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Received: 5 August 2020    Revised: 17 January 2021    Accepted: 13 February 2021

DOI: 10.1002/dev.22115

SPECIAL ISSUE

Theory of mind processing in expectant fathers: Associations

with prenatal oxytocin and parental attunement

Sofia I. Cardenas  | Sarah A. Stoycos | Pia Sellery |

Narcis Marshall | Hannah Khoddam | Jonas Kaplan | Diane Goldenberg |
Darby E. Saxbe

Department of Psychology, University of

Southern California, Los Angeles, CA, USA
Correspondence
Darby E. Saxbe, Department of
Psychology, University of Southern
California, Los Angeles, CA 90089, USA.
Email: dsaxbe@usc.edu
Funding information
Robert Wood Johnson Foundation;
National Science Foundation, Grant/
Award Number: 1552452 and 1842487
Abstract
Social cognition may facilitate fathers' sensitive caregiving behavior. We administered
the Why-­How Task, an fMRI task that elicits theory of mind processing, to expect-
ant fathers (n = 39) who also visited the laboratory during their partner's pregnancy
and provided a plasma sample for oxytocin assay. Three months postpartum, fathers
reported their beliefs about parenting. When rating “Why” an action was being per-
formed versus “How” the action was being performed (Why > How contrast), partici-
pants showed activation in regions theorized to support theory of mind, including the
dorsomedial prefrontal cortex and superior temporal sulcus. Fathers' prenatal oxy-
tocin levels predicted greater signal change during the Why > How contrast in the
inferior parietal lobule. Both prenatal oxytocin and attunement parenting beliefs were
associated with Why > How activation in the dorsolateral prefrontal cortex, a theory
of mind region implicated in emotion regulation. Posterior parahippocampal gyrus and
dorsolateral prefrontal cortex activation during the Why > How contrast predicted
fathers' attunement parenting beliefs. In conclusion, fathers' neural activation when
engaging in a theory of mind task was associated with their prenatal oxytocin levels
and their postpartum attunement parenting beliefs. Results suggest biological and
cognitive components of fathering may track with the theory of mind processing.

KEYWORDS
fatherhood, neuroimaging, oxytocin, parental attunement, theory of mind

1  |  I NTRO D U C TI O N of mind—­may support fathers' ability to provide sensitive and at-

Father caregiving behavior yields long-­
term benefits to children
in social, behavioral, and cognitive domains (Sarkadi et al., 2008).
Extensive research examines the complex underpinnings of moth-
ers' relationship with infants, including biological, behavioral, and
psychological adaptations that serve to support the infants' survival
(Norholt, 2020). Infants form bonds with fathers (Cabrera et al.,
2018), but less remains known about the neurocognitive mecha-
nisms that support the transition to fatherhood. Within the context
of father–­infant relationships, social cognition—­specifically, theory
tuned caregiving, allowing fathers to infer what infants feel and need
(Abraham et al., 2014; Frith & Frith, 2006). Preliminary research
suggests that the neural regions that support the theory of mind
(e.g., superior temporal sulcus) may also underlie fathering behavior
(Abraham et al., 2014). Fathers' theory of mind ability may be a key
building block underlying fathers' engagement in attuned caregiving
behavior.
The research literature on the fathering brain is scarce and
preliminary. Most parenting-­
focused neuroimaging research has
measured parents' neural responses to infant stimuli, such as

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© 2021 Wiley Periodicals LLC     1
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2      CARDENAS et al.
photographs, infant cry sounds, or video clips of the infant (e.g., Atzil
et al., 2012; Khoddam et al., 2020; Kuo et al., 2012). These stud-
ies have found associations between neural activity in brain regions
broadly supporting social cognition, including theory of mind, and
the quality of fathering behaviors. However, these studies do not
specify the mental processes that fathers engage in when watching
infant stimuli, leaving unanswered questions. Thus, although prior
studies provide insight into the neural correlates of engaging with
infant stimuli, there is a gap in understanding the neural correlates
of theory of mind in parents, despite its importance for later par-
enting behavior. Furthermore, though several studies have linked
hormones with the neural systems implicated in fathering (Abraham
et al., 2014; Mascaro et al., 2014; Wittfoth-­Schardt et al., 2012),
studies that use tasks meant to isolate specific socio-­emotional pro-
cesses would allow for the identification of processes implicated in
father neurobiology. Emerging evidence suggests changes in men's
hormones before pregnancy may indicate preparation for caregiving
(Khoddam et al., 2020; Saxbe et al., 2017). However, no studies to
our knowledge have looked specifically at prenatal levels of oxyto-
cin, a neuropeptide hormone that has been associated with social
affiliative behavior, within expectant fathers.
This study addresses these gaps in the literature by investigat-
ing the neural correlates of theory of mind within expectant fa-
thers. We also examined whether paternal prenatal oxytocin levels
predict neural activation to theory of mind and whether prenatal
activation during theory of mind predicts subsequent postpartum
self-­reported paternal beliefs about parenting. Fathers specifically
reported on whether they believe infants benefit from parenting
that is more attuned—­that is, more sensitive and responsive to their
behaviors and signals.
1.1  |  Fathering behavior and theory of mind
The neurobiology of paternal caregiving is an emerging field of re-
search that overlaps with existing research on the neurobiology of
motherhood. Extensive literature evaluates the neural basis of par-
enting behaviors in human maternal caregivers (Cárdenas et al., 2019;
Rilling & Mascaro, 2017). One seminal study found that the human
maternal brain undergoes structural changes in gray matter across
the prenatal and postpartum period, including regions involved in
theory of mind and language processing (e.g., superior temporal sul-
cus, middle and superior temporal gyrus, parahippocampal gyrus)
and emotion, memory, and self-­awareness (e.g., precuneus, posterior
cingulate cortex); these structural changes predicted parent-­related
outcomes, such as mother-­to-­infant attachment, degree of hostility
toward the infant, and functional activity when looking at own ver-
sus other infants (Hoekzema et al., 2017). Another longitudinal study
looked at structural gray-­matter changes in fathers' brains during
the postpartum period (from 2–­4 weeks postpartum to 12–­16 weeks
postpartum; Kim et al., 2014); the study found that fathers had in-
creased gray matter volume in regions underlying motivation and
attachment (e.g., hypothalamus, amygdala, striatum) and decreases
in gray matter volume in regions involved in processing threat and
ambiguity (e.g., orbitofrontal cortex, and insula) and self-­awareness
(e.g., posterior cingulate cortex). Thus, preliminary studies suggest
human maternal and paternal brains show structural changes across
the transition to parenthood that may support caregiving behaviors.
The human maternal brain recruits several subcortical regions
involved in motivation (Gregory et al., 2015) and cortical systems
involved in cognitive and emotional empathy (Rilling, 2013). One of
the cortical systems supports the ability to consider the thoughts
and feelings of others (i.e., theory of mind). This neural “theory of
mind” system is composed of a group of regions including temporo-
parietal junction, dorsomedial prefrontal cortex, ventromedial pre-
frontal cortex, superior temporal sulcus/superior temporal gyrus,
and precuneus (Gallagher & Frith, 2003; Molenberghs et al., 2016).
An emerging body of research applies neurobiological methods
for understanding paternal caregiving behavior. Atzil et al. (2012)
measured mothers' and fathers' brain activity in response to their
infants' videos. While mothers had greater activity in limbic areas,
such as the right amygdala, fathers had greater activity in social-­
cognitive cortical areas, such as the dorsal prefrontal cortex. A
second study by the same research group (Abraham et al., 2014)
presented first-­time mothers and fathers in an fMRI scanner with
videos of themselves playing with their infants and a stranger play-
ing with a strange infant. They compared three groups of first-­time
parents with varying degrees of involvement in childrearing: primary
caregiver mothers in a heterosexual relationship, secondary care-
giver fathers in a heterosexual relationship, and primary caregiver
fathers in a homosexual relationship raising infants without mater-
nal involvement. When contrasting self-­infant interactions and un-
familiar parent–­infant interaction, the study found similar levels of
activation in brain regions supporting emotion and motivation (e.g.,
ventral anterior cingulate cortex, ventral tegmental area, anterior
insula/inferior frontal gyrus) and mentalizing network (e.g., ventro-
medial prefrontal cortex, temporal poles, lateral frontopolar cortex).
However, primary caregiver mothers and primary caregiver fathers
showed greater activation in the amygdala to self-­infant interactions
versus unfamiliar parent–­infant interactions compared to secondary
caregiver fathers. When viewing self-­infant interactions versus un-
familiar parent–­infant interactions, both groups of fathers exhibited
greater activation in the superior temporal sulcus, an area widely
associated with the theory of mind. Findings from these two studies
suggest that the neurobiology of fatherhood has some overlap and
some distinction from that of mothers and the degree of caregiving
behavior may play a role in how caregivers process infant-­related
stimuli. Additionally, these studies provide preliminary evidence that
the theory of mind network may play a particularly important role in
supporting fathering behavior.
1.2  |  Measuring neural correlates of theory of mind
Theory of mind is the consideration of the mental states and inten-
tions of people (Weimer et al., 2017). Theory of mind also allows
CARDENAS et al.
individuals to perceive the behavior as driven by unobservable
thoughts (Spunt & Lieberman, 2012). By age four, most typically de-
veloping children achieve an understanding of the mind (Cutting &
Dunn, 1999). However, knowledge about mental states continues to
increase after the age of four, including interpretive theory of mind
or the ability to understand that individuals interpret events differ-
ently (Carpendale & Chandler, 1996). Differences in theory of mind
abilities for children correlate with higher general social competence
(e.g., end conversations appropriately, engage in cooperative play
behaviors, follow rules during games; Lalonde & Chandler, 1995).
Theory of mind abilities improve in typically developing adults be-
tween late adolescence and adulthood (Dumontheil et al., 2010).
Thus, theory of mind has implications for social competence and can
change across development.
Extensive research seeks to develop accurate behavioral and
neural measures that reflect the multidimensional, dynamic, and
variable nature of the theory of mind construct (e.g., Keysar et al.,
2003). Neuroimaging studies using theory of mind-­related tasks
reveal a consistent activation of brain regions including the medial
prefrontal cortex, temporal poles, temporoparietal junction, pre-
cuneus, and posterior superior temporal sulcus (e.g., Frith & Frith,
2003, 2006; Gallagher et al., 2000; Saxe et al., 2006). However,
activation in the theory of mind network varies across individual
studies based on the mental state evaluated (belief vs. desire) and
the stimuli used (verbal vs. non-­verbal; Spunt & Adolphs, 2014).
This study used the Why-­H ow Task, which isolates the multiple
cognitive processes underlying the day-­
to-­
day theory of mind
that occurs when individuals perceive others' actions (Spunt &
Lieberman, 2012). The task is one of several variants created by
a team of researchers studying social cognition (Spunt & Adolphs,
2014; Spunt & Lieberman, 2012). The “Why” process is supported
by brain regions associated with theory of mind, whereas the
“How” process is associated with areas related to action percep-
tion (Spunt & Lieberman, 2012). In the task, participants watch
sixteen blocks of eight photographs. Each of the blocks leads to
a response question meant to elicit processes associated with ac-
tion perception (“Is the person looking sideways?”) or theory of
mind (“Is the person helping?”; Spunt & Adolphs, 2014).
1.3  |  The role of oxytocin
Some research suggests that oxytocin may support social cognition
and pro-­sociality in humans (for review, see Bartz et al., 2011). One
study found that men in a within-­subject, double-­blind, placebo-­
controlled trial performed better in the Reading the Mind in the Eyes
Test (RMET) after receiving the oxytocin administration compared
to men who received placebo (Domes et al., 2007). In a double-­blind,
placebo-­controlled study, Yue et al. (2017) found that women who
inhaled oxytocin versus placebo displayed faster response times
when judging others' perspectives. This same effect was not found
in males, indicating that oxytocin may differently impact men's and
women's perspective-­t aking (Yue et al., 2017). Although some data
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in men and women suggest that oxytocin may causally support social
cognitive processes, participants' sex must be taken into account.
Many studies have investigated the neuroendocrine under-
pinnings of parenting (Gordon et al., 2010; Scatliffe et al., 2019).
Some studies have found associations between fathers' levels of
hormones, including oxytocin, testosterone, and vasopressin, and
their caregiving behavior (Feldman & Bakermans-­Kranenburg, 2017;
Gettler, 2014; Storey & Ziegler, 2016). Oxytocin has been associated
with social and affiliative behavior, including behavioral synchrony
and responsiveness in mothers and fathers (Feldman et al., 2010;
Morris et al., under review; Scatliffe et al., 2019). In fathers, oxytocin
has been specifically implicated in stimulatory parenting behaviors
(Feldman et al., 2010; Scatliffe et al., 2019) supporting father–­infant
attachment (George et al., 2010). Furthermore, experimentally ad-
ministered oxytocin levels elicit more stimulating play in fathers
(i.e., interactions that promote child exploration, often described as
“rough and tumble” play; Gordon et al., 2010; Naber et al., 2010;
Weisman et al., 2014). However, to our knowledge, no study has
assessed whether prenatal oxytocin levels in expectant fathers are
linked with enhanced postpartum caregiving outcomes or attitudes.
Furthermore, the prior literature does not reconcile whether men's
ability to engage in theory of mind is linked with prenatal oxyto-
cin and subsequent postpartum father caregiving attitudes and
behaviors.
Few studies have investigated associations between oxytocin,
brain activity, and father caregiving behavior (e.g., Abraham et al.,
2014; Atzil et al., 2012). Atzil et al. (2012) had mothers and fathers in
an fMRI scanner watched videos of own infant play and other infant
play. Mothers showed relatively greater activation in subcortical
regions linked with emotion processing (e.g., amygdala) and reward
(e.g., caudate), whereas fathers had greater activation in social cog-
nitive networks that support social cognition and empathy (i.e., me-
dial PFC, precuneus, and inferior parietal gyri). Furthermore, fathers'
postpartum plasma oxytocin levels negatively correlated with activ-
ity in the left inferior and superior frontal gyri, left primary motor
cortex, medial prefrontal cortex, and left anterior cingulate cortex
(Atzil et al., 2012). Building upon this literature, Abraham et al. (2014)
assessed oxytocin, brain activity, and parent caregiving behavior.
All participants provided salivary oxytocin data, completed a func-
tional MRI task in which they watched videos of themselves playing
with their infant (i.e., self-­infant interaction) or an unfamiliar parent
playing with an unfamiliar infant (i.e., unfamiliar parent–­infant), and
took part in a father–­infant play task micro-­coded for parent–­infant
behavioral synchrony. Although oxytocin levels were similar across
mothers and fathers, fathers showed greater activity in a region of
the brain involved in theory of mind, perspective-­t aking, and empa-
thy (i.e., superior temporal sulcus). Fathers' superior temporal sulcus
(STS) activation while watching infant videos correlated positively
with parent–­infant synchrony as well as oxytocin levels. The rela-
tionship between STS and synchrony was mediated by oxytocin.
This study suggests that fathers' social cognition, oxytocin levels,
and fathering behavior may be interrelated constructs. However,
as this study used a non-­standardized fMRI task, further research
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4      CARDENAS et al.
should clarify how oxytocin interacts with specific social-­cognitive
processes. Additionally, this study used salivary oxytocin assayed
without extraction. Although salivary oxytocin measures have been
utilized in the parenting literature, there is some doubt about the
reliability of these measures and uncertainty of the mechanism by
which oxytocin enters the saliva (for review, see MacLean et al.,
2019).
Surprisingly, no studies to our knowledge have assessed prena-
tal oxytocin levels in expectant fathers. Men and women have been
found to show shifts in hormone levels from the prenatal to the
postpartum period, and some evidence suggests that these shifts in
hormones support parenting outcomes (Edelstein et al., 2017; Saxbe
et al., 2017). For instance, Storey et al. (2000) found that men and
women had similar stage-­specific shifts in cortisol, testosterone,
and prolactin across the prenatal and postpartum periods. However,
some research suggests that oxytocin does not shift similarly across
pregnancy. An older study by Leake et al. (1981) found that healthy
men, non-­pregnant women, and pregnant women (15–­42 weeks
gestation) had similar levels of plasma oxytocin, suggesting that oxy-
tocin levels during pregnancy may not change. In contrast, Gordon
et al. (2010) found intraindividual stability during the first 6 months
postpartum and interrelated plasma oxytocin levels in mother-­father
dyads at 1 and 6 months postpartum. Furthermore, paternal oxy-
tocin correlated with stimulatory parenting behavior. These find-
ings suggest that oxytocin levels may be consistent across time and
provide preliminary support for investigating the utility of prena-
tal oxytocin in men as a predictor of postpartum father caregiving
outcomes.
Theory of mind processing may inform paternal beliefs and cog-
nitions about parenting. Parents' tendency to consider the thoughts
and needs of infants (i.e., engage in theory of mind) is related to timely
and appropriate responsiveness to infants' needs (Ereky-­Stevens,
2008). Prior research suggests that parents' beliefs and principles
about parenting are associated with their actual parenting behaviors
during early infancy (Winstanley & Gattis, 2013). However, to our
knowledge, no studies have assessed whether expectant fathers'
theory of mind activation relates to any aspects of their postpartum
parenting, including their caregiving beliefs and cognitions.
1.4  |  The current study
Although neural and behavioral research suggests that oxytocin and
theory of mind may support fathers in the transition to parenthood,
our paper uniquely uses a longitudinal approach that combines a
standardized prenatal fMRI theory of mind task, prenatal oxytocin
levels, and postpartum beliefs and cognitions about parenting. This
study used the Why-­How Task (Spunt & Adolphs, 2014), an fMRI
task designed to elicit theory of mind processing within a sample
of expectant fathers. Moreover, we used immunoassay with extrac-
tion to measure oxytocin levels in plasma, which is recommended
for plasma oxytocin assay (Lefevre et al., 2017). We controlled for
fathers' education, given evidence that education may be associated
with fathering behavior (Cabrera et al., 2007; Malin et al., 2012). We
also controlled for partners' pregnancy stage.
We tested three hypotheses:
(i) Consistent with Spunt and Adolphs (2014), we predicted that ex-
pectant fathers would show greater signal change during the
Why versus How contrast in regions that have been associated
with theory of mind specifically (e.g., dorsomedial prefrontal cor-
tex; ventromedial prefrontal cortex; orbitofrontal cortex; tem-
poroparietal junction; posterior cingulate cortex; temporal pole;
anterior superior temporal sulcus).
(ii) As discussed earlier, oxytocin may influence fathering behavior
and may be associated with neural activity in regions linked to
theory of mind (Abraham et al., 2014). We hypothesized that
fathers with higher prenatal oxytocin levels would show more
signal change in brain regions associated with theory of mind
processing (i.e., brain regions listed in hypothesis i) during the
Why > How contrast.
(iii) We hypothesized that activation during the Why > How contrast
in theory of mind regions would be associated with greater en-
dorsement of thoughts and beliefs associated with attuned care-
giving behavior.
2  |  M ATE R I A L S A N D M E TH O DS
2.1  |  Participants
This study uses data from the larger longitudinal Hormones and
Attachment across the Transition to Childrearing (HATCh) study,
which follows couples from the mothers' mid-­to-­late pregnancy
through the first year postpartum. We recruited participants
through social media advertising (e.g., Facebook, online parenting
groups), flyers, and word of mouth. This study used self-­reported
data provided by fathers from prenatal laboratory visits, con-
ducted with both members of the couple when mothers were in
mid-­
to-­
late pregnancy, subsequent father-­
only MRI visits that
we scheduled within approximately 2 weeks of the prenatal in-­
laboratory visit, and postpartum questionnaires collected online
approximately 3 months after the birth. Eligible couples were co-
habitating, first-­t ime parents of a singleton pregnancy, and did not
report any medications or conditions known to interfere with en-
docrine system hormones (e.g., steroid medicines, Cushing's dis-
ease). We also excluded couples who reported psychiatric illness
requiring medication or illegal drug use. Users of tobacco, mari-
juana, and we allowed some psychiatric medications if able to ab-
stain for 24 h before their study visit. Additional exclusion criteria
included contraindications for magnetic resonance imaging (MRI),
such as left-­
handedness, neurological or movement disorders,
claustrophobia, history of brain injury, psychotropic medication,
or severe learning disability. Additionally, participants needed
to have sufficient English language fluency to complete study
CARDENAS et al.
measures and scanning procedures. The university Institutional
Review Board (IRB) approved all procedures, and all participants
signed informed consent forms before participation.
Data for this study were available for 39 expectant fathers who
provided prenatal demographic and neuroimaging data. Of these 39
fathers, 34 provided prenatal blood samples for oxytocin assay, and
we excluded one oxytocin sample due to laboratory processing is-
sues. Of the 39 fathers with demographic and neuroimaging data,
37 fathers provided data on self-­reported parental attunement at
3  months, and two fathers did not provide 3-­month questionnaire
data. Fathers were, on average, 31.56  years old (SD  =  4.25  years).
The sample was ethnically and racially diverse, with fathers report-
ing European American (33.3%), Latino (30.8%), Black or African
American (5.1%), Asian-­American (25.7%), and multiracial or other
heritage (5.1%). The majority of expectant fathers (76.9%) reported
a college degree or higher.
2.2  |  Data availability statement
The data that support the findings of this study are available from
the corresponding author upon reasonable request.
2.3  |  Procedure
During the prenatal in-­
laboratory visits, fathers and mothers
participated in three semi-­
s tructured discussion tasks: (a) 10-­
min conversation about hopes, fears, and expectations about
birth and their transition to parenthood, (b) 10-­min conversation
about projected division of childcare, and (c) 15-­min conversation
about areas of conflict within the relationship. In addition to the
aforementioned discussion tasks, couples completed psychoso-
cial questionnaires, including the measures described below. At
the end of the laboratory visit, a licensed phlebotomist conducted
blood draws. Fathers returned to completed their scan session
within several weeks of their in-­laboratory visit; within this sam-
ple, the lag time between the prenatal laboratory visit and the
scan ranged from 1 day to 5.71 weeks, with the majority of fathers
(32 out of 39 expectant fathers; 82.05%) completing MRI scan vis-
its within 2 weeks of the in-­laboratory visit. During the MRI visit,
fathers completed the Why-­H ow Task (Spunt & Adolphs, 2014) as
part of a larger MRI data collection protocol.
2.3.1  |  Oxytocin collection
We collected blood for the plasma oxytocin assay into a sterile
EDTA vacutainer tube. We added twenty microliters of a protease
inhibitor (Amastatin; 10 µM final concentration) to the tube to
limit oxytocin degradation. Then, we centrifuged blood samples
for 10  min to separate plasma. We stored aliquots at −80°C and
shipped on dry ice to the University of Miami School of Medicine
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      5
Diabetes Research Institute (Armando Mendez, PI) for oxytocin
processing.
2.3.2  |  Oxytocin processing
We used enzyme-­linked immunosorbent assay (ELISA) kits (Arbor
Assays; Ann Arbor, MI) to calculate oxytocin immunoreactivity.
In our sample, the lower limit of detection was 0.8 pg/ml. In line
with prior work (Szeto et al., 2011), we extracted 2.2 ml of plasma.
Furthermore, we reconstituted in 220 µl assay buffer leading to a
10-­fold concentration compared to the starting plasma volume. We
performed assays in line with manufacturer instructions. We as-
sessed samples in duplicate. The inter-­assay coefficient of variation
was less than 10%. Of the MRI sample, nine fathers with oxytocin
(27% of the sample) had oxytocin levels below detection levels fol-
lowing extraction, similar to prior research analyzing extracted ox-
ytocin (e.g., Szeto et al., 2011; Tabak et al., 2011). Consistent with
prior work, we assigned a value of 0.4 pg/ml to samples below the
detection level (Saxbe et al., 2019).
We analyzed the extracted oxytocin data for outliers and
normality using SPSS Statistics 26 (IBM) (M = 1.99; SD = 1.90
Skewness  =  1.87). Furthermore, we truncated the data by drop-
ping outliers greater than three standard deviations from the
sample (3%). We found that extracted oxytocin data remained
positively skewed after excluding outliers (M = 1.50; SD = 1.05;
Skewness  =  0.74). As a consequence, we natural log-­t ransformed
the data to satisfy normality assumptions (M  =  0.23; SD  =  0.88;
Skewness = −0.03).
2.3.3  |  Why-­how task
The Why-­H ow Localizer Task is a standardized task for investi-
gating social cognition (Spunt & Adolphs, 2014). The task uses
Psychophysics Toolbox Version 3 (PTB-­3) and MATLAB (The
MathWorks, Inc.). The task presents individuals with 16 blocks of
items, with each block consisting of a question prompt and eight
photographs. The task consists of 42 pictures of common hand ac-
tions and 42 pictures of familiar facial expressions. The question
prompts present as pre-­tested yes/no questions, with participants
given a limited amount of time for response. The task requires ap-
proximately 6 min and 30 s to complete. Participants complete the
task in a suite for a magnetic resonance imaging (MRI) scanner.
Within the scanner, participants watch stimuli while lying down
in the scanner and can use a button box programmed to allow for
yes/no responses.
The Why-­How Task features a 2 (condition: Why, How) × 2 (be-
havioral category: face, hand) factorial design (see Figure 1). For
the behavioral factor, participants watch a photograph with either
a face or a hand. For the stimulus factor, participants receive a
stimulus prompt that asks either a Why question (i.e., the question
elicits theory of mind) or a How question (i.e., the question evokes
 |
6      CARDENAS et al.
F I G U R E 1  Conditions of the Why-­How Task. The above diagram
displays the 2 × 2. factorial design of the Why-­How Task with type
of question (condition: Why, How) and stimulus (condition: face,
hand).
action-­perception). In this study, similar to Spunt and Adolphs (2014),
we collapsed the behavioral category conditions (i.e., face, hand) and
focused on Why and How conditions. We contrasted Why > How
to specifically examine the neural correlates of theory of mind pro-
cessing. We also scored the Why-­How task results behaviorally for
accuracy and response time and entered this information in SPSS for
further analysi.
2.3.4  |  fMRI data acquisition
We acquired whole-­brain images on a Siemens 3 Tesla MAGNETON
Prisma System scanner. We acquired high-­resolution, T1-­weighted
images using a 3D Magnetization Prepared Rapid Acquisition
Gradient Echo (repetition time, 2530  ms; echo time, 3.13  ms; flip
angle, 10°), with an isotropic voxel resolution of 1  mm3. We col-
lected functional data using a T2* weighted echo-­planar imaging
(EPI) with an interleaved sequence (194 2.5 mm transversal slices;
repetition time, 2000 ms; echo time, 25 ms; field of view, 192 mm2;
3.0 × 3.0 × 2.5 mm voxels, flip angle, 90 degrees). Functional scans
employed Siemens' 3D PACE prospective motion correction (and
were then pre-­
processed for motion further offline, described
below; Thesen et al., 2000).
We presented stimulus presentation and response recording
using MATLAB (version 2012a; MathWorks Inc., Natick, MA, USA).
We used an LCD projector to show stimuli on a rear-­projection
screen. Participants made responses using their right index and mid-
dle fingers on a button box.
2.3.5  |  fMRI data analysis
We analyzed neural responses to the Why > How contrast using
FEAT (FMRI Expert Analysis Tool) Version 6.00, part of FSL
(FMRIB's Software Library, www.FMRIb.ox.ac.uk/fsl). We used
FLIRT (Jenkinson et al., 2002; Jenkinson & Smith, 2001) to regis-
ter high-­resolution structural and/or standard space images. For
pre-­
processing, we conducted motion correction with MCFLIRT
(Jenkinson et al., 2002), non-­brain removal using BET (Smith, 2002),
spatial smoothing using a Gaussian kernel of FWHM 5 mm, and
high-­pass temporal filtering with Gaussian-­weighted least-­squares
straight-­line fitting and a sigma = 50.0 s).
Next, we analyzed data using a General Linear Model (GLM)
with a multi-­level mixed-­effects design. In the GLM, the observed
hemodynamic response function (HRF) signal is predicted by one or
more explanatory variables that reflect a specific factor, also called
regressor or regressor of interest. The GLM is a method of model-
ing an observed neural signal in relation to one or more independent
or explanatory variables, which are also referred to as regressors
(Jenkinson & Chappell, 2018). As such, we entered each component
of the task as a regressor (Why-­Face trials, Why-­Hand trials, How-­
Face trials, Why-­Hand trials) and modeled by convolving the task
design with a double-­gamma hemodynamic response function. We
defined the task periods from the first photograph in each block to
the stimulus offset of the last photograph in each block. We also
included in the model the temporal derivatives of the task regres-
sors and six motion parameters as nuisance regressors. We created
contrasts as linear combinations of the explanatory variables to look
at overall task effects and condition effects (e.g., Why > How). At
the individual subject level, we generated statistical maps. We then
computed brain-­activity maps for each of the task effects and con-
dition effects combining across all subjects using a higher-­
level
mixed-­effects design using FLAME to produce contrast-­level activity
maps. This study focused on the Why > How contrast. All higher-­
level analyses included fathers' education level and weeks pregnant
as covariates. To account for multiple comparisons, we applied clus-
ter thresholding using Gaussian Random Field theory with a cluster
size probability threshold of p < 0.05. For the main effect (Why >
How contrast), we used a cluster-­forming z threshold of 3.1, a more
stringent threshold. Given that we had a smaller sample for regressor
analyses (prenatal oxytocin, postpartum attunement), we used a less
stringent cluster-­forming z threshold of 2.3 to account for low power
and avoid type II error. All coordinates reported are in the Montreal
Neurological Institute (MNI) standard brain space.
2.4  |  Measures
2.4.1  |  Demographics
At the prenatal visit, fathers self-­reported their educational attain-
ment with the following options: high school/GED, some college,
associate degree, bachelor's degree, master's degree, professional/
doctorate). Fathers also reported on age, and mothers reported
their expected due date, from which we calculated their pregnancy
stage (number of days pregnant) at the time of their prenatal study
visit.
CARDENAS et al. |
      7

TA B L E 1  Descriptive statistics of sample demographics and self-­

2.4.2  |  Parental attunement reported measures.

Fathers' ratings of thoughts and behaviors completed a series Variable Subcategory Value/mean (%/SD)

of online questionnaires, including the Baby Care Questionnaire Education High school/GED 1 (2.6%)
(BCQ; Winstanley & Gattis, 2013). The BCQ is a 30-­item question- Some college 7 (17.9%)
naire that asks participants how strongly they agree or disagree Associate degree 1 (2.6%)
with a statement related to principles that guide feeding, holding, Bachelor's degree 12 (30.8%)
and soothing behaviors. Participants rate each item on a Likert
Master's degree 11 (28.2%)
Scale from 1 (strongly disagree) to 4 (strongly agree). The BCQ
Professional/doctorate 7 (17.9%)
generates two subscales, “Structure” and “Attunement,” which
Race European American 13 (33.3%)
reflect parents' endorsement of more structured (reliant on rou-
Latino 12 (30.8%)
tines and schedules) versus more attuned (responsive to in-­the-­
Black or African 2 (5.1%)
moment infant cues) parenting style principles. We specifically
American
assessed the Attunement scale for this project. BCQ Attunement
Asian-­American 10 (25.7%)
subscale scores are generated by averaging scores on attunement
Multiracial or other 2 (5.1%)
items, such as “Babies benefit from physical contact with parents
Age at prenatal 31.56 (4.25), 23–­41
when they wake during the night,” Parent(s) should find a pattern
visit
of feeding/eating that suits their baby,” and “Responding quickly to
Extracted 0.23 (0.88),
a crying baby leads to less crying in the long run.” A prior validation
oxytocin −0.92–­1.92
study showed that the BCQ attunement subscale had acceptable
Weeks pregnant 27.84 (4.71),
internal consistency (Cronbach's alpha >0.70), acceptable test–­ 20.37–­38.52
retest reliability (>0.70), and external validity (i.e., endorsement
Weeks between 1.63 (1.15),
of attunement principle was correlated with higher bed-­sharing, laboratory 0.14–­5.71
breastfeeding, and holding; Winstanley & Gattis, 2013). We com- and MRI
puted internal consistency on our sample and found acceptable Parental 2.91 (0.31),
reliability in our sample's BCQ Attunement scores (Cronbach's attunement 2.42–­3.77
alpha = 0.70). Weeks pregnant is the self-­reported time fathers reported their female
partners were pregnant on the day of the laboratory visit.

3  |   R E S U LT S (37) = −8.38, p < 0.01, such that participants responded more slowly

We present descriptive statistics in Table 1. Zero-­order correlations
between study variables are shown in Table 2. Fathers' education
and age were positively correlated (r (39) = 0.57, p < 0.01). Age cor-
related with accuracy during How trials (r (39)  =  0.35, p < 0.05).
Fathers' accuracy during Why trials correlated with fathers' accu-
racy during How trials (r (38)  =  0.78, p < 0.01). Fathers' response
time during Why trials correlated with fathers' response time during
How trials (r (38) = 0.93, p < 0.01). We also found a trending negative
correlation between extracted oxytocin and response time during
How trials (r (32) = −0.35, p = 0.05). Of interest, we found a trending
significance between prenatal oxytocin and postpartum attunement
(r (31) = 0.33, p = 0.069, see Figure 2).
3.1  |  Behavioral results
Within this sample, we found behavioral results consistent with
Spunt and Adolphs (2014). The percent accuracy on How (M = 94%,
SD  =  6.2%) trials differed from Why (M  =  91%, SD  =  7.3%) trials,
t (38)  =  4.09, p < 0.01, such that participants responded less ac-
curately to Why trials. Response time to How trials (M = 818 ms.,
SD = 134 ms.) differed from Why trials (M = 900 ms., SD = 155), t
during Why trials.
3.2  |  fMRI results
3.2.1  |  Covariates: Associations between
education and weeks pregnant during theory of mind
Higher educational attainment predicted greater signal change in
theory of mind regions during the Why > How contrast. When we
added education level as a regressor into the Why > How contrast
(see Table 3 and Figure 3), signal changes associated with this co-
variate were found in four clusters, including the right precuneus,
bilateral precentral gyri, left postcentral gyrus, and right inferior
temporal gyrus. Given these findings, we included education as a
covariate in all analyses with cross-­subject regressors. The preg-
nancy stage was also included as a covariate in all analyses to control
for potential differences resulting from men's partners' pregnancy
stage. When we added weeks pregnant as a regressor into the Why
> How contrast (see Table 4 and Figure 4), activation occurred in a
cluster near the cingulate, largely comprised of white matter. Thus,
we mean-­centered education level and pregnancy stage (i.e., weeks
pregnant) and included as confound regressors in all analyses.
 |
8      CARDENAS et al.

TA B L E 2  Bivariate correlation of main study variables.

Variable 1 2 3 4 5 6 7 8

1. Age
2. Education 0.57***
3. Weeks pregnant 0.22 0.29*
4. Prenatal oxytocin −0.05 −0.10 0.23
5. Parental attunement −0.10 −0.15 −0.10 0.33*
6. Why trials accuracy 0.15 0.13 0.02 −0.11 −0.18
7. How trials accuracy 0.35** 0.19 0.14 −0.09 −0.21 0.78***
8. Why trials RT 0.28* 0.12 −0.03 −0.28 −0.11 0.25 0.05
9. How trials RT 0.17 0.07 −0.08 −0.35** −0.16 0.28* 0.01 0.93***

Weeks pregnant is the self-­reported time fathers reported their female partners were pregnant including the time between the laboratory visit and
the MRI visit.
*p < 0.10; **p < 0.05; ***p < 0.01.

3.75
Postpartum self-reported parental attunement

3.50

3.25

3.00

2.75

2.50

-1.00 -.50 .00 .50 1.00 1.50 2.00

Prenatal plasma oxytocin

F I G U R E 2  Scatterplot of prenatal plasma oxytocin and postpartum self-­reported parental attunement.

3.2.2  |  Hypothesis 1: Neural activation during main
effect of task
We partially replicated the key neural findings from the Spunt and
Adolphs (2014) paper. The full list of brain regions activated by
Why > How contrast is listed in Table 5. A visual representation
of the brain regions activated by Why > How contrast is shown in
Figure 5. When contrasting activation during Why trials, compared
with How trials (i.e., Why > How contrast), we found signal change
in regions from the original group-­level results of the study: left
dorsomedial prefrontal cortex, left orbitofrontal cortex, right tem-
poroparietal junction (angular gyrus), bilateral posterior cingulate
cortex, and right anterior superior temporal sulcus. These results
largely replicate findings from the original Why-­How paper (Spunt
& Adolphs, 2014). However, during the Why > How contrast, this
study found additional signal change in several areas not found in
the original task study: left amygdala, left dorsolateral prefrontal
cortex, left caudate, left thalamus, and right posterior superior tem-
poral gyrus.
3.2.3  |  Hypothesis 2: Associations between
oxytocin and BOLD signal during theory of mind
Prenatal oxytocin was added as a between-­subjects regressor in the
group-­level analysis of the Why > How contrasts. Higher prenatal
CARDENAS et al.       9|
TA B L E 3  Neural regions positively
MNI coordinates
correlated with education during the Why
> How contrast. Region L/R k x y z Z

Precuneus R 2127 18 −62 42 4.55

R -­ 30 −40 46 4.38
R -­ 10 −66 60 4.05
R -­ 54 −52 50 3.93
R -­ 32 −50 56 3.87
R -­ 34 −56 64 3.85
Precentral gyrus R 824 10 −32 50 3.76
L -­ −22 −60 56 3.73
R -­ 2 −42 54 3.71
R -­ 4 −38 54 3.69
R -­ 8 −34 44 3.52
L -­ −16 −58 52 3.17
Postcentral gyrus L 632 −46 −28 52 4.02
L -­ −62 −38 44 3.91
L -­ −62 −42 44 3.8
L -­ −48 −26 44 3.52
L -­ −32 −26 42 3.45
L -­ −40 −18 60 3.23
Inferior temporal gyrus R 494 50 −58 −8 3.84
R -­ 38 −56 2 3.46
R -­ 30 −64 0 3.36
R -­ 18 −60 14 3.34
R -­ 24 −74 2 3.24
R -­ 28 −58 −2 3.24

All peaks survived a whole-­brain search thresholded at a voxel-­wise family-­wise error rate of 0.05
and a cluster corrected at z = 2.3. x, y, z = Montreal Neurological Institute (MNI) coordinates in the
left-­right anterior-­posterior, and inferior-­superior dimensions, respectively (n = 39).

F I G U R E 3  Group-­level results of the Why > How contrast with education as a regressor. Sagittal, coronal, and axial view of whole-­brain
activation during the Why > How contrast. Analyses cluster corrected at z = 2.3 (n = 39).
 |
10      CARDENAS et al.

TA B L E 4  Neural regions positively

MNI coordinates
correlated with weeks pregnant during
Region L/R k x y z Z Why > How contrast.

White matter/cingulate gyrus R 400 26 −46 12 3.34

R -­ 36 −60 4 3.32
R -­ 32 −62 8 3.31
R -­ 16 −38 28 3.22
R -­ 20 −48 18 3.21
R -­ 34 −68 −2 3.16

All peaks survived a whole-­brain search thresholded at a voxel-­wise family-­wise error rate of 0.05
and a cluster corrected at z = 2.3. x, y, z = Montreal Neurological Institute (MNI) coordinates in the
left-­right anterior-­posterior, and inferior-­superior dimensions, respectively (n = 39).

F I G U R E 4  Group-­level results of the Why > How contrast with weeks pregnant as a regressor. Sagittal, coronal, and axial view of
whole-­brain activation during the Why > How contrast. Analyses cluster corrected at z = 2.3 (n = 39).

plasma oxytocin predicted greater signal in theory of mind regions
during the Why > How contrasts. Specifically, signal change emerged
in eight clusters, including bilateral temporoparietal junction (angular
gyrus), bilateral supramarginal gyrus, bilateral dorsolateral prefrontal
cortex, bilateral paracingulate gyrus, bilateral intracalcarine cortex,
bilateral posterior cingulate gyrus, and right superior temporal gyrus
(see Table 6 and Figure 6).
bilateral dorsolateral prefrontal cortex and right posterior parahip-
pocampal gyrus (see Table 7 and Figure 7).
3.2.5  |  Exploratory Analyses: Overlap between
oxytocin and postpartum attunement activation
during theory of mind

To follow-­up on the above-­reported findings, we assessed whether

3.2.4  |  Hypothesis 3: Associations between
postpartum attunement and activation
during theory of mind
We also explored whether signal change in theory of mind regions
during the Why > How contrast predicted greater endorsement of
an attuned parenting philosophy at 3 months postpartum. We found
that postpartum attunement was associated with signal change for
the Why-­How contrast in two regions including portions of the
there were areas of significant overlap in signal change associated with
both prenatal oxytocin and postpartum attunement during the Why
> How contrast. Specifically, we used fslmaths (Smith et al. 2004) to
mask the thresh_zstat image of the Why > How contrast with oxy-
tocin as a regressor (i.e., hypothesis 2) with the thresh_zstat image of
the Why > How contrast with postpartum attunement as a regressor
(i.e., hypothesis 3). The results of this masking (Figure 8) revealed over-
lapping activation in a mostly right-­lateralized region in the prefrontal
cortex, mostly composed of the dorsolateral prefrontal cortex.
CARDENAS et al. |
      11

TA B L E 5  Group-­level results of the

MNI coordinates
Why > How contrast.
Region L/R k x y z Z

Orbitofrontal cortex L 6372 −48 16 −22 6.45

L -­ −58 −8 −14 6.4
L -­ −42 28 −14 6.37
L -­ −56 4 −16 6.29
L -­ −52 24 12 6.22
L -­ −48 30 −6 6.21
Dorsomedial prefrontal cortex L 5759 −6 56 38 7.22
L -­ −8 64 26 7.2
L -­ −4 44 50 7.18
L -­ −10 60 32 7.18
L -­ −2 48 −16 7.16
L -­ −10 44 46 7
Posterior cingulate cortex R 1836 0 −50 30 6.27
L -­ −4 −60 34 6.08
L -­ −2 −60 30 5.93
L -­ −4 −50 22 5.64
L -­ −10 −52 4 4.31
R -­ 14 −48 6 3.64
Anterior superior temporal sulcus R 684 58 2 −22 5.31
R -­ 60 −6 −18 5.25
R -­ 62 −2 −22 5.03
R -­ 54 8 −22 4.98
R -­ 50 −8 −12 4.89
R -­ 48 −14 −10 4.8
Amygdala L 261 −26 −18 −18 5.01
L -­ −20 −10 −14 4.96
L -­ −28 −6 −22 4.19
L -­ −36 −16 −22 3.43
Dorsolateral prefrontal cortex L 229 −42 14 54 4.22
L -­ −36 24 52 4.22
L -­ −34 18 50 4.17
Temporoparietal junction (angular gyrus) R 161 48 −58 24 4.24
R -­ 52 −62 28 4.02
R -­ 58 −56 26 3.64
Caudate L 159 −12 14 12 4.65
L -­ −10 −4 12 3.29
L -­ −14 14 0 3.25
Thalamus L 102 −4 −12 6 4.31
L -­ −2 −16 12 3.91
Posterior superior temporal gyrus R 100 64 −34 4 3.94
R -­ 54 −30 2 3.86
R -­ 46 −34 −2 3.78

All peaks survived a whole-­brain search thresholded at a voxel-­wise family-­wise error rate of 0.05
and a z-­threshold of 3.1. x, y, z = Montreal Neurological Institute (MNI) coordinates in the left-­right
anterior-­posterior, and inferior-­superior dimensions, respectively (n = 39).
 |
12      CARDENAS et al.
F I G U R E 5  Group-­level results of the Why > How contrast with education and weeks pregnant as covariates. Sagittal, coronal, and axial
view of whole-­brain activation during the Why > How contrast. Analyses cluster corrected at z = 3.1 (n = 39).
4  |  D I S C U S S I O N
In this study, we partially replicated the results from the Spunt
and Adolphs (2014) paper within a sample of expectant fathers.
Consistent with our hypotheses, we found that theory of mind pro-
cessing during the Why > How contrast was associated with signal
change in mentalizing network structures, including both anterior
and posterior cortical midline structures and the right temporopa-
rietal junction (angular gyrus). We also found activation to Why >
How in a few additional regions, including the left dorsolateral pre-
frontal cortex, right posterior superior temporal gyrus and subcor-
tical regions (left caudate, left thalamus, left amygdala). Moreover,
we found that prenatal oxytocin in expectant-­fathers during the
Why > How contrast was associated with similar signal change as
the Why > How contrast, including frontal and posterior cortical
midline structures as well as the bilateral temporoparietal junction
(angular gyrus). Signal change in the bilateral dorsolateral prefrontal
cortex and right posterior hippocampal gyrus during the Why > How
contrast predicted greater self-­reported beliefs and cognitions re-
garding attuned parenting styles approximately 6 months later when
infants were 3 months of age.
Although not originally found by Spunt and Adolphs (2014), we
observed activation in the left amygdala and left caudate during
the Why > How contrast in expectant fathers. Interestingly, social
neuroscientists have posited that regions associated with process-
ing emotional salience (e.g., fearful faces) may foster higher order
empathic behavior by making individuals aware of the suffering of
others (Marsh, 2016). Within parenting, the amygdala may promote
mothers' ability to detect biologically salient information in the care-
giving environment (Swain et al., 2014). The caudate is a reward re-
gion and is theorized to support mothers' motivation to engage with
their infants (Noriuchi et al., 2008). Men's testosterone across the
transition to parenthood, which may reflect parenting investment,
has been associated with increased caudate activation (Kuo et al.,
2012). Although preliminary, our findings suggest that expectant
fathers are engaging both cortical and subcortical regions when
completing the Why-­How theory of mind task; further research can
investigate whether these patterns of activation are dynamic in new
parents.
Although not the focus of the study, fathers' educational attain-
ment was associated with Why > How activation in areas involved
in vision and the processing of words (e.g., inferior temporal gyrus;
Dien et al., 2013), the mirror neuron system (e.g., precentral gyrus,
postcentral gyrus; Wu et al., 2017), and theory of mind (e.g., pre-
cuneus; Saxe et al., 2006). In the parenting network, the mirror
neuron system and the theory of mind network work together to
support a parents' ability to quickly resonate with infant behaviors
(i.e., mirror neuron system), consider intentions (i.e., theory of mind
network), and provide caregiving behavior that syncs with the child's
needs (Feldman, 2015). Extensive research suggests that fathers
with higher education levels use more advanced vocabulary, which
is linked with children's emotion regulation language development
(Cabrera et al., 2007; Pancsofar & Vernon-­Feagans, 2010). Thus, our
findings might reflect that more educated fathers may exhibit more
comfort or engagement with the Why-­How Task, which requires
participants to read questions quickly.
Additionally, fathers' prenatal oxytocin levels predicted acti-
vation in areas of the brain that support embodied simulation and
theory of mind. Of note, we collected prenatal oxytocin following a
laboratory visit that included partner interaction and questions rel-
evant to the transition to parenthood. Activation during the Why >
How contrast was associated with prenatal oxytocin in a region that
included the bilateral temporoparietal junction (angular gyrus) and
bilateral supramarginal gyrus, which compose the inferior parietal
CARDENAS et al. |
      13

TA B L E 6  Neural regions positively correlated with prenatal TA B L E 6  (Continued)

oxytocin during Why > How contrast.
MNI coordinates
MNI coordinates
Region L/R k x y z Z
Region L/R k x y z Z
Superior R 340 48 −20 −4 4.04
TPJ/SMG L 3882 −48 −56 46 4.68 temporal R -­ 62 −20 2 3.21
gyrus
L -­ −58 −48 40 4.68 R -­ 62 −28 2 3.10
L -­ −50 −50 38 4.66 R -­ 70 −26 −4 3.88
L -­ −42 −52 54 4.54 R -­ 60 −12 −10 3.44
L -­ −52 −38 42 4.06 R -­ 60 −22 −18 3.28
L -­ −20 −74 42 4.05
All peaks survived a whole-­brain search thresholded at a voxel-­wise
TPJ/SMG R 1481 44 −56 50 4.17 family-­wise error rate of 0.05 and a z-­threshold of 2.3. x, y, z = Montreal
R -­ 46 −50 32 3.67 Neurological Institute (MNI) coordinates in the left-­right anterior-­
posterior, and inferior-­superior dimensions, respectively (n = 33). TPJ/
R -­ 34 −80 32 3.94
SMG =Temporoparietal Junction (Angular Gyrus)/Supramarginal Gyrus.
R -­ 40 −60 46 3.93
R -­ 48 −44 56 3.87
R -­ 52 −46 40 3.63
lobule (IPL). The angular gyrus, which is part of the temporopari-
etal junction, has been implicated in theory of mind and mentalizing
Dorsolateral R 817 34 34 30 3.57
prefrontal tasks (for review, see Seghier, 2013). Concerning parenting, the IPL
R -­ 44 30 26 3.45
cortex is part of the embodied simulation network as well as the mirror neu-
R -­ 44 32 38 3.2
ron system (Feldman, 2015). The mirror neuron system supports an
R -­ 52 36 26 3.2
individual's ability to observe and mimic the emotions and behaviors
R -­ 36 18 36 3.16
of others (for review, see Rizzolatti & Craighero, 2004). The embod-
R -­ 22 50 24 3.25 ied simulation network supports a parents' ability to mentally sim-
L 811 −36 −2 54 3.76 ulate the behavior of the infants and consider their intentions and
L -­ −38 20 50 3.60 needs (Feldman, 2015). The Why > How contrast was also related
L -­ −50 26 32 3.47 to oxytocin in areas that support social cognition, including the pos-
L -­ −36 26 44 3.47 terior cingulate cortex, a key region of the Default Mode Network
L -­ −38 32 28 2.97 (Li et al., 2014). Given the minimal research on oxytocin in expect-

L -­ −50 32 24 2.96 ant fathers and the preliminary evidence we found of an association
between oxytocin and social cognition, we recommend that future
Paracingulate R 707 12 30 26 3.58
gyrus studies investigate oxytocin and measures of social cognition across
L -­ −10 42 30 3.29
the transition to fatherhood.
R -­ 2 14 56 3.05
Prenatal activation to the Why > How contrast in regions that
L -­ −6 28 44 3.14
support social cognition, behavioral organization, and emotion
R -­ 8 60 28 3.22
regulation predicted fathers' postpartum endorsement of a more
-­ 0 30 22 3.09 attuned parenting style, as assessed 3  months following the birth.
Intracalcarine R 561 2 −64 16 3.27 Specifically, attunement was associated with activation in two clus-
cortex L -­ −16 −62 0 3.23 ters, including the bilateral dorsolateral prefrontal cortex and right
L -­ 12 −78 6 3.16 posterior parahippocampal gyrus. The dorsolateral prefrontal cor-
L -­ −12 −72 14 3.16 tex has been activated in studies assessing attention (Doricchi et al.,
L -­ −8 −68 10 3.04 2010; Shulman et al., 2010), executive control (Wagner et al., 2001),
L -­ −18 −72 2 3.03 and theory of mind (Kobayashi et al., 2007). The parahippocampal

Posterior R 429 2 −36 46 3.71

gyrus is part of the paralimbic region and underlies context and
cingulate memory processing (Bohbot et al., 2015). With regard to parenting,
R -­ 2 −44 50 3.57
gyrus the dorsolateral prefrontal cortex is posited to be part of the pa-
L -­ −2 −30 44 3.29
rental emotion-­regulation/executive network (Feldman, 2015). The
L -­ −10 −24 42 3.25
emotion-­regulation/executive network is theorized to contribute to
L -­ −12 −20 40 3.22
parents' management of emotions, attention, multi-­t asking, and or-
L -­ −4 −22 46 2.92
ganization (Feldman, 2015; Swain et al., 2014). Furthermore, in a lon-
gitudinal study of cortical plasticity in new fathers, Kim et al. (2014)
found that fathers' show an increase in gray matter volume in the lat-
(Continues) eral prefrontal cortex across the first and fourth month postpartum.
 |
14      CARDENAS et al.

F I G U R E 6  Group-­level results of the Why > How contrast with oxytocin as the main regressor and education and weeks pregnant as
covariates. Sagittal, coronal, and axial view of whole-­brain activation during the Why > How contrast. Analyses cluster corrected at z = 2.3
(n = 33).

TA B L E 7  Neural regions positively

MNI coordinates
correlated with postpartum attunement
Region L/R k x y z Z during Why > How contrast.

Dorsolateral prefrontal cortex R 2120 32 34 28 3.98

L -­ −12 44 36 3.74
R -­ 30 8 40 3.62
R -­ 36 22 38 3.58
L -­ −8 56 24 3.55
R -­ 14 52 26 3.5
Posterior parahippocampal gyrus R 498 14 −34 −4 3.68
R -­ 10 −36 −4 3.66
R -­ 2 −42 0 3.57
R -­ 18 −34 −14 3.15
R -­ 0 −56 16 3.09
R -­ 16 −30 2 3.06

All peaks survived a whole-­brain search thresholded at a voxel-­wise family-­wise error rate of 0.05
and a z-­threshold of 2.3. x, y, z = Montreal Neurological Institute (MNI) coordinates in the left-­right
anterior-­posterior, and inferior-­superior dimensions, respectively (n = 37).

Prior research suggests that the paralimbic region, which includes
the parahippocampal gyrus, is involved in processing own-­infant
stimuli (Swain, 2008). We found that fathers' neural activation in
response to a theory of mind task during their partner's pregnancy
predicted their subsequent principles and cognitions about attuned
parenting at 3 months after birth. For example, they endorsed be-
liefs that infants benefit from eating on demand and being soothed
to sleep rather than kept on strict schedules. More attuned par-
enting may require more competent mentalizing abilities because
parents need to “read” infants' cues rather than follow pre-­ordered
routines. It is intriguing that fathers' prenatal theory of mind activa-
tion predicted their subsequent beliefs about this style of parenting.
Both prenatal oxytocin and postpartum endorsement of attuned
parenting styles showed similar activation in the dorsolateral pre-
frontal cortex during the Why > How contrast. As mentioned, the
dorsolateral prefrontal cortex is implicated in executive functioning
and is posited to support parent attention and emotion regulation
(Feldman, 2015). The dorsolateral prefrontal cortex has not been
previously associated with oxytocin within the context of parenting.
However, research assessing the neural underpinnings of social sup-
port found that oxytocin enhanced the benefits of romantic partner
touch during shock, and oxytocin was associated with increased ac-
tivity in the middle frontal gyrus, which is part of the dorsolateral
prefrontal cortex (Kreuder et al., 2018). Relatedly, Weisman et al.
CARDENAS et al. |
      15

F I G U R E 7  Group-­level results of the Why > How contrast with the Baby Care Questionnaire (BCQ) attunement scale as the main
regressor and with education and weeks pregnant as covariates. Sagittal, coronal, and axial view of whole brain activation during the Why >
How contrast. Analyses cluster corrected at z = 2.3 (n = 37).

F I G U R E 8  Overlapping activity during the Why > How contrast with oxytocin and postpartum attunement as the main regressors.
Sagittal, coronal, and axial view of whole-­brain activation. Analyses cluster corrected at z = 2.3 and a p value of .05 (n = 33 for oxytocin,
n = 37 for BCQ attunement).

(2014) found a link between oxytocin administration and changes in
testosterone levels linked with enhanced fathering behaviors (e.g.,
vocal synchrony, positive affect, greater touch). Within this sample,
we have found that paternal postpartum oxytocin levels are asso-
ciated with more father–­infant touch during parenting interaction
(Morris et al., under review). This study found associations in the
dorsolateral prefrontal cortex during theory of mind with prenatal
oxytocin and fathers' greater endorsement of attunement as a post-
partum parenting principle. Given that all variables were measured
once, we cannot infer directionality or causality between prenatal
oxytocin and theory of mind processing and postpartum attunement
principles. As a natural extension of our work, future studies can
assess trajectories of oxytocin, theory of mind processing, and par-
enting across the transition to parenthood to assess longitudinal
trajectories.
This study has a number of limitations. Our sample was ethnically
diverse, but participants were largely from highly educated back-
grounds. Although larger than other samples in the neurobiology
of parenting literature, the sample size was small (39 fathers with
MRI data; 33 with oxytocin data; 37 with postpartum attunement
data). An additional limitation is that for several of our fathers, oxy-
tocin levels were either missing (due to refusal or sample processing
 |
16      CARDENAS et al.
issues) or undetectable (due to overly low levels). Furthermore,
we note that this study only involved one neuroimaging timepoint
during the transition to parenthood. The extant literature supports
that neural regions involved in social cognition can develop and
change over time (Blakemore, 2008; Dumontheil et al., 2010). Future
research that incorporates multiple scans throughout the transition
to parenthood can better characterize the fathering brain. As the
first study to examine the theory of mind processing, oxytocin, and
postpartum parenting attitudes together in one investigation, this
work would benefit from replication and extension prior to further
interpretation.
Despite the aforementioned limitations, this study makes sev-
eral important contributions to research on parenting and child
development. This study extends prior work on the neurobiology
of fatherhood by using a standardized task to measure the theory
of mind in expectant fathers. This is also the first study examining
prenatal oxytocin levels in tandem with brain activation in expect-
ant fathers. Our sample of expectant fathers was racially and eth-
nically diverse and contributed longitudinal, multimodal data. Our
results suggest that oxytocin may support social cognition process-
ing during the prenatal period. Additionally, fathers who showed
greater prenatal neural theory of mind activation subsequently
endorsed more attuned parenting styles at 3 months postpartum.
These findings further the current understanding of neurobiolog-
ical factors that support fathers' preparation for parenthood and
highlight future directions for the parenting brain research.
AC K N OW L E D G M E N T S
This work was supported by National Science Foundation (NSF) Career
Award (1552452; Saxbe), National Science Foundation Grant/Award
(DGE-­1842487; Cárdenas), and a Health Policy Research Scholars
Award funded by the Robert Wood Johnson Foundation (Cárdenas).
Portions of this work were presented at the International Society of
Developmental Psychobiology (ISDP) Conference; we thank ISDP and
their sponsors (i.e., NICHD; Columbia University's Nurture Science
Project) for granting a Travel Award to Sofia Cárdenas.
C O N FL I C T S O F I N T E R E S T
The authors have no conflict of interests to report.
AU T H O R C O N T R I B U T I O N S
Sofia I. Cardenas Conceptualization (equal); Formal Analysis
(equal); Investigation(supporting); Writing—­
O riginal Draft
Preparation (lead); Sarah A. Stoycos: Investigation (equal)); Project
Administration (leading); Writing—­Review & Editing (supporting);
Pia Sellery: Investigation (supporting); Project Administration
(supporting); Writing—­
Review & Editing (supporting); Narcis
Marshall: Investigation (supporting); Writing—­
Review & Editing
(supporting); Hannah Khoddam: Investigation (supporting);
Project Administration (supporting); Writing—­
Review & Editing
(supporting); Jonas Kaplan: Formal Analysis (equal); Writing—­
Review & Editing (supporting); Diane Goldenberg: Investigation
(equal); Project Administration (supporting); Darby E. Saxbe:
Conceptualization (equal); Funding acquisition (lead); Writing—­
Review & Editing (supporting).
ORCID
Sofia I. Cardenas  https://orcid.org/0000-0001-7873-1215
Darby E. Saxbe  https://orcid.org/0000-0001-8951-4216
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