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Psychiatry and Psychology Bokulić E, Mikulec S. How a new father’s brain changes. pp. 107 – 111 How a New Father’s Brain Changes Ema Bokulić University of Zagreb, School of Medicine 0000-0002-5732-7560 Sonja Mikulec University of Zagreb, School of Medicine 0000-0002-6192-1554 Abstract

The specificity of human species is prolonged care for their infants which involves parents of both sexes. Fathers provide ‘stimulatory’ contact to their infants making them explore their surrounding and become more independent, unlike mothers who provide nurture and affectionate care. Neuroimaging studies suggest that paternal care is associ- ated with higher activity in cortical structures that are a part of the social brain - empathy, mentalizing and executive network (cognitive control) and mirror neuron system. Behavioural changes mediated by various hormones also serve as an adaptation to the new role of being a father. , and altogether help fathers to establish an emotional bond with their infant, directing their efforts towards paternal childcare, ensuring that the infant gets the best possible environment for growth and development. To support this, the mating effort of fathers decreases, along with responses to sexually provocative stimuli. However, these studies should be reproduced on a Keylargerwor sampleds: and should consider complex interactions between hormones and neurotransmitters.

hormones, mating effort, neuroimaging, neuroplasticity, parental behaviour, paternal behaviour, THE ROLE OF social FATHERS brain IN HUMAN SPECIES

neuron system (inferior parental lobule (IPL), inferior (frontal (IFG) and supplementary motor area (SMA)), Human infants are, among all other species in the animal mentalizing network (/gyrus kingdom, the ones in need of nurture for the longest STS/STG), precuneus, posterior cingulate cortex (PCC), time. At birth, the size of their brain marks only 25% temporoparietal junction (TPJ), ventromedial prefrontal of the adult brain1, which is one of the crucial reasons cortex (vmPFC), and emotion regulation and/or executive for prolonged parental care needed for human infants network/cognitive control (frontopolar cortex, dorso- to develop. One special characteristic of parenthood in lateral (dlPFC), medial orbitofrontal human species is that fathers are present from the birth cortex (mOFC), middle frontal gyrus (MFG)). All of the of the child and long after in childhood and adolescence. aforementioned brain regions are a part of overlapping1 Moreover, studies have shown that parenting „styles“ cortical networks that constitute the ‘social’ brain. differ between sexes. Mothers are the ones who provide nurture and affectionate care, while fathers are involved Becoming a parent requires adaptation to certain novel- in stimulatory contact – they ‘stimulate’ their infants to ties in life – forming a parent-infant bond and changes explore the external world and get more independent. in relationship dynamics between both parents, just to Both parents are needed to protect the child from the name a few. This adaptation is possible because of the harsh environment and raise him into a 1,2,3human being neuroplasticity of the brain, which 1,2,3 includes remodelling capable of surviving in the outside world. of different pathways within. Some researchers even NEUROIMAGING STUDIES AND NEUROPLASTICITY hypothesize that it was the specific parental caregiving of our species in particular which gave rise to the evo- lution of the social brain, not vice versa. 1 Studies have shown that mothers display more activity in subcortical When it comes to neuroimaging studies on the brains structures, which indicates that this is an evolutionarily of fathers, there is not a sufficient amount of available conserved salience-vigilance pathway. Also, it is believed material to make clear-cut conclusions; the results only1,2,3 that subcortical structures are sensitized by outline a picture yet to be upgraded by future research. hormones. On the other hand, fathers, unlike most of The research mostly focuses on testing responses of par- the mothers, displayed activity in the mirror network, ents’ brains to different modalities (visual, auditory or which indicates that paternal pathway is based on corti- multimodal) of infant stimuli (‘own infant’ versus control cal networks involved in perceptual-motor coupling and1 condition) using fMRI. The results reveal the existence of representation of the infant’s state in the parent’s brain. a global ‘parental caregiving’ network (Figure 1.) which Besides, there is a difference in functional connectivity involves structures involved in empathy network (anterior between mothers and fathers. A research conducted on insula (AI) and anterior cingulate cortex (ACC)), mirror mothers and homosexual men as primary caregivers and 107 Gyrus

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Psychiatry and Psychology Bokulić E, Mikulec S. How a new father’s brain changes. pp. 107 – 111

Figure 1. Source: Feldman R.The The human adaptive parental human caregiving parental brain: network. implications for children’s social development. Trends Neurosci. 2015;38(6):387-399. doi:10.1016/j.tins.2015.04.004. Copyright © 2015 Elsevier Ltd. All rights reserved.

fathers as secondary caregivers showed that, in mothers, Moreover, a study was conducted to examine whether there (there is high activation of , whereas in secondary- is activity present in the same brain regions of parents caregiving fathers high activity of superior temporal sulcus of both sexes as a reaction to their own infant. Indeed, STS) was present. However, in primary-caregiving fathers the shared activity was present in the right insula, which there was high activity of both amygdala and STS, thus was functionally connected to regions of the ‘social brain’ suggesting that the paternal brain activates maternal – ACC, motor and premotor areas, IFG, IPL and mPFC, which pathways to1 increase infant survival in the absence of are a part of the mirror and mentalizing network. This the mother. Furthermore, the paternal caregiving system suggests that there is a brain-to-brain synchrony, which involves cortical structures, whereas maternal caregiving most probably had an important1,2 role in the evolution of pathways rely more on subcortical reward and vigilance the biparental human family. structures and regions1 involved in empathy, mirror and mentalizing networks. The cortical structures involved in Furthermore, it is considered that one of the important father-infant interaction imply that this is an evolutionarily mechanisms of plasticity is brain-to-brain synchrony younger system than the1,2 one in mothers, which involves between parents of both sexes. In addition, in a research subcortical structures. using fMRI in parents of both sexes as a reaction to the same (own) infant1,2 coordinated changes in BOLD signal were observed.

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Psychiatry and Psychology Bokulić E, Mikulec S. How a new father’s brain changes. pp. 107 – 111

Neuroplasticity of the brain is also quantified by looking at Increased OT in fathers could support5 the same neural the changes in volume in certain brain regions. In fathers, circuit, resulting in engaged childcare. the evidence of these changes was found as an increase in grey matter in amygdala, striatum, , The third hypothesis explains these changes as a way of subgenual cortex, lateral PFC and STG. A decrease in grey1,2 channelling men’s energy and abilities toward parenting matter was found in OFC, PCC, fusiform gyrus and insula. and away form mating. It is well researched that high The interpretation of these results is that the decrease T levels predict divorce and are negatively correlated in the aforementioned brain regions, which are a part of with 5relationship quality, whilst low T causes low li- default mode network, indicates a shift of resources to bido. Intranasal OT administration diminishes interest other regions, for example lateral OFC and striatum, in this2 in approaching unknown, attractive women in partnered way making possible focus and adaptation to parenting. men. Altogether, this evidence supports the thesis that However, future studies are needed to clarify how long hormonal changes modify the neural feedback to sexually these changes maintain and whether there are changes provocative stimuli, facilitating5 caregiving behaviour and in other structures according to2 the level of involvement reducing mating efforts. of the father in the child’s life. 1. Oxytocin Neuroimaging studies comparing activity of brain regions Oxytocin is produced in both brain and body and for with levels of oxytocin showed that decreases in plasma scientific6 purposes its plasma levels are usually meas- OT in fathers were correlated to activity in cognitive ar- ured. In humans, oxytocin is found to have a significant eas responsible for regulating and organizing behavioral impact on behaviour, forming7 bonds with your significant responses to emotional salient stimuli4 (dorsolateral PFC, other, children and friends. A research in which baseline dorsal ACC, IPC and precentral gyrus). and postpartum oxytocin levels were measured on both mothers and fathers showed that in both sexes there was Furthermore, a study measuring parents’ response to an increase in OT across the post-partum 6 months time infant cues showed a correlation between an increase in interval. (6) It is considered that6,7 a rise in oxytocin levels arginine level (AVP) and activity of inferior mediates parental motivation. frontal gyrus and insula in father, but not in mothers. These findings suggest that there is an increased social-cognitive4 In another study, plasma and salivary oxytocin levels were response to infant cues specific to fathers. measured before and after 15 min of „play and touch“ inter- HORMONES AND THEIR INFLUENCE ON FATHER’S action of fathers and mothers, respectively, with their 4-6 BRAIN months old infant. The results showed that the fathers with higher baseline oxytocin showed more stimulatory contact and their oxytocin levels had risen after the interaction,6 unlike the fathers that showed low stimulatory contact. Recent research shows strong evidence that hormonal On the other hand, mothers that had higher levels of OT changes play an important role in establishing and main- were more involved in affectionate contact and their OT taining paternal childcare. It is, however, still unclear levels also had risen after the interaction. This shows there how these changes in hormone levels, especially those are differences between parent-infant interaction styles of testosterone (T) and oxytocin (OT), affect neural path- and implies6 that both styles are influenced by oxytocin ways responsible for emotional and behavioural states levels. Furthermore, certain studies showed that, when which promote successful childcare. Three hypotheses both parents had high levels of plasma oxytocin, they also have been discussed. displayed higher levels of triadic synchrony6 and more sensitive and responsive parenting. One hypothesis says that these changes increase empathic responding to children’s cues, resulting in positive out- In one study, the behaviour of fathers after intranasal comes for a child. Increased OT levels and decreased T oxytocin administration was evaluated during play session could promote such response. For example, intranasal OT with their toddlers. The fathers showed greater support treatment leads fathers to engage more in social activities in learning and exploring in regard of child’s autonomy6 with their children, while high T levels correspond with and less hostility when compared with placebo condition. less sympathy in response to infant cries, exhibiting5 less affection and less involvement in parental care. 2. Testosterone One generally connects testosterone – the male sex hor- The second hypothesis proposes that these changes mone – with reproductive behaviour such as seeking new strengthen paternal caregiving by augmenting the reward mates and sexual activity (both traits being characterized value of child stimuli. This hypothesis is based upon the by high T levels). On the contrary, parenting activities and fact that the ventromedial prefrontal cortex (vmPFC/ child caregiving are connected with lower T levels. One OFC) is involved in reward processing and OFC mediates study observed neural responses of fathers to video clips responses to children’s faces. Furthermore, research car- of their infants, a sex-, age- and ethnicity-matched other ried out on nulliparous women showed that intranasal OT infant and a Raggedy Andy doll presented in random order. (administration acts at the ventral tegmental area (VTA) Additionally, saliva samples for testosterone were taken to promote secretion in before and after interaction with the infant. After analysing NA), thus enhancing the reward value of social stimuli. fMRI data, the results showed that videos of their own ba- 109 Gyrus

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Psychiatry and Psychology Bokulić E, Mikulec S. How a new father’s brain changes. pp. 107 – 111 bies activated a wide network of prefrontal and subcortical However, higher baseline PRL couldn’t predict who will regions in the fathers’ brains when compared to videos of become a father by the time of the follow-up, 4.5 years the doll. Moreover, these regions were significantly more later. The most surprising result was that non-fathers with activated by viewing videos of their own when compared higher PRL had more lifetime sexual partners and more to videos of other infants. There was also an infant-related sexual activity, in contrast to the fact that PRL promotes11 activation in OFC of fathers, supporting the fact that this nurturing behaviour and suppresses mating effort. part of the brain is important for reward processing and emotions, especially for following and comprehending 4. changing emotions. Interestingly, this experiment found The role of cortisol in mediating parental behaviour that fathers with higher T levels after interacting with was discovered when scientists investigated maternal their infants expressed stronger activation to clips of responsiveness to infant’s cues. According to these recent their own than to clips of other infants. This result leads studies, the birth of a child induces adrenal activation to a conclusion that there could be a positive correlation which may be a good predictor of responsiveness to between T and neural response to infant’s cues, contrary infant’s cues. High levels of circulating cortisol correlate to results of previous experiments. A possible explanation with mother’s positive behaviour towards her infant. One is that testosterone increases promote parental protecting8 can conclude that a certain12 level of arousal is required behaviours, like responses to urgent infant cries. for optimal maternal care.

Another study investigated how personality traits relate Studies conducted on biparental non-human primates to hormones and human behaviour, focusing on sensation- (marmosets and tamarins) showed13 that parity affects seeking (SS) as a personality trait and testosterone as a prolactin and cortisol levels in fathers. Human fathers also hormone. SS behaviour types like gambling, alcohol use exhibit different cortisol and prolactin levels depending and multiple sexual partners are positively correlated with on their parity. First-time fathers and non-fathers have T levels in men. Considering that SS behaviour actually higher cortisol levels after hearing an infant cry, suggesting represents mating effort, which is characterized by high they are more alert and experience greater . This T levels, one can easily establish a connection between indicates a more affective response in inexperienced males. this personality trait and T levels by filling in a simple On the other hand, prolactin levels increase with parity – questionnaire about personality types. The collected data experienced fathers who have two or more children have confirmed previous findings about the role of T in pater- higher prolactin and lower cortisol levels. However, it is nal behaviour. Both lower T levels and9 lower SS promote not clear whether the changes in new fathers’ hormonal12 paternal and caregiving behaviour. profile are infant-induced or do they precede the birth.

Scientists also concluded that T levels change during the transition to fatherhood, when a man is expecting his first child. These endocrinological changes, particularly the decrease of T levels, serve as an adaptation to the CONCLUSION new role of being a father. Along with lower T levels, new fathers felt dissatisfied with their relationships, which was probably due to new responsibilities and nurturing the newborn, consequently spending less quality time These studies were conducted on a relatively with their partner. From the perspective of evolutionary small sample, so one cannot make general con- psychology, an interesting finding is that the decline of T clusions about the influence of hormones on levels was greater in fathers with higher baseline T, pos- male reproductive and parental behaviour before sibly as a means of reducing mating effort and promoting reproducing the studies on a larger sample. Con- nurturing behaviour. These fathers also reported greater tradictory findings could be the result of differ- dissatisfaction with their relationship and intimacy after ent roles male hormones have during different the childbirth, leading to a conclusion that these fathers10 stages in life. Changing behavioural effects that were more sexually active prior to birth of their child. hormones have depending on men’s romantic and parenthood status could be the result of complex 3. Prolactin interactions of hormones and neurotransmitters Prolactin (PRL) has the main role in in the brain which11 still need to be discovered and in women, facilitating and maternal nurturing fully understood. behaviour. Recently carried out study investigated the role of prolactin in male nurturing and sexual behaviour. Men who participated in the study were divided in three groups – ‘cohabitating partnered’, ‘non-cohabitating part- nered’ and ‘non-partnered’. Two other important traits were frequency of sexual activity in the last month and whether they were fathers or not. Participants had their blood taken and serum was used to measure PRL levels. Results have shown that fathers in committed relation- ships had the highest PRL, particularly fathers of infants. Gyrus 110

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Psychiatry and Psychology Bokulić E, Mikulec S. How a new father’s brain changes. pp. 107 – 111 References:

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UčinakSažetak očinstva na promjene u mozgu muškaraca Ljudska se vrsta razlikuje od većine drugih sisavaca po tome što dulje brine za svoje potomke i što su uključeni roditelji oba spola. Očevi su uključeni u ‘stimulatorni’ kontakt, potičući potomke da istražuju okolinu i steknu samostalnost. Neuroimaging studije pokazuju da je očinska briga povezana s većom aktivnošću u kortikalnim strukturama koje su dio ‘socijalnog’ mozga – neuronskim putevima uključenima u empatiju, mentalizaciju i kontrolu kognitivnih procesa te sustavom zrcalnih neurona. Različiti hormoni koreliraju s promjenama u ponašanju koje služe kao prilagodba na novu ulogu oca. Oksitocin, testosteron i prolaktin zajednički pomažu očevima ostvariti emotivnu povezanost s njihovim djetetom. Osim toga, ti hormoni omogućuju potpuno usmjeravanje očeve pažnje na dijete, osiguravajući time najbolju moguću okolinu za rast i razvoj. U prilog toj teoriji govori i činjenica da se zavodničko ponašanje kod očeva smanjuje, kao i odgovor na vidne seksualno provokativne podražaje. Unatoč tome, provedena istraživanja se trebaju ponoviti na Klvećemjučn uzorkue riječi: ispitanika te bi morala uzeti u obzir moguće složene interakcije hormona i neurotransmitera u mozgu.

hormoni, neuroimaging, neuroplastičnost, očinsko ponašanje, roditeljsko ponašanje, socijalni mozak, traženje partnera Received December 15, 2015. Accepted October 17, 2016.

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