Fathers Today: The Role of Hormones in Father*s Sensitive and Protective Parenting

Several studies in humans have shown associations of oxytocin and vasopressin
levels with parent-child interaction (Apter-Levi, Zagoory-Sharon, & Feldman,
2014* Atzil, Hendler, Zagoory-Sharon, Winetraub, & Feldman, 2012* Bick &
Dozier, 2010* Feldman, Gordon, Schneiderman, Weisman, & Zagoory-Sharon, 2010).
Furthermore, experimental manipulation of oxytocin and vasopressin levels
through nasal administration affects parenting behavior and the neural
processing of infant signals (Cohen-Bendahan, Beijers, van Doornen, & de
Weerth, 2015* Naber, van IJzendoorn, Deschamps, van Engeland, &
Bakermans-Kranenburg, 2010* Riem et al., 2011; Thijssen et al., 2018; Van *t
Veer et al., 2019) .

We propose a randomized, double-blind, placebo-controlled within-subject design
to gain insight into the hormonal and behavioral dynamics of the paternal role
in a critical phase of parenthood: the transition to having the first baby. The
focus lies on the 50% of parents who have tended to be neglected in research
and *until recently in family policies: fathers. A special focus is on a
dimension of parenting that has received considerable attention in animal
research but, despite its evolutionary importance, not in studies on humans:
the role of the parent as protector. Protection is a crucial aspect of human
parenting. This is perhaps demonstrated most convincingly when we are
confronted with the absence of parental protection, i.e. neglect, or child
physical abuse.

In a seminal paper, Shelley Taylor and her colleagues proposed the
tend-and-befriend model as an alternative to the fight-or-flight model of
behavioral responses to stress (Taylor et al., 2000). Tending, the protection
and care of offspring, and befriending, the formation and maintenance of
interpersonal relationships with conspecifics, were proposed as strategies that
females use in times of stress to defend themselves and their offspring. A
central role in this model is attributed to oxytocin, which provides the
neuroendocrinal basis for affiliation with social groups. A second hormone that
may play a role in protective fathering is vasopressin. In men, vasopressin
levels have been associated with parenting behavior (Abraham & Feldman, 2018).
Vasopressin administration to fathers-to-be promotes attention to virtual
baby-related avatars (Cohen-Bendahan et al., 2015) and affects neural and
behavioral responses to infant cry sounds (Thijssen et al., 2018; Alyousefi-Van
Dijk et al., 2019), pointing to a role for vasopressin in responding to infant
distress.

In research on parenting quality, parental sensitivity is a key construct. It
refers to the ability to attend to infant signals and to respond promptly and
appropriately (Ainsworth, Bell, & Stayton, 1974). Studies show that fathers on
average are less sensitive towards their infants and toddlers than mothers
(Barnett, Deng, Mills-Koonce, Willoughby, & Cox, 2008* Hallers-Haalboom et al.,
2014* Schoppe-Sullivan et al., 2006* Volling, McElwain, Notaro, & Herrera,
2002), although seeing infants has similar motivational salience to men and
women (Parsons et al., 2011). Similarly to the pattern of associations for
mothers, higher levels of paternal sensitivity predict more favorable child
outcomes (Lewis & Lamb, 2003). Sensitive parenting starts with the processing
of infant signals, which has been shown to be affected by oxytocin levels (Riem
et al., 2011) and vasopressin levels (Thijssen et al., 2018)

Mapping parental brain responses to infant stimuli using fMRI has increased our
knowledge of brain processes involved in parenting sensitivity. Brain regions
expected to be important to parenting are circuitries related to (1)
arousal/salience (amygdala, ventral striatum), (2) reflexive care
(hypothalamus), (3) emotion regulation (insula, medial prefrontal cortex,
anterior cingulate cortex), and cognitive / empathic processing (insula,
inferior frontal and orbitofrontal gyri, temporoparietal junction) (Swain et
al., 2014; Witteman, 2019). Exposing parents to child stimuli in fMRI studies
activates neural systems involved in these regions. Effects of oxytocin and
vasopressin on the amygdala and the insula, medial prefrontal cortex, and
inferior frontal gyrus have been established in females (Atzil et al., 2012*
Riem et al., 2011). Replication in fathers is badly needed.

In this proposed RCT fathers will be observed with their own child, and using
standardized infant stimuli. We will test the effects of hormone administration
(oxytocin and vasopressin) on the processing of infant crying, on protective
parenting, and on the quantity (involvement) and quality (sensitivity) of
father-child interaction. Testing the effects of hormone administration on the
processing of infant crying, protection, involvement, and sensitivity may help
unravel the mechanisms of effective parenting.

In this randomized control trial (RCT) the following hypothesis will be tested:
Intranasal administration of oxytocin and vasopressin affect neural and
behavioral responses to infant signals and threat to the infant.

We will employ a randomized, double-blind, placebo-controlled within-subject
design with 55 fathers of a 2-7 month-old infant. Fathers will participate in
three experimental sessions, which take place with intervening periods of 1-2
weeks, with intranasal administration of 24 IU of (1) oxytocin, (2) 20 IU
vasopressin, or (3) a placebo. The three conditions imply six possible
counterbalanced orders of conditions, and assignment of participants to order
of administration will be random. Administration will be double-blind. The data
collection is expected to take approximately 1 year. The study will be
conducted at the fMRI facilities at the Spinozacentrum. A successful pilot
study has been conducted.

administration of (1) oxytocin, (2) vasopressin, or (3) placebo

There are no risks associated with the assessments used in this study. Possible
side effects of oxytocin and vasopressin are negligible. No adverse effects
have been reported in participants/patients undergoing MRI at the currently
available field strengths. The pilot study has not revealed any adverse
outcomes. We asked fathers to evaluate their participation, and they were
positive (*In de evaluatievragen, die digitaal en niet in het zicht van de
onderzoeker werd ingevuld, gaven de deelnemers een positieve beoordeling aan
het onderzoek: Op een schaal van 1-10 was het gemiddelde *rapportcijfer* voor
algemene ervaringen als deelnemer aan dit onderzoek een 7,9 (range 7-10; alle
deelnemers gaven dus participatie aan het onderzoek minimaal een *ruim
voldoende* *. Uit het verslag van de pilotstudie verstuurd aan de METC, 27
december 2016).

Once we understand the neurobiological underpinnings of good-enough and poor
parental sensitivity and protection, better attempts can be made to improve
parenting and reduce the adverse effects of poor parenting. The proposed study
is ground-breaking in that it includes paternal protection, an important
dimension of parenting that has been neglected in all imaging studies and
virtually all behavioral studies of parenting to date, maybe because of the
almost exclusive focus on mothers