combat, but also in those involved in simulated battles. For example, testosterone concentrations were elevated in winners and reduced in losers of regional chess tournaments. Male fans of both the Brazilian and Italian teams were recruited to provide saliva samples to be assayed for testosterone before and after the final game of the World Cup soccer match in Brazil and Italy were tied going into the final game, but Brazil won on a penalty kick at the last possible moment.

    The Brazilian fans were elated and the Italian fans were crestfallen. When the samples were assayed, 11 of 12 Brazilian fans who were sampled had increased testosterone concentrations, and 9 of 9 Italian fans had decreased testosterone concentrations, compared with pre-game baseline values Dabbs, For example, testosterone concentrations also influence sexual motivation and behavior in women. On three separate occasions, women provided a pre-activity, post-activity, and next-morning saliva sample.

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    Thus, an anticipatory relationship exists between sexual behavior and testosterone. Testosterone values were higher post-intercourse compared to exercise, suggesting that engaging in sexual behavior may also influence hormone concentrations in women. Hens and roosters are different. Cows and bulls are different. Men and women are different. Even girls and boys are different. The behavior of boys and girls differs in many ways. Girls generally excel in verbal abilities relative to boys; boys are nearly twice as likely as girls to suffer from dyslexia reading difficulties and stuttering and nearly 4 times more likely to suffer from autism.

    Boys are generally better than girls at tasks that require visuospatial abilities. Girls engage in nurturing behaviors more frequently than boys. Young men are twice as likely as young women to suffer from schizophrenia.