Daniel Messinger, Ph.D.
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Individual change over time
 Reorganizes
▪ Multiple systems (entire person)
 Successive, sequential
▪ Crawl before you walk
 Non-reversible (stable)
▪ You can’t go back
 Normative
▪ Everyone’s doing it -- but what if everyone’s not doing it?
▪ Continued education (or earlier employment)
▪ marriage, divorce, childrearing,
▪ immigration
 Continues over lifespan?
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What biological mechanisms are implicated
during birth and postnatal bonding?
 Parent-infant relationship affects brain
development and social regulation
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What can we learn from rodents?
How does that differ from humans?
Ehrlich
Estrogen
 Progesterone
 Oxytocin
 Prolactin
 Testosterone
Their roles are fairly conserved across taxa, but
involve more cortical regulation in humans.
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Will M.
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Virgin rodents (and other species) find infant
stimuli aversive
Postpartum rodent moms demonstrate a switch
in the valence of infant stimuli
 Blood transfusions from a pregnant to a virgin rodent
resulted in increased maternal responsiveness
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Why?
 Estrogen and progesterone during pregnancy +
progesterone at birth maximizes brain sensitivity to
oxytocin and prolactin
Ventral tegmental area: maternal motivation
Ventral tegmental area: maternal motivation
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Ventral tegmental area: maternal motivation
Medial Preoptic
Area robustly
activated by
infant stimuli
Ventral
tegmental area:
maternal
motivation
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Oxytocin
 Implicated broadly in social bonding / parenting
 Released centrally during birth
▪ role in approach behavior in mothers
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Rodents are promiscuous parents
Sheep form selective mother-infant bonds
 Oxytocin signaling at play

fMRI studies demonstrate activation in
mesolimbic dopamine system
 VTA
 Nucleus accumbens
 Medial orbitofrontal cortex
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Evident for both mothers and fathers
Different from rodents
 Nonparents activate these regions as well
 Nulliparous women: nucleus accumbens
activation directly related to baby cuteness

Infant crying
triggers neural
responses
 Mesolimbic
dopamine system
 Anterior insula
(empathy)
 Prefrontal cortex
(emotion regulation)

Oxytocin:
 Is positively correlated with affectionate contact
and positive engagement
 Studied via intranasal administration in fathers

Genetic studies demonstrate oxytocin’s
relationship to parenting
www.nature.com/n
ature/journal/vaop/
ncurrent/full/nature
14402.html#videos
After recording
responses to pup calls in
virgin left AI, we paired
calls for 3–5 min with
either topical oxytocin
application (oxytocin
pairing) or optical
stimulation of AI in OxtIRES-Cre animals
(optogenetic pairing
BJ Marlin et al.
Nature 000, 1-6
(2015)
doi:10.1038/natur
e14402
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Role of VTA is similar
Not enough research on the MPOA
Anterior insula and prefrontal cortex are
important for regulating responses to infant
distress
Oxytocin is important for maternal
responsiveness, but measurement problems
make things in humans ambiguous
Androgen makes males into cads, not dads.
Will M.

Rats are absentee dads
 Little attention paid to oxytocin
in nonhuman dads
 Mixed evidence surrounding
testosterone
 Some mammals: increase in
vasopressin
 Higher testosterone
implicated in mating effort,
but
▪ Less sympathy for other crying
babies
▪ Lower paternal caregiving
▪ Lower responsiveness to infants
 Testosterone decreases
when men become fathers,
▪ Increased empathy
▪ Increased frustration tolerance
▪ Decreased sexual motivation
(that could compete with
parenting effort)
Older men (n = 371; mean: 61.2 years of
age) reporting support
2. Support from two or more sources lower
testosterone than men with no support.
3. Emotional support from kin + non-kin or
multiple kin sources lower testosterone
than those with no support
4. More nurturing through (family) lifecycle..
1.
1. Lee T. Gettler, Rahul C. Oka. Hormones and Behavior, 2015;
DOI: 10.1016/j.yhbeh.2015.10.003
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Less parenting effort can result in reduced
sensitivity to parenting hormones in
offspring, who go on to parent less.
Also less pair bonding behavior.
Increased amygdala and internalizing
problems in humans
Oxytocin implicated in attachment
Will M.

Licking and grooming (L&G)
 Rats reared by low L&G moms demonstrate low L&G
when they become mothers
▪ Effects seen in mesolimbic dopamine pathway through
adulthood

Later-life pair bonding
 Disrupted by repeated neonatal social isolations
 Oxytocin neurons stimulated pharmacologically
facilitate better later-life pair bonding

Paternal Care
 Prairie voles raised with absentee dads show
impairments in pair bonding behavior and less L&G
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Research on children raised in orphanages
Focus on amygdala and prefrontal cortex
 Postinstitutionalized children demonstrate
▪ Larger amygdala volumes
▪ Increased amygdala response to fearful faces
▪ Altered connectivity between amygdala and medial
prefrontal cortex

Oxytocin
 Girls who experience childhood neglect or abuse
show lower oxytocin in cerebrospinal fluid as
adults
 Implicated in attachment
▪ High levels of oxytocin in securely attached parents
might facilitate more affectionate behavior toward
child, who then becomes more securely attached.
▪ Insecurely attached mothers have lower oxytocin
response to their children
Father’s Brain is Sensitive to
Childcare Experiences
Bichay

Current socio-cultural changes increased
father’s involvement in childrearing

Structures associated with caregiving
 Emotional Processing Network
 Cortical Mentalizing Network

Oxytocin supports development of parental
caregiving
Bichay

To understand the brain basis of human
fatherhood, its comparability with the
maternal brain, and its sensitivity to
caregiving experiences
Bichay

89 first-time parents
 20 primary-caregiving (PC) heterosexual mothers
 21 secondary-caregiving (SC) heterosexual fathers
 48 primary caregiving (PC) homosexual fathers
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First session
 Salivary samples collected for oxytocin
 Parents interviewed and completed self-report
measures
 Videotaped interacting with infants and alone

Second session
 fMRI imaging
Bichay

Neural parental caregiving
network found across all
parents raising infants

PC mothers amygdala
activation
SC Fathers STS
activation
PC Fathers amygdala
and STS activation
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Bichay

PC Mothers
 Parent-infant synchrony correlated
with amygdala
 Oxytocin correlated with ventral
anterior cingulate cortex (vACC)
▪ another component of emotional
processing network

PC and SC Fathers
 Parent-infant synchrony correlated
with STS
 Oxytocin correlated with STS

PC Fathers connectivity
between the amygdala and STS
necessary for optimal caregiving
Bichay

For all fathers, direct responsibility
alone with child correlated with
amygdala-STS connectivity
Caregiving role parent-infant
synchrony
 Caregiving role amygdala activation
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Mothers:
 Caregiving role amygdala
synchrony
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Fathers:
 STS synchrony
 STS oxytocin synchrony
Bichay
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Parenting related to
global parental
caregiving neural
network
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Caregiving
experiences involve
structural and
functional changes
in the father’s brain
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What are some of
the implications of
this study?
Bichay
Kelly Shaffer


Oxytocin (OT) underlies formation of social
bonds and is associated with positive
parenting behaviors for mothers and fathers
Parent-infant OT responses are related – a
“cross-generational link”
Parental OT system functioning likely shapes
the capacity for social engagement in the child
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Intranasal OT administration increases
peripheral OT
OT related to many social and parenting
behaviors and cognitions cross-sectionally
Do manipulations in parental OT increase
parents’ social engagement with their child?
Do manipulations in parental OT have parallel
effects on the infant?
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OT administration to Fathers will
 Enhance father’s peripheral OT, parasympathetic
activity (RSA), and father-typical social behavior
 Have parallel effects on infants’ OT, RSA, and
behavioral responses to the father
RSA = Respiratory Sinus Arrhythmia
Measure of parasympathetic activity indexing capacity to respond flexibly to
environment  enhances ability to be socially engaged
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35 father-infant (5 mo) dyads at 2 visits
0 mins
Fathers only:
• PANAS
• Saliva
• RSA
• OT/PL admin
40 mins
65 mins
45 mins
85 mins
Fathers & Infants:
Fathers & Infants: Fathers & Infants:
• Saliva
• RSA
• Saliva
• Behavioral coding
Fathers
Infants
Social gaze
Social gaze
Positive affect
Positive affect
Father vocalizations
Exploratory play
http://www.psy.miami.edu/faculty/mmccullough/Papers/McCullough-Churchland-Mendez-Final.pdf
Shaffer | Weisman et al., 2012
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Infants’ OT increases correlated with
 Fathers’ OT increases after administration
 Synchronous social behavior with Father
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No differences in father’s self-reported
emotions between OT and placebo visits
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OT administration to a parent:
 Enhances parent’s functioning in physiological and
behavioral systems that facilitate parent-child bond
▪ Salivary OT
▪ Autonomic response to free play
▪ Parenting behavior (touch, social reciprocity)
 Has parallel effects on infant’s functioning
▪ Salivary OT
▪ Autonomic response to free play
▪ Greater social engagement (social gaze, exploration)
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Synchronized OT between humans may be
critical biological basis for human social
cognition by representing another’s state in
one’s own physiology

OT administration improves symptoms of autism
and schizophrenia
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Maternal postpartum depression and premature
birth associated with disruptions in OT,
parasympathetic NS, and social-behavioral systems
 What are your reactions to OT therapy?
 What additional research would you want to see
done before recommending (or not)?
(Doss et al., 2009)
Rubenstein
Little agreement on the impact of the transition to parenthood
on marital functioning
Different methods
• Cross-sectional studies of parenthood
• Longitudinal studies beginning in pregnancy
• Inclusion of nonparents in longitudinal samples
Interrupted time-series (ITS) design
• Isolates change that can be attributed to birth from change that
was expected based on ongoing changes in the couples’
relationship.
Rubenstein
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The majority of relationship constructs
showed an immediate or delayed impact of
the transition to parenthood.
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All relationship constructs showing change
exhibited sudden worsening of the
relationship in either mothers or fathers.
Parents: dotted = fathers, solid = mothers
Nonparents: dotted = males, solid = females
Parents
Rubenstein
Nonparents
dotted = males, solid = females
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For mothers and fathers, sudden changes in
marital satisfaction, problem intensity, and
relationship dedication varied significantly
between individuals.
Mothers’ sudden changes in poor conflict
management and relationship confidence
showed significant between-individual
variability
Enduring vulnerabilities
• History of parental divorce or conflict  larger decreases in
marital satisfaction [mothers]
• Living together before marriage  greater observed negative
communication [mothers and fathers]
Nature of stressful event
• Female children  larger decreases in marital satisfaction
[mothers] and larger increases in problem intensity [fathers]
• Having a child quickly after marriage  greater decreases in
marital satisfaction [fathers]
• Lower income (but not more financial stress) at birth  larger
decreases in marital satisfaction [fathers]
* Not predictive: planned or unplanned pregnancy, financial stress
Rubenstein
• Higher marital satisfaction  larger decreases in
marital satisfaction [mothers and fathers]
• Higher relationship confidence  smaller decreases in
marital satisfaction [fathers]
• Higher relationship confidence and/or higher reported
poor conflict management  larger increases in
problem intensity [mothers and fathers]
• Higher relationship confidence and/or higher observed
negative communication  larger increases in poor
conflict management [mothers]
Rubenstein
Parents and nonparents generally show similar
amounts of decline in overall relationship
functioning over the first 8 years of marriage but
these changes tend to occur suddenly following
the birth of the baby for parents and more
gradually over time for nonparents.
Rubenstein
Danzi
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Parents reported higher levels of life satisfaction,
happiness, and meaning in life than nonparents
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Having more children was correlated with life satisfaction and meaning
in life (but not happiness)
Danzi
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Parents reported more happiness, more positive
emotion, more meaning in life, and less depressive
symptoms than nonparents
Danzi
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Parents reported more positive emotions and more meaningfulness
during childcare than other daily activities
Danzi