2012. Vol.3, No.6, 467-479
Published Online June 2012 in SciRes (
Copyright © 2012 SciRes. 467
Relationships as Regulators
Tiffany Field1,2
1Touch Research Institute, Medical School, University of Miami, Miami, USA
2Fielding Graduate University, Santa Barbara, USA
Received March 7th, 2012; revised April 7th, 2012; accepted May 10th, 2012
This paper reviews the Hofer (1984, 1996) and Field (1985, 1994) models on relationships as regulators,
suggesting that relationships regulate optimal stimulation and thereby modulate arousal levels and attenu-
ate stress. In these models, the behavioral, physiological and biochemical rhythms of individuals become
synchronized within close relationships like mother-infant and peer relationships both in human and ani-
mal species, and they become more coordinated over time, with some potentially remaining stable, much
like zeitgebers. Hofer supports his model by data on infant rat separation stress and Field describes “psy-
chobiological attunement” between human infants and their mothers and between young peers. This re-
view revisits the “relationships as regulators” model, summarizing studies on relationships between
non-depressed versus depressed mothers and their infants, between infant, preschool and preadolescent
friends versus acquaintances and between happily versus unhappily married couples. Although some be-
havioral and physiological data support Hofer’s and Field’s “relationships as regulators” model, many
studies on relationships have focused instead on the effects of separation or loss. Both Hofer and Field
suggest that the real question is “what was there about the relationship that was then missing after the
loss?” Future research could address the question of potential mediators and underlying mechanisms for
relationships becoming regulators. Potential mediators are explored here including mirror neurons, affec-
tive priming, imitation and empathy. The individuals’ rhythms and the attraction to others’ rhythms as
regulators may be an epigenetic programming phenomenon, suggesting both genetic and early experience
effects that endure across development.
Keywords: Relationships; Psychobiological Attunement; Arousal; Separation
This paper reviews models on relationships as regulators ad-
vanced by Hofer (1984, 1996) and Field (1985, 1994). In their
model, relationships are seen as regulating optimal stimulation
and arousal levels for the purpose of controlling stress. This
phenomenon can be seen in behavioral, physiological and bio-
chemical synchrony in relationships across development from
mother-infant interactions to young peer interactions to those of
older couples. Much of the literature has focused on the effects
of separation and loss rather than the mediating variables or the
ways in which relationships become regulators. Some potential
mediators are reviewed here including mirror neurons, affective
priming, imitation and empathy. Examples are given of early
mother-infant interactions from different species as illustrative
of the epigenetic programming that may contribute to an indi-
vidual’s rhythms and the attraction to others as regulators.
Hofer (1984, 1996) and Field (1985, 1994) advanced models
on relationships as regulators of stimulation and arousal modu-
lation and tested them on mother-infant rat and mother-infant
human relationships. Although these models inspired a signifi-
cant body of research, they have not been embraced by the
scientific community. Neuroscience data have suggested poten-
tial mediators for relationships as regulators including mirror
neurons, affective priming, imitation and empathy. This paper
reviews data on those models and suggestions for future re-
In his seminal paper on “relationships as regulators”, Hofer
described how he discovered this model when the mother rat
was separated from her offspring, and distress cries and phy-
siological disorganization ensued (Hofer, 1984). He referred to
these changes following the separation as “perhaps resulting
from withdrawal of specific sensory motor regulators”. He also
alluded to the sensory deprivation of explorers, shipwrecked
sailors, prisoners and those in solitary confinement studies in
which similar chronic symptoms occurred. He described the
behavior following the loss of another person as desynchroni-
zation. As Hofer noted, “…nonverbal signals, mannerisms,
tones of voice, gestures, facial expressions, brief touches, and
even the timing of events and pauses between words may have
physiological consequences, often outside of awareness” (Hofer,
1984). He concluded that paper with a note on the importance
of looking at the relationship “before the loss occurred rather
than beginning after the loss”.
Hofer later posed the question “How can the absence of
something or somebody cause such disturbance?” (Hofer, 1996).
He cited several examples from animal models including his
own work on providing heat as a mother substitute for infant rat
pups as well as the work of others on the moving terrycloth
surrogate mother for Rhesus monkey infants who had become
disorganized following separation from their mothers (Mason
& Berkson, 1975). Several neuroscientists have presented data
showing the survival value of the mother rat’s tongue licking
for excretion and for increased growth hormone in the heart,
liver and brain as well as for “turning-on the growth gene” (see
Schanberg & Field, 1987, for a review). Further, increased
tongue licking and grooming (LG) and arched-back nursing
(ABN) by rat mothers have altered the offspring’s glucocorti-
coid receptors in the hippocampus (Weaver et al., 2004). Off-
spring of mothers that showed high levels of LG and ABN were
found to differ in DNA from those with low levels. These dif-
ferences emerged over the first week of life, were reversed with
cross-fostering and persisted into adulthood. They were also
associated with altered glucocorticoid receptors observed among
the infant rats following maternal separation.
Hofer also borrowed examples from the human contact lite-
rature to make his point that physical contact had organizing
effects. He noted the synchrony in menstrual cycles after
women started living in groups (McClintock, 1983; Weller &
Weller, 1993), how social interactions facilitated recovery from
jet leg (Klein & Wegmann, 1974), and how, in contrast, sensory
deprivation could have extremely disorganizing effects (Heron,
1961). He also referred to external regulators as substituting for
a natural regulator, citing an example from our research on
massaging preterm infants to reduce touch deprivation while
the preemies were in incubators separated from their parents
(Field, Schanberg, Scafidi, Bauer, Vega-Lahr, Garcia et al.,
1986). However, as Hofer suggested, the supplemental stimula-
tion may not replace the normal sensory motor stimulation that
would have taken place within the mother’s uterus. Again, he
suggested “looking carefully for exactly what was lost when
loss occurs”.
A Deficit Model of Loss
Human bereavement has been characterized by similar be-
haviors including agitation, crying, aimless activities/inactivity,
sighing, respiration and muscular weakness (Shear & Shair,
2005). These authors quoted Hofer from his 1996 paper saying
that “The central characteristic of the disturbance is the failure
of the normal smooth modulation and coordination of affect,
behavior and physiological function into a stable daily pattern.
This is felt by the individual as a sense of internal disorganiza-
tion. Visual tasks, attention, concentration, sleep, food intake,
and mood become fragmented” (Shear & Shair, 2005: p. 582).
Shear and Shair (2005) cited many studies of married cou-
ples who have different combinations of secure and insecure
attachment configurations, as if espousing the Bowlby (1982)
attachment model. Although, midway through their paper, they
returned to the important Hofer statement that “…disrupted
hidden biobehavioral regulators may also cause problems for
bereaved people.” For example, some have shown that both the
frequencies of performing simple daily activities and the regu-
larity with which these activities are performed are an impor-
tant part of circadian rhythms that get disrupted with loss of the
partner (Monk, Houck, & Shear, 2005). Dysregulation of the
system can result in dysphoric emotions as well as disrupted
physiological functioning. Disturbance in the pattern of daily
activities could occur during bereavement because of the loss of
stimulation and arousal modulation provided by the partner
during those activities, much like the zeitgeber provided by the
circadian light/dark cycle (Field, 1985). Consistent with this
idea, Monk et al. (2005) found significant reductions in social
rhythm activity levels in patients with complicated grief (Monk
et al., 2005). Thus, some researchers have supported Hofer’s
animal model data with research on humans experiencing rela-
tionships as regulators.
Social Pain
Research on social pain was also inspired by Hofer. For ex-
ample, Chen, Williams, Fitness, and Newton (2008) referred to
the statement by James (1950) “If no one turned around when
we entered, answered when we spoke, or minded what we did,
but if every person we met ‘cut us dead,’ and acted as if we
were non-existing things, a kind of rage and impotent despair
would ere long well up in us, from which the cruelest bodily
tortures would be a relief” (James, 1950). James argued that
people would prefer physical over social pain (Chen et al.,
As Chen et al. (2008) further noted in a paper “When hurt
will not heal” four studies documented that social pain was as
real and intense as physical pain. As these authors suggested,
the social pain system may have “piggy backed” on the brain
structure that evolved earlier for physical pain. Individuals in
the se studies relived and re-experienced social pain more readily
and more intensely than physical pain, and, they performed
worse on cognitively demanding tasks after they relived social
pain than physical pain.
Functional magnetic resonance imaging studies confirmed
that social pain was equivalent to physical pain (Eisenberger,
Lieberman, & Williams, 2003; Singer, Seymour, O’Doherty,
Kaube, Dolan, & Frith, 2004). In the Eisenberger et al. (2003)
study, social pain like physical pain increased activity in the
anterior cingulate cortex and the right ventral prefrontal cortex.
In the study by Singer et al. (2004), functional imaging was
conducted while participants experienced a painful stimulus
and compared it to the same painful stimulus being experienced
by a loved one who was present in the same room. Again, the
anterior cingulate cortex was activated when the participants
perceived pain and also by a signal that a loved one experi-
enced pain. The activation of this region also correlated with
empathy ratings.
Social pain has also been illustrated by data showing the
similarity of heartbreak or a broken heart and real heart attacks
(Wittstein, Thiemann, Lima, Baughman, Schulman, Gersten-
blith, et al., 2005). In this study, the pain and the other symp-
toms after loss of a loved one were so similar to a real heart
attack that physicians were unable to differentiate the two syn-
dromes without performing an angiogram. The physical pain in
the heart or chest, a condition they called “broken heart syn-
drome” is thought to result from a release of catecholamines by
the brain following the trauma of breaking up or losing some-
one. The catecholamines reportedly weakened the heart muscle
and, although the heartache simulated symptoms of a heart
attack, those with broken heart syndrome typically had fewer
risk factors for heart disease, and they usually recovered faster
than those who had real heart attacks (Wittstein et al., 2005).
Although significantly elevated norepinephrine and epinephrine
levels were noted in the bloodstream of the individuals with
broken heart syndrome, and although they experienced symp-
toms similar to a real heart attack including chest pain, fluid in
the lungs, shortness of breath and heart failure, the angiograms
revealed no blockages in the arteries of the heart (Wittstein et
al., 2005). Also, blood tests failed to reveal elevated levels of
cardiac enzymes that get released into the bloodstream from
damaged heart muscle during real heart attacks. Again the focus
was on loss, which is understandable given that the broken
heart syndrome was precipitated by loss.
Copyright © 2012 SciRes.
Psychobiological Attunement
In a paper similar to Hofer’s (1984) paper, relationships as
regulators were referred to as “Psychobiological Attunement”
(Field, 1985). Many of the studies reviewed there also focused
on lost relationships rather than the critical qualities of rela-
tionships. For example, we studied separations between moth-
ers and infants (when mothers were hospitalized for childbirth),
separations between young peers (who were moved to new
classes or new schools) and the romantic break-ups between
university students.
Mother-Child Separations
In the childbirth study, mothers were separated from their
infants, toddlers or preschoolers for the birth of another child
(Field & Reite, 1984). The children were agitated during their
mothers’ hospitalization, showing increased negative affect,
activity level, heart rate, night wakings and crying. Longer than
usual periods of deep sleep at this stage were interpreted as
conservation withdrawal.
After the mother returned, decreases were noted in positive
affect, activity level, heart rate, and active sleep, effects that are
suggestive of depression. The parents also reported illnesses,
clinging and aggressive behaviors as well as changes in eating,
toileting and sleep patterns. Typically, the mothers were tired,
and some experienced postpartum depression, suggesting that
the mother remained unavailable to the child despite her physi-
cal presence. Inevitably, the mother-child relationship was al-
tered by the arrival of the new sibling. The children were clearly
agitated by being separated from their mothers even though
they were cared for by their fathers. The fathers may not have
been providing optimal stimulation or modulation of their chil-
dren’s arousal because of their lesser experience with the
child’s stimulation and arousal modulation needs. The chil-
dren’s depression could have been a homeostatic mechanism
offsetting the arousal or agitation, or it might have resulted
from inadequate stimulation.
We then compared the children’s responses to separations
due to their mothers’ hospitalizations for the birth of another
child and separations for their mothers’ conference trips to ex-
plore whether it was the separation per se that was stressful or
the altered parent-child relationship following the birth of the
sibling (Field, 1991). As can be seen in Table 1, a number of
significant differences emerged. The parents reported that more
sleep and behavior problems occurred during the hospital than
the conference trip separations. In addition, less smiling was
noted during the play observations, and the children spent a
greater proportion of their nap time in active sleep. This latter
difference was interpreted as conservation withdrawal. The
children’s greater agitation during the hospital as opposed to
the conference separations may have exhausted them more,
leading to more sleep. Following the return of the mother, the
parents continued to report more sleep and general behavior
problems in their children following the hospital as opposed to
the conference trip separations. Those children also showed less
smiling, less fantasy play and fewer positive verbal interactions.
Thus, the hospital separations were more stressful for the chil-
dren than the separations for conference trips, possibly because
the children were anticipating the arrival of a new sibling that
had been explained by the parents as well as the children’s
anticipated change in their relationship with their parents,
Table 1.
Means for children’s behaviors observed during separation and after the
mother’s return from a conference trip versus a hospitalization for the
birth of a sibling (all group mean differences significant at p < .05).
(Adapted from Field, 1994) .
Type of Se paration
Observation Period Conference Trip Hospitalization
Sleep proble ms (rating) 1.0 2.4
Behavior problems (ra t ing) .7 1.6
Smiling (% time ) 7.4 2.7
Active slee p (% time) 4.3 10.8
After mother’s return
Sleep problems (rating) .6 2.4
Behavior problems (ra t ing) .8 1.6
Smiling (% time ) 8.9 5.4
Positive verbal interaction (% time) 13.1 4.9
Fantasy play (% time) 38.7 23.2
namely having to now share those relationships with their sib-
ling. Separation from parents has been linked to stress re-
sponses including elevated cortisol levels that have been noted
during daycare versus being at home, especially when experi-
encing low quality daycare where the separation from parents is
particularly stressful (Geoffrey, Cote, Parent, & Seguin, 2006).
A meta-analysis has also shown higher cortisol levels during
daycare versus being at home (Vermeer & van Ijzendoorn,
Infant-Peer Separations
Children show similar symptoms when they lose each other,
as was observed in a study on separation stress of nursery
school infants and toddlers graduating to new classes (Field,
Vega-Lahr, & Jagadish, 1984). The play behaviors and sleep
patterns of infants (M age = 15 months) and toddlers (M age =
2 years) were observed during the first and fourth week of the
month preceding and following their graduation to new nursery
classes. As compared to baseline, observations during the week
preceding graduation and the week following graduation to a
new class revealed greater amounts of fussing, verbal interac-
tion, physical contact (both affectionate and aggressive), wan-
dering, and fantasy play. Activity levels were elevated and
absenteeism was more frequent. Latency to sleep was longer,
more crying occurred preparatory to sleep and a lesser percent-
age of nap time was spent sleeping. The infants as compared to
the toddlers were less agitated just prior to graduation, but more
agitated during the first week in their new class. Those in-
fants/toddlers who moved to a new class with a close friend
were less distressed by the transfer than those who did not
move with a close friend.
Breakup Distress in University Students
The distressful effects of losing a relationship as a regulator
are further illustrated by research on breakup distress in univer-
sity students after losing a romantic partner. In the first of our
series of studies on university students’ breakup distress, 37%
Copyright © 2012 SciRes. 469
of the variance on Breakup Distress Scale scores was explained
by depression, feelings of betrayal, having less time since the
breakup and assigning a higher rating to the relationship that
had been lost (Field, Diego, Pelaez, Deeds, & Delgado, 2009).
In a study on a second sample, intrusive thoughts contributed to
28% of the variance (Field, Diego, Pelaez, Deeds, & Delgado,
2012a). Depression and sleep disturbances were also related to
breakup distress in this sample. Other negative emotions and
behaviors included anxiety, anger, disorganized behavior and
inferior academic performance (Field, Diego, Pelaez, Deeds, &
Delgado, 2012b). Studies on the reasons for breakups revealed
that insecurity (Pelaez, Field, Diego, Deeds, & Delgado, 2011)
and loss of intimacy (Field, Diego, Pelaez, Deeds, & Delgado,
2010) were the most significant relationship problems leading
to breakup. Although female students typically reported greater
breakup distress, these studies are limited in their generalizabi-
lity because the sample was primarily Hispanic female psycho-
logy students. Nonetheless, the data highlight the negative ef-
fects of breakup distress for university students.
The Loss of Stimulation and Arousal Modulation
In the model we called “psychobiological attunement” or
“being on the same wavelength,” each partner provides mean-
ingful stimulation for the other and has a modulating influence
on the other’s arousal level (Field, 1985). Both excessive
stimulation and inadequate stimulation (according to the indi-
vidual’s thresholds for optimal stimulation) are aversive, while
stimulation that brings or keeps an individual within an optimal
arousal zone is considered reinforcing. Excessive stimulation
tends to produce over-arousal that is aversive, and too little sti-
mulation leads to boredom and sub-optimal levels of arousal
that are also aversive. Thus, loss of a relationship means the
loss of both activating and calming stimulation. The individual
experiencing the loss would be expected to fluctuate or vacil-
late between one end of the continuum of under-stimulation to
the other end of the continuum of over-stimulation and not be
able to regulate or modulate these levels to experience optimal
levels of stimulation/arousal.
Other terms we have used are synchrony between partners
and sharing rhythms. Synchrony is a term that is usually ap-
plied to the matching of rhythms in the physiological or physi-
cal activities of individuals. Examples of this can be seen in
partners who are extremely close tending to coordinate their
physical movements and expressions while talking, and their
cortisol cycles tending to be synchronized on weekends when
they are together (Field, 1985). Thus, attunement or “being on
the same wavelength” happens for behavioral, physiological,
and even biochemical rhythms of the individuals in the rela-
tionship. Seemingly, this could happen if each partner of the
dyad is sensitized or sensitive and responsive to each other’s
stimulation and arousal-modulation needs, as in a feedback
loop, and each accordingly adjusts his or her behavior to facili-
tate the synchrony of the dyad.
Physical intimacy can enhance attunement (Field, 2010b). By
physical closeness/touch, individuals can learn each other’s
stimulation and arousal-modulation needs. Although it is possi-
ble to self-regulate in the absence of an intimate partner, it may
not be as easy or effective. When a partner is no longer there,
and touch-stimulation for example is missing, dysregulation
may occur. Disruption of attunement may lead to physiological
disorganization, to depressed behavior in some cases, and to
changes in the immune system. Separation from the relation-
ship may result in physiological and behavioral dysregulation
simply because the source of stimulation and arousal modula-
tion that maintained the individual’s behavioral and physio-
logical organization is no longer present.
Examples of relationships as regulators or attunement in re-
lationships can be found across the lifespan, and developmental
changes may occur in the thresholds for stimulation and arousal
modulation. For example, thresholds for stimulation may be
lower in infancy and old age, thus requiring lower levels of
stimulation and greater arousal modulation (Field, 2010b). The
immature infant is more readily aroused and more needy of the
parent’s arou sal modulation.
Parent-Infant Inter actions
The infant and the parent appear to synchronize their beha-
viors and their gaze patterns in tandem, as in a dance, with the
parent necessarily being sensitive to changes in the infant’s
arousal and the infant, in turn, responding to the parent’s sensi-
tive behaviors. This phenomenon has been demonstrated by
many researchers (Papousek, 2007; Stern, 2004; Trevarthen,
1979; Tronick, 2003). In the Papousek (2007) study, for exam-
ple, infants in one group showed signs of difficult temperament
including hypersensitivity and problems in arousal regulation.
They were able to keep a certain balance as long as they re-
ceived intense stimulation but became disorganized in response
to the lack of stimulation. The mothers responded contingently
with intensified stimulation to any sign of fatigue or hypo-
arousal on the part of the infant in order to avoid excessive
crying. But they failed to provide what these inconsolable in-
fants would have needed the most, namely reduction of stimu-
lation, calming and settling to sleep. Infants in another group
had already learned to use more or less dysfunctional regulatory
strategies (gaze avoidance, staring and withdrawal) for coping
with their mothers’ highly intense, intrusive stimulation. Par-
ents who show sensitivity to the affective and attentive rhythms
of their infants are able to adjust their behaviors and accord-
ingly bring the infant to a more organized state (Field, 2007).
Because of the immaturity of the infant, much of the synchrony
of the interaction is dependent on the parent. If parents fail to
provide optimal levels of stimulation and modulate their stimu-
lation as the infant’s arousal level rises, the infant begins to
show more gaze aversion and fussiness, thus disrupting the
synchrony of their interaction (Field, 2007).
Elevated heartrate, gazing away and negative affect of in-
fants during their interactions with parents may relate to an
information overload and elevated arousal levels deriving from
excessive stimulation (Field, 2007). In their natural attempts to
elicit positive affect, some parents provide excessive stimula-
tion and fail to modulate arousal as their infants become dis-
tressed (Paponsek, 2007). As we have also noted, the heartrate
curves of mothers and infants parallel each other during inter-
actions, with increases in heartrate noted in both mothers and
infants during stressful, disturbed interactions and parallel de-
creases during more harmonious interactions, suggesting phy-
siological attunement (Field, 2007).
In a study by Feldman and Eidelman (2007), mother-infant
and father-infant gaze synchrony were associated with greater
vagal activity in the infants. The authors suggested that when
the parents were better able to coordinate their gaze with their
infants’ gaze, the infants showed greater vagal activity. Parents’
Copyright © 2012 SciRes.
regulatory activity would invariably contribute to regularity of
infant behavior. In another recent study, the regularity of infant
behavior at age one month based on parents being “regulators”
significantly predicted the child’s attentiveness and anxiety
levels (negative correlation) at five different time points from
kindergarten through ninth grade (Monk et al., 2010).
High-risk parents such as depressed mothers have difficulty
modulating their stimulation and being in synchrony with their
infants (Field, 2007). In a study on depressed and non-de-
pressed mother-infant dyads (Field, Healy, Goldstein, & Gu-
thertz, 1990) interaction synchrony was assessed when the in-
fants were 3-months-old. The mothers’ and infants’ attentive
and affective behavior states were coded on a continuum from
negative to positive including angry, disengaged, attentive and
playful states. The non-depressed mothers and infants spent
more time together in positive behavior states, and the de-
pressed mothers and their infants shared more time together in
negative behavior states. Shared behavior states occurred less
often for the depressed dyads than for the non-depressed dyads
(see Figure 1).
In another study, both behavioral states and heartrate were
subjected to cross-spectral analysis (Field, Healy, & LeBlanc,
1989). The data were analyzed to determine the coherence of
the mothers’ and infants’ behavior and the mothers’ and in-
fants’ heart rate. Coherence has been used as a statistical term
to indicate concordant or synchronous activity between two
data streams independent of the variable measured. The non-
depressed mothers and their infants had greater coherence in
their behaviors than the depressed dyads. Models of the wave
forms of these mother-infant behavior states for the non-de-
pressed and depressed dyads are given in Figures 2 and 3. The
model wave forms illustrate the rhythmic structure of the inter-
action. Examples of synchrony can be seen at the points where
the waveforms of the mothers’ and infants’ behavior states are
similar in direction and form. The non-depressed mothers’ and
infants’ heartrate were also more coherent than the heartrate of
the depressed mothers and infants. Greater coherence was also
shown in the non-depressed mothers’ heartrate and their in-
fants’ behaviors which was not surprising given that non-de-
pressed mothers are noted to be more sensitive/responsive to
their infants’ behaviors and that appears to be reflected in their
heartrate responses to their infants’ behaviors.
This model of an interactive “dance” characterized by syn-
chrony and attunement has been challenged by data suggesting
that synchrony is achieved less than 30% of the time in mother-
infant dyads (Tronick, 2003). Tronick and colleagues have
devoted more attention to how infants learn interactive “repair”.
Nonetheless, the synchrony/attunement model has continued to
serve as a criterion for harmonious early interactions.
Concordance in Play Behaviors and Physiology of
Preschool Friends
Concordance has also been noted among young friends in
several studies. For example, close friend preschool pairs show
concordance in their play behavior (Roopnarine & Field, 1984).
Concordance has also been noted in the heartrate patterns of
kindergarten children playing tog ether in their classroom (Wade,
Ellis, & Bohrer, 1973). Still another example is that the cortisol
cycles of preschool playmates have been notably concordant
during school days, but not on weekends (Montagner, Restoin,
& Henry, 1982).
Figure 1.
Mean percent time mothers and infants shared behavioral states
(standard deviations are indicated by vertical lines and asterisks in-
dicate statistically significant differences between adjacent bars).
(Adapted from Field et al., 1990).
Figure 2.
Similar wave forms for nondepressed mothers and their infants
suggest greater concordance in their behaviors. (Adapted from
Field et al., 1989).
Figure 3.
Wave forms for depressed mothers and their infants moving in
opposite directions suggest less concordance of their behaviors.
(Adapted from Field et al., 1989).
Copyright © 2012 SciRes. 471
In a study we conducted, preschool close friends were identi-
fied by behavioral observations of classroom play, by socio-
grams and by child and teacher sociometric ratings (Goldstein,
Field, & Healy, 1989). Preschool close friend pairs as compared
to acquaintance pairs showed greater concordance on play be-
haviors including parallel play and imitation (see Table 2).
Greater concordance was also noted in the heartrate of close
friend pairs than acquaintance pairs. And, finally, the cortisol
levels of close friend pairs were more concordant than those of
acquaintance pairs. In addition, cortisol levels were more ele-
vated when the children were playing with their acquaintances
than when they were playing with their friends, suggesting that
their play interactions with close friends were less stressful than
they were with acquaintances. The greater concordance of be-
havior, heartrate and cortisol suggests that behavioral, physio-
logical, and biochemical attunement can occur in close rela-
tionships between children as early as preschool age.
In a similar study by our group, preschoolers were asked to
identify their preferred playmates (Roopnarine & Field, 1984).
Analyses conducted on close friend pairs suggested that they
spent a greater percent time in fantasy play and verbal interac-
tion (positive, negative and neutral) as well as time spent mak-
ing requests, using imperatives and directing and submitting to
each other (see Table 3). As we suggested, it is not clear
whether the children were initially matching on these behaviors
or whether the matching of behaviors evolved during the course
of their friendship formation. These data suggest, nonetheless,
that close preschool friends appear to interact very similarly.
Concordance of Behavior and Physiology in
Pre-Adolescent Friends
Surprisingly very little research has been conducted on the
concordance of face-to-face interaction behavior and physio-
logy in close friend pairs among older children and adolescents.
In our research on pre-adolescents, comparisons were made be-
tween close friend pairs and acquaintance pairs to determine
whether their behavior and physiology were synchronized
(Field, Greenwald, Morrow, Foster, Guthertz, Healy et al.,
1992). The pre-adolescents reported more positive feelings and
greater liking for the interactions they experienced with close
friends versus acquaintances. The close friend pairs were more
attentive toward each other, more affectively positive, more
vocal, more active and more playful with each other. The group
of best friend dyads also had lower cortisol levels, suggesting
that they were less stressed by their interactions (see Table 4).
Table 2.
Concordance for behaviors of preschoolers interacting with friends and
with acquaintances. Smaller numbers indicate greater concordance (or
less variance). (Adapted from Gol dst ei n e t a l., 1989).
Variable Friends Acquaintances p
Fantasy play 132.7 77.6
Solitary play 145 .2 143.4
Parallel play 2.1 18.1 .001
Commands 82.9 145.7
Requests 16.1 42.8 .05
General conversation 66.0 126.9
Following/imitating 3.0 8.4 .05
Table 3.
Percent time individuals spent in different behaviors when playing with
their close friends versus with acquaintances (children who were not
close friends). Interobserver reliability coefficients in parentheses. (Ad-
pted from Roopnarine & Field, 1984).
Behaviors Children with
Friends Children without
Friends p
Fantasy play (88) 25.25 6.83 .05
Positive Verbal
Interaction (96) 24.88 10.00 .005
Negative Verbal
Interaction (90) 16.62 3.58 .005
Neutral Verbal
Interaction (86) 50.69 29.17 .005
Statements (93) 61.86 33.58 .005
Requests (1 00) 2.37 .00 . 05
Imperatives (96) 19.44 8.08 .05
Questions (96) 6.62 4.17
Directing (99) 28.31 12.33 .01
Submitting ( 100) 4.25 1.16 .01
Giving (99) 3.06 5.00
Taking (99) 1.69 3.67
Sharing (98) 12.44 6.83
Helping (10 0 ) 1.94 1.83
Imitating (100) 6.56 4.08
Watching (88) 12.13 35.67 .005
Fighting (95) 12.06 11.08
Greater concordance was noted within friendship pairs for at-
tentiveness, vocal activity, activity level, physical attractiveness,
involvement and relaxation ratings. These data suggest that
close friend pairs not only have more fun during their interac-
tions (i.e. they like them more and they feel more positive about
them), but they also show greater similarity or concordance on
a number of behaviors.
Coordinated vocal activity has also been noted in best friend
pairs. In a study we conducted on pre-adolescent best friend
versus acquaintance pairs, vocal activity was coded by input-
ting the audio signals from each person into a computer system
known as the Automated Vocal Transaction Analyzer (Feld-
stein & Field, 2002). Vocal states were then determined in-
cluding speaking turns, switching pauses and simultaneous
speech or joint speech which was categorized as non-interrup-
tive or interruptive. The best friend pairs tended to coordinate
the durations of their vocal behaviors with each other more
often than the acquaintance pairs, and the girl-girl pairs coordi-
nated the durations of their pauses significantly more often than
the boy-boy pairs, suggesting that the girl-girl pairs may have
been more attentive and involved in their interactions than the
boys were with each other.
Interpersonal Regulation in Adults
Most of the interpersonal regulation studies on adults have
been conducted with married couples by Gottman and his col-
leagues (Gottman & Levenson, 2002). Many of the co-regu-
lation behaviors that have been observed in mother-infant in-
teractions and child-child interactions have not yet been ex-
plored during marital interactions such as the switching pauses
Copyright © 2012 SciRes.
Table 4.
Means for self-ratings, observer ratings, interaction behavior states, joint
states, and biochemical/physiological measures of friends and acquain-
tances among pre-adolescents. ( Adapted from Field et al., 1992).
Friends Acquaintances
Measure M SD M SD p
Feelings 4.1 .5 3.8 .5 .01
Liking 3.8 .8 3.5 .8 .005
Observer ratings
Attentiveness 3.3 .6 2.5 .7 .001
Affect 3.0 .9 2.3 .6 .001
Vocalizations 3.1 .7 2.5 .6 .001
Activity leve l 2.7 .8 2.1 .9 .001
Involvement 3.8 .7 2.6 .8 .001
Relaxation 3.7 .6 2.9 .7 .001
Playfulness 2.6 1.2 1.8 1.0 .001
Global rating 3.5 .8 2.3 .8 .001
Attractiveness 3.0 1.5 2.5 1.6
Behavior states (% time)
Disengaged 1.2 2.8 5.7 9.2 .001
Neutral 15.7 19.0 46.1 23.2 .001
Interested 59.1 19.4 46.5 22.7 .005
Animated 7.7 8.8 .9 3.4 .001
Playful 16.4 19.5 .9 3.9 .001
Joint states (% time)
Disengaged .0 .0 .4 .4 .005
Neutral .8 .5 1.2 .5 .05
Interested 41.3 21.7 18.9 13.9 .005
Animated 2.3 .4 .2 .2 .005
Playful 1.8 .5 .4 .7
Physiological measures
Cortisol levels .60 .34 1.06 1.0 .001
Heart peri od 660.1 73.0 660.4 73.6
Vagal tone 6.1 1.1 6.1 1.0
and speaking turns just described for preadolescents. Studies
have been conducted on the matching of positive and negative
affect states and on the linkage of physiological activity (Car-
rere & Gottman, 1999; Gottman & Levenson, 2002; Gottman et
al., 2003). Specifically, co-regulation has been documented for
behavioral states, for physiological measures including hear-
trate and galvanic skin response (Levenson, Carstensen, &
Gottman, 1994), for biochemical measures such as cortisol
(Loving, Crockett, & Paxson, 2009) and for the relationships
between dysregulation or the absence of co-regulation and im-
mune and health measures (Robles & Kiecolt-Glaser, 2003). In
addition, comparisons have been made across gender, across
different age groups and across similar and dissimilar personal-
ity couples.
Behavioral Regulation
Although behavior matching has not been studied in adults to
the same extent as it has in mother-infant dyads and in pre-
school and preadolescent friend pairs, the linkage between
positive affect in partners and between negative affect in part-
ners has been studied by Gottman and his colleagues (e.g. Car-
rere & Gottman, 1999). Others have studied interpersonal
regulation defined as changing behaviors so as to coordinate
with one another (Rusbult, Kumashiro, Kubacka, & Finkel,
2009). Still others have talked about partners who are attached
to each other providing affect regulation by “offering comfort
and support, making us laugh, communicating empathy, ex-
tending a listening ear, distracting us from our problems, and
sharing in our successes” (Diamond, Hicks, & Otter-Henderson,
2008). They refer to the importance of day to day proximity,
offering data that those who have longer phone conversations
during separations have less relationship distress. As Diamond
et al. (2008) have suggested, interpersonal regulation is achi-
eved by individuals modulating their affective responses to
internal and external stimuli or by partners reciprocally regu-
lating one another’s psychological and physiological states.
Physiological Regulation
Co-regulation of physiological states has been studied by a
number of investigators. In one model on co-regulation of phy-
siology, the authors suggested that co-regulation relies heavily
on a model of co-mingled physiology between romantic part-
ners and has been variously called co-regulation, attunement
and social zeitgebers (Sbarra & Hazan, 2008). These authors
described a model very similar to those models that had been
advanced earlier by Hofer (1984) and by Field (1985). Co-regu-
lation was said to be an up or down-regulation of the partners’
physiological arousal which was considered a property of the
relationship as opposed to either individual alone and was de-
scribed as occurring via several modalities (touch, smell, eye-
contact, cognition). Sbarra and Hazan (2008) also suggested
that sexual and physical intimacy are the strongest physiologi-
cal reward systems for romantic partners, “providing the most
efficient and metabolically cost-effective means of regulating
affect by synchronizing physiological systems to those of their
Several studies have been conducted on the concordance of
adult partners’ heartrate, pulse transit time, skin conductance
level and body movements (Levenson & Gottman, 1983, 1985,
1992, 1994). They assessed the degree to which each spouse’s
physiological activity across those four measures could be pre-
dicted from the other’s activity. Physiological interrelatedness
or what they referred to as linkage between the spouses ac-
counted for over 60% of the variance in marital satisfaction
(Levenson & Gottman, 1983). Over 80% of the variance in
satisfaction change over a three-year-period was accounted for
by heartrate. Physiological linkage was a better predictor of
current levels of marital satisfaction, and mean physiological
levels were better predictors of future levels of marital satisfac-
tion. The more aroused the partners were, the greater the satis-
faction declined. As marital satisfaction declined, the husband’s
and wife’s health declined. Although other factors could have
contributed to the health decline, a significant amount of the
variance in health was explained by marital satisfaction. Inter-
Copyright © 2012 SciRes. 473
estingly, in the paradigm used by this group, a kind of physio-
logical substrate was identified (Jacobson & Gottman, 1999).
Although causality was not implied in these results, when one
spouse rated videotapes of the other spouse, if the rater’s
physiological responses matched those of the spouse being
observed on the video, the rater was more accurate in predicting
the target spouse’s feelings.
Another example of relationships as regulators is that social
interaction moder a t e s t he relationship between depressive mood
and heart rate variability (HRV) or vagal activity (indicators of
calmness) (Schwerdtfeger & Friedrich-Mai, 2009). In this study,
when depressed individuals were alone, they showed lower
HRV and more negative affect. When they were interacting
with a partner, family member or friend, their HRV increased,
as did their positive affect. The control group’s social interac-
tions with strangers or colleagues, on the other hand, were not
accompanied by higher HRV.
Biochemical Regulation
Perhaps the earliest signs of biochemical regulation can be
seen in the mirroring of the mother’s prenatal biochemical pro-
file by the neonate. In several studies we have documented si-
milar biochemical profiles between pregnant women (both de-
pressed and non-depressed) and their neonates including nore-
pinephrine, serotonin, dopamine and cortisol (see Field, Diego
& Hernandez-Reif, 2010, for a review). Functional magnetic
resonance imaging has shown that romantic love in adults acti-
vated dopamine-rich areas of the brain associated with reward
and motivation in at least one study (Aron et al., 2005). Roman-
tic relationships have also been accompanied by increased
nerve growth factor and increased cortisol, but also by in-
creased oxytocin (Loving, Crockett, & Paxson, 2009). In an-
other study, physical contact between couples contributed to
oxytocin increases, which was not surprising, as the oxytocin
responses to physical contact are connected to dopaminergic
reward systems (Young & Wang, 2004). As oxytocin increased,
parasympathetic activity (calmness) increased and cortisol de-
creased. Those with more positive emotions and better sleep
had better health. These data suggest questions for further re-
search including “how co-regulation develops?” and “how si-
milar partners’ biochemical profiles become?”
Dysregulation and Its Consequences for Health and
Immune Func ti on
In a two-factor model, Gottman and Levenson (2002) sug-
gested two patterns that lead to dysregulation in couples in-
cluding an emotionally inexpressive pattern that is low in both
positive and negative affect (those being later divorcing couples)
and an emotionally volatile attack-defend pattern (those leading
to earlier divorce). They labeled the pattern of negativity the
“four horsemen of the apocalypse,” (the four horsemen being
criticism, defensiveness, contempt and stonewalling). Else-
where, Gottman and his colleagues described dysregulated in-
teractions as being high in negative affect, with heightened
arousal levels playing a role in the poor health of individuals in
distressed marriages (Jacobsen & Gottman, 1999).
Much of the work on the impact of poor relationships on the
immune syst em comes from Kiecolt-Glaser and her colleagues.
In one of their papers, they suggested that three primary physio-
logical pathways mediate the relationship between stressful
social relationships and health, those being cardiovascular, ne-
uroendocrine and immune function (Robles & Kiecolt-Glaser,
2003). Increased blood pressure and heartrate accompanied
aroused interactions. In contrast, daily contact between those
with a good relationship led to decreased diastolic blood pres-
sure. Others have noted decreases in both systolic and diastolic
blood pressure in those having daily interactions (Gump, Polk,
Kamarck, & Shiffman, 2001; Holt-Lunstad, Uchino, Smith,
Olson-Cerny, & Nealey-Moore, 2003). In the Robles and Kie-
colt-Glaser (2003) study, aroused interactions were also associ-
ated with elevated epinephrine, norepinephrine, cortisol, ACTH
and growth hormone as well as decreased prolactin. Negative
interactions contributed to 20% of the variance in the change in
cortisol. In turn, there was a decrease in natural killer cells.
Ironically, impaired immune function has continued into sepa-
ration and divorce following a negative relationship including
higher antibody titres to the Epstein-Barr virus and decreased
natural killer cell activity (Powell, Lovallo, Matthews, Meyer,
Midgley, Baum et al., 2002). Increased inflammatory cytokine
production has also been noted (Black, 2002). This may relate
to the negative effects of continuing intrusive thoughts about
the distressed relationship and/or the loss of physical contact
and its interpersonal regulation effects (Field, 2009). Poorer
health habits, of course, confound the physiological effects on
immune function.
Similarity of Partners
It is not clear how partner relationships become co-regulate d.
One possibility is that partners become increasingly similar
across time so that one person is the reflection of the other, and
each becomes easier to read so as to feel co-regulated (Soto &
Levenson, 2009). These researchers showed that over time the
individuals of satisfied couples become increasingly similar in
their behavior, suggesting that similarity contributes to a posi-
tive marital status. Others have suggested that similarity be-
tween partners attracts them to each other in the first place and
leads to more persistent relationships versus breakups (Rusbalt,
Kumashiro, Kubacka, & Finkel, 2009).
Some have theorized that when children and adults interact
frequently with a given peer, they come to behave in similar
ways, and, in this way, they become physiologically attuned to
each other (Chapple, 1970; Warner, 1979). Colloquial expres-
sions characterize interaction synchrony between close friends
as “being in tune with each other” or “being on the same wave-
length”. However, very little research has been conducted on
the process whereby close friends become attuned to each
other’s behavior.
As Chapple (1970) theorized, each person in a close friend
dyad has a preferred “interaction tempo” that has been de-
scribed in terms of simple parameters such as cycle length and
percent time spent active. The partners are thought to influence
each other’s interaction tempos as they converse and try to
achieve smooth coordination. As Chapple (1970) has suggested,
similarities of their interaction tempo make this an easier task,
with partners becoming easily entrained to their interaction
cycles. The example he gives is that the cycle length for
speaker A would equal the length of speaker B with the percent
time talking totaling 100%. In those dyads, interactions would
be enjoyable, and the partners would be attracted to each other.
However, if the partners found it difficult to achieve smooth
coordination of cycles, resulting in long mutual pauses and/or
constant interruptions, they would then find their interactions
Copyright © 2012 SciRes.
less pleasant. This theory would suggest that as there is greater
coupling between partners’ behaviors and physiology, there
would be more positive affect and a greater liking between
partners. However, this the ory needs further testing.
Older couples are reputedly less aroused and express more
positive affect, which may relate to their longer relationships
and greater familiarity with each other (Levenson et al., 1994).
They are also more physically affectionate (Gottman, Coan,
Carrère, & Swanson, 1998). More physical touch might enable
greater sensitivity to reading each other’s signals and thereby
greater attunement (Field, 2010b). Still another characteristic of
older couples is that they display more humor which has been
related to greater happiness (Jacobson & Gottman, 1999). Cou-
ple humor in particular has been associated with more affec-
tionate and playful interactions in older couples (Driver &
Gottman, 2004).
Gender Differences
Throughout the literature, gender differences have been
noted for regulation, dysregulation and immune consequences.
Men reportedly have more negative affect which is correlated
with greater physiological arousal in men but not in women
(Levenson et al., 1994). Typically, when a male initiates an
issue, he notices his partner’s negative response at a much
lower threshold than a woman does, and men become more
angry than women when presenting an issue, making physio-
logical reactivity a greater issue for men than for women
(Gottman et al., 2003). It is not surprising, then, that men ex-
perience greater immune dysfunction (Robles & Kiecolt-Glaser,
2003). In contrast, if the marriage is distressed, women are
more likely to experience health-related problems (Jacobsen &
Gottman, 1999). This may relate to men being more attuned to
their own physiology and generally avoiding marital conflict
discussions whereas women are noted to start over 80% of
marital conflict discussions (Levenson et al., 1994).
Potential Underlying Mechanisms/Mediators
It is not clear how the synchrony/coherence/concordance pa-
tterns occur or what happens if they don’t occur. Potential un-
derlying mechanisms for coherence/concordance patterns in-
clude mirror neurons, affective priming, imitation and empathy.
As was noted by Papousek (2007), Rizzolatti and co-workers
have detected so-called mirror-neuron networks in the premotor
cortex of non-human primates which function to control goal-
directed or intentional action, but which are also activated and
resonate when a primate merely observes a conspecific or a
human carrying out the same goal-directed action (Rizzolatti,
Fadiga, Gallese, & Fogassi, 1996). According to neuroimaging
studies in adults and studies using event-related potentials in
infants, mirror neuron systems also exist and function in human
brains and most likely also in the brains of preverbal infants
(Arbib, 2005; Bauer, 2005; Rizzolatti, Fadiga, Fogassi, & Ga-
llese, 2002). They are currently discussed as the evolutionary
basis for human empathy, affective resonance, understanding
attention and intentions, observational learning and language
acquisition. They may also provide the neurobiological basis
for the phenomenon of newborn imitation, of mutual facial and
vocal mirroring, immediate coupling of perception and action,
and of early intersubjective affective sharing. Affective priming
has also been suggested as a kind of automatic response of
positive affect to an attachment figure (Banse, 1999), but failed
to reveal individual differences related to relationship satisfac-
tion. And empathy, or the accurate perception of signals has
also been suggested as a cross-cultural mechanism, although
physiological linkages appear to be less cross- cultural (Soto &
Levenson, 2009).
Potential mediators such as early imitation appear to exist
across species, although they take different behavior forms. For
examples, Suomi and his colleagues have demonstrated imita-
tion of facial gestures including lip smacking, tongue protru-
sions, mouth opening, hand opening and open/closing of eyes
(control condition) in neonatal rhesus macaques (Ferrari, Visal-
berghi, Paukner, Fogassi, Ruggiero, & Suomi, 2006). The mo-
ther macaques were thought by Suomi and his colleagues to
facilitate this imitation by their exaggerated facial expressions,
speech, mutual gaze and body contact (Ferrari, Paukner, Ionica,
& Suomi, 2009). They further labeled this as “regulation of
infant emotions” and as a precursor of more complex forms of
social exchange including perspective-taking and empathy (Fe-
rrari, Paukner, Ruggiero, Darcy, Unbehagen et al., 2009). In
another monkey species, they reported that Capuchin monkeys
preferred human imitators over non-imitators (Paukner, Suomi,
Visalberghi, & Ferrari, 2009). The monkeys, for example,
looked longer at imitators and spent more time in proximity to
The first report of human neonatal imitation by Meltzoff and
Moore (1977) showed neonates imitating tongue protrusion
followed by research we conducted demonstrating imitation of
exaggerated facial expressions including happy, sad and sur-
prised faces (Field, Woodsen, Greenberg, & Cohen, 1982).
Althouth these data were subsequently replicated (Heimann,
Laberg & Nordoen, 2006). It is not surprising that imitation
occurs in the human neonate given the already described stu-
dies by Suomi and his colleagues on imitation by infant mon-
keys, although considerable controversy has existed in the lit-
erature on neonatal imitation for several years. As Suomi (2006)
suggested, humans often unconsciously and unintentionally
imitate the behaviors of others during social interactions, which
appears to increase rapport, liking and empathy between inter-
action partners (Paukner et al., 2009). They further suggested
that this behavior matching leads to prosocial behavior towards
others and may have been “one of the mechanisms at the basis
of altruistic behavioral tendencies in the Capuchin monkeys and
in other primates including humans” (Paukner et al., 2009).
Epigenetic Programming May Contribute to
Individual s’ Rhythm s and the Attr act i o n to Others’
Rhythms as R e gulators
Epigenetic programming or the process whereby “the envi-
ronment interacts with the genome to produce individual dif-
ferences in the expression of specific traits” has been advanced
by Meaney and his colleagues (e.g. Bagot & Meaney, 2010).
According to Meaney and his group, the genome is progra mmed
by the epigenome. Epigenetic ‘mechanisms’ are thought to
mediate the effects of behavioral and environmental exposures
early in life, as well as susceptibility to disease later in life.
They suggest that in contrast to genetic sequence differences,
epigenetic aberrations are potentially reversible, raising the
possibility of interventions reversing epigenetic programming
problems (Szyf & Meaney, 2008).
Meaney and his colleagues have noted that adult rat offspring
Copyright © 2012 SciRes. 475
of mothers who showed greater pup licking/grooming had
greater hippocampal glucocorticoid receptor expression, more
complex dendritic structure and enhanced synaptic potentiation
(van Hasselt et al., 2011). The authors suggested, however, that
this literature has been based on studies where the total amount
of maternal care was directed towards the entire litter, thus
ignoring any potential for in-litter variation. In their study, in-
dividual differences were noted in the amount of licking/
grooming provided to individual pups (van Hasselt et al., 2011).
The pup licking/grooming score was positively correlated with
the already mentioned brain development variables, suggesting
that even moderate variability in early environments signifi-
cantly affected adult hippocampal function. These effects have
been reversed by cross-fostering, suggesting that they are de-
termined by epigenetic rather than genetic processes (McGo-
wan, Suderman, Sasaki, Huang, Hallett et al., 2011). Further,
variations of maternal behavior in the rat model have been as-
sociated with differences in estrogen-oxytocin interactions and
in dopamine levels which are involved in the establishment and
maintenance of social bonds (Shahrokh, Zhang, Diorio, Gratton,
& Meaney, 2010). And, post-weaning isolation reduced mater-
nal licking/grooming and oxytocin receptor binding in the off-
spring of high licking/grooming mothers, whereas social en-
richment enhanced exploration, licking/grooming behavior and
oxytocin receptor binding in low licking/grooming mothers
(Champagne & Meaney, 2007).
In several different studies, Meaney and his colleagues iden-
tified more than 900 genes that were stably regulated by ma-
ternal care (Weaver, Meaney, & Szyf, 2006). As this group
suggested, these studies “define a biological basis for the inter-
play between environmental signals and the genome in the
regulation of individual differences in behavior, cognition and
physiology” (Zhang & Meaney, 2010). The generalization of
this process across species and across development, however,
needs to be tempered by the observation that there is also re-
search showing differences across strains of the rat model and
epigenetic programming (Lester, Tronick, Nestler, Abel, Koso-
fsky et al., 2011).
Nonetheless, this research highlights the epigenetic pro-
gramming that may occur in early mother-infant interactions.
This may explain why mother-peer-reared monkeys are less
affected by stressors than peer-reared or surrogate-peer-reared
monkeys (Dettmer, Novak, Suomi, & Meyer, 2011). Suomi and
his colleagues also referred to gene-environment interactions
throughout development with respect to Rhesus monkeys and
humans (see Suomi, 2006 for a review). An example of their
research is that the short allele of the serotonin transporter gene
is associated with deficits in neurobehavioral functioning dur-
ing infancy and in poor controlled aggression and low serotonin
metabolism throughout juvenile and adolescent development in
monkeys who are reared with peers but not in monkeys who are
reared with their mothers and peers during infancy. Long sero-
tonin alleles appeared to dampen the adverse early attachment
relationships while “maternal buffering” appeared to reduce the
risk for those with the short alleles (Suomi, 2006).
Similar examples of maternal care as potential epigenetic
programming appear in the early mother-infant and father-
infant literature including our research on enhanced growth and
development in those infants receiving massage (see Field,
2010a, for a review). And, early interactions have been facili-
tated by touch, imitation and sensitive reading of cues by par-
ents, most especially in high-risk infants such as preterm in-
fants and infants of depressed mothers. The still-face (mother
remaining still-faced) interaction has been used as a model for
simulating maternal depression effects. Feldman and her col-
leagues illustrated maternal touch as a regulator during their
still-face interactions (Feldman, Singer, & Zagoory, 2010). This
paradigm of adding mother touch to reduce infant stress during
the still-face situation has been effectively used by both non-
depressed (Pelaez-Nogueras, Gewirtz, Field, Cigales, Malphurs
et al., 1996b) and depressed mothers (Field et al., 2007; Pe-
laez-Nogueras, Field, Hossain, & Pickens, 1996a). In still an-
other still-face study, cortisol reactivity was higher in infants
during the still-face condition, and cortisol levels were lower
for infants in the still-face plus maternal touch condition
(Feldman et al., 2007). Vagal tone was also lower during the
still-face than the still-face plus maternal touch interaction.
Maternal touch was associated with higher infant vagal tone
and lower maternal and infant cortisol. Others have noted that
regulatory touching occurs naturally on the part of the mothers
when they are asked to remain still-faced (Jean & Stack, 2009).
In the Jean and Stack (2009) study, mothers used more nurtur-
ing touch when their infants were distressed during the still-
face period.
Interaction coaching techniques have been used to help im-
prove the interactions of high-risk dyads, for example, the in-
teractions of mothers and their preterm infants whose cues are
more difficult to read and the interactions of infants and their
depressed mothers who are less attentive to their infants’ sig-
nals. Examples of interaction coaching are asking the mothers
to imitate their infants’ behaviors and to be silent during gaze
aversion when the infant appears to be highly aroused, and to
simplify their behaviors by repetition (Field, 1983). These
techniques seem to sensitize the mothers to their infants’ gaze
and affect and thereby diminish the infants’ gaze aversion and
fussiness as well as facilitate their attentiveness and positive
affect such as smiling and laughing. In this way, the mother or
father and infant can become attuned to each other, and their
interactions become more harmonious. Effectively, in these
interventions the parent is being taught to provide optimal
stimulation and arousal modulation.
Future Directions
Relationships may not work because as in oscillators, indi-
viduals may not be on the same wavelength. This may relate to
their having different thresholds for stimulation as well as
arousal modulation. Chapple’s work exemplifies how some
individuals are more disturbed by being interrupted and being
“talked over” versus some who are more disturbed by the latent
responding of a confederate (Chapple, 1970). Other examples
are depressed mothers being unresponsive due to their high
thresholds to their infant’s stimulation and preterm infants be-
ing unresponsive to the mothers because of their high thresh-
olds for stimulation. Individual differences may exist in thresh-
olds of partners who break up as in one being too sensitive, i.e.
having a low threshold while the other may be too insensitive,
i.e. having a high threshold. More laboratory research is needed
on measuring the streams of behavior and physiological re-
sponding in natural interactions as opposed to the conflict-like
interactions studied by Gottman and his colleagues (Gottman et
al., 1992, 1998, 2002, 2003). And, laboratory interventions, e.g.
biofeedback-interactions as in observing one’s physiological
responses and bug-in-the-ear interaction feedback, might be
Copyright © 2012 SciRes.
informative as to how flexible and responsive disturbed rela-
tionships are to change. The stream of emotions from extremely
positive (highly energized, fast-paced talking with laughter) to
sober, reflective slow-paced talking, to highly charged angry
exchanges may need to be modulated by both partners simulta-
neously. And, the highly positive to highly negative interac-
tions may be less arousing/dysregulating in the presence of
physical contact, just as the mother holds the crying infant to
comfort and soothe. This behavior/physiology could be simul-
taneously measured to determine more precise ways in which
relationships might serve as regulators.
In summary, Hofer (1984, 1996) and Field (1985, 1994) ad-
vanced models on relationships as regulators, with Hofer sup-
porting his model by data on infant rats separated from their
mothers and Field describing a psychobiological attunement
between human infants and their mothers. Many studies on
relationships have focused on temporary separations and loss
associated with death and breakups, although both Hofer and
Field suggested that the real question is “what was there about
the relationship that was then missing after the loss?” Some
studies have addressed that question by looking at good vs. less
good relationships. Examples of these given in this review in-
clude relationships between non-depressed versus depressed
mothers and their infants, preschool and preadolescent friends
versus acquaintances, and happily versus less happily married
couples. Some behavioral and physiological data support
Hofer’s and Field’s “relationships as regulators” model, al-
though very little is known about the underlying mechanisms
for relationships as regulators. Further research is needed on the
potential mediators reviewed here, including mirror neurons,
affective priming, imitation and empathy as well as the epige-
netic programming that may contribute to relationships as re-
gulators across species and across development. Further, re-
search is needed on the development of the individual’s rhy-
thms and the attraction and adjustment to others’ rhythms as
regulators in relationships.
We would like to thank those who participated in our studies.
This research was supported by a merit award (MH46586) NIH
grants (AT00370 and HD056036) and Senior Research Scien-
tist Awards (MH00331 and AT001585) and a March of Dimes
Grant (12-FYO3-48) to Tiffany Field and funding from John-
son & Johnson Pediatric Institute to the Touch Research Insti-
Arbib, M. (2005). From monkey-like action recognition to human lan-
guage: An evolutionary framework for neurolinguistics. Behavioral
and Brain Sciences, 28, 105-124. doi:10.1017/S0140525X05000038
Aron, A., Fisher, H., Mashek, D. J., Strong, G., Li, H., & Brown, L. L.
(2005). Reward, motivation, and emotion systems associated with
early-stage intense romantic love. Journal of Neurophysiology, 94,
327-337. doi:10.1152/jn.00838.2004
Bagot, R. C., & Meaney, M. J. (2010). Epigenetics and the biological
basis of gene x environment interactions. Journal of American Aca-
demy of Child Adolescence Psychiatry, 49, 752-771.
Banse, R. (1999). Automatic Evaluation of self and significant others:
Affective priming in close relationships. Journal of Social and Per-
sonal Relationships , 16, 803-821. doi:10.1177/0265407599166007
Bauer, J. (2005). Warum ich fühle, was du fühlst. Intuitive Kommu-
nikation und das Geheimnis der Spiegelneurone. Hamburg: Hoff-
mann und Campe.
Black, P. H. (2002). Stress and the inflammatory response: A review of
neurogenic inflammation. Brain, Behavior and Immunity, 16, 622-
653. doi:10.1016/S0889-1591(02)00021-1
Bowlby, J. (1982). Attachment and loss: Vol. 1 attachment (2nd ed.).
New York: Basic Books.
Carrère, S., & Gottman, J. M. (1999). Predicting divorce among new-
lyweds from the first three minutes of a marital conflict discussion.
Family Process, 38, 293-301. doi:10.1111/j.1545-5300.1999.00293.x
Champagne, F. A., & Meaney, M. J. (2007). Transgenerational effects
of social environment on variations in maternal care and behavioral
response to novelty . Behavioral Neuroscience, 121, 1353-1363.
Chapple, E. D. (1970). Culture and biological man: Exploration in
behavioral anthropology. New York: Holt, Rinehart & Winston.
Chen, Z., Williams, K. D., Fitness, J., & Newton, N. C. (2008). When
hurt will not heal: Exploring the capacity to relive social and physical
pain. Psychological Science, 19, 789-795.
Diamond, L. M., Hicks, A. M., & Otter-Henderson, K. (2008). Every
time you go away: Changes in affect, behavior, and physiology asso-
ciated with travel-related separations from romantic partners. Journal
of Personality and Social Ps y c h o l o g y , 95, 385-403.
Dettmer, A. M., Novak, M. A., Suomi, S. J., & Meyer, J. S. (2011).
Physiological and behavioral adaption to relocation stress in differ-
entially reared rhesus monkeys: Hair cortisol as a biomarker for
anxiety-related responses. Psychoneuroendocrinology, Epub ahead
of print.
Driver, J. L., & Gottman, J. M. (2004). Daily marital interactions and
positive affect during marital conflict among newlywed couples.
Family Process, 43, 301-314. doi:10.1111/j.1545-5300.2004.00024.x
Eisenberger, N. I., Lieberman, M. D., & Williams, K. D. (2003). Does
rejection hurt? An fMRI study of social exclusion. Science, 302,
290-292. doi:10.1126/science.1089134
Feldman, R., & Eidelman, A. I. (2007). Maternal postpartum behavior
and the emergence of infant-mother and infant-father synchrony in
preterm and full-term infants: The role of neonatal vagal tone. De-
velopmental Psychobiology, 49, 290-302.
Feldman, R., Singer, M., & Zagoory, O. (2010). Touch attenuates in-
fants’ physiological reactivity to stress. Developmental Science, 13,
271-278. doi:10.1111/j.1467-7687.2009.00890.x
Feldstein, S., & Field, T. (2002). Vocal behavior in the dyadic interac-
tions of preadolescent and early adolescent friends and acquaintances.
Adolescence, 37, 495-513.
Ferrari, P. F., Pau kne r, A., Ionica, C., & Suomi, S. J. (2009). Reciproca l
face-to-face communication between rhesus macque mothers and
their newborn infants. Current Biology, 19, 1768-177 2.
Ferrari, P. F., Paukner, A., Ruggiero, A., Darcey, L., Unbehagen, S., &
Suomi, S. J. (2009). Interindividual differences in neonatal imitation
and the development of action chains in rhesus macques. Child De-
velopment, 80, 1057-1068. doi:10.1111/j.1467-8624.2009.01316.x
Ferrari, P. F., Visalberghi, E., Paukner, A., Fogassi, L., Ruggiero, A., &
Suomi, S. J. (2006). Neonatal imitation in rhesus macaques. PLoS
Biology, 4, e302. doi:10.1371/journal.pbio.0040302
Field, T. (1983). Early interactions and interaction coaching of high-
risk infants and parents. In M. Perlmutter (Ed.), Minnesota sympo-
sium on child psychology. Hillsdale, NJ: Lawrence Erlbaum Associ-
Field, T. (1985). Attachment as psychobiological attunement: Being on
the same wavelength. In M. Reite, & T. Field (Eds.), Psychobiology
of attachment and separation . New York: Academic Press.
Field, T. (1991). Young children’s adaptations to repeated separations
Copyright © 2012 SciRes. 477
from their mothers. Child Development, 62, 539- 547.
Field, T. (1994). The effects of mother’s physical and emotional un-
availability on emotion regulation. Monographs of the Society for
Research in Child Development, 59, 208-227.
Field, T. (2007). The Amazing infant. London: Blackwell.
Field, T. (2009). Heartbreak. New York: Xlibris.
Field, T. (2010a). Postpartum depression effects on early interactions,
parenting and safety practices: A review. Infant Behavior and De-
velopment, 33, 1-6. doi:10.1016/j.infbeh.2009.10.005
Field, T. (2010b). Touch for socioemotional and physical well-being: A
review. Developmental Review, 30, 367-383.
Field, T., Diego, M., & Hernandez-Reif, M. (2010). Prenatal depression
effects and interventions: A review. Infant Behavior and Develop-
ment, 33, 409-418.
Field, T., Diego, M., Pelaez, M., Deeds, O., & Delgado, J. (2009).
Breakup distress in university students. Adolescence, 44, 705-727.
Field, T., Diego, M., Pelaez, M., Deeds, O., & Delgado, J. (2010).
Breakup distress and the loss of intimacy in university students.
Psychology, 1, 173-177. doi:10.4236/psych.2010.13023
Field, T., Diego, M., Pelaez, M., Deeds, O., & Delgado, J. (2010a).
Intrusive thoughts: A primary variable in breakup distress. College
Student Journal, in press.
Field, T., Diego, M., Pelaez, M., Deeds, O., & Delgado, J. (2010b).
Negative emotions and behaviors are markers for breakup distress.
College Student Journal, in press.
Field, T., Greenwald, P., Morrow, C., Foster, T., Guthertz, M. et al.
(1992). Behavior state matching during interactions of preadolescent
friends versus acquaintances. Developmental Psychology, 28, 242-
250. doi:10.1037/0012-1649.28.2.242
Field, T., Healy, B., Goldstein, S., & Guthertz, M. (1990). Behavior
state matching and synchrony in mother-infant interactions of non-
depressed versus depressed dyads. Developmental Psychology, 26,
7-14. doi:10.1037/0012-1649.26.1.7
Field, T., Healy, B., & LeBlanc, W. (1989). Sharing and synchrony of
behavior states and heart rate in nondepressed versus depressed
mother-infant interactions. Infant Behavior and Development, 12,
357-376. doi:10.1016/0163-6383(89)90044-1
Field, T., Hernandez-Reif, M., Diego, M., Feijo, L., Vera, Y. et al.
(2007). Still-face and separation effects on depressed mother-infant
interactions. Infant Mental Health Journal, 28, 314-323.
Field, T., & Reite, M. (1984). Children’s responses to separation from
mother during the birth of another child. Child Development, 55,
1308-1316. doi:10.2307/1130000
Field, T., Schanberg, S. M., Scafidi, F., Bauer, C. R., Vega-Lahr, N. et
al. (1986). Tactile/kinesthetic stimulation effects on preterm neonates.
Pediatrics, 77, 654- 658.
Field, T., Vega-Lahr, N., & Jagadish, S. (1984). Separation stress of
nursery school infants and toddlers graduating to new classes. Infant
Behavior and Development, 7, 527-530.
Field, T., Woodson, R., Greenberg, R., & Cohen, D. (1982). Discrimi-
nation and imitation of facial expressions by neonates. Science, 218,
179-181. doi:10.1126/science.7123230
Geoffroy, M. C., Cote, S. M., Parent, S., & Seguin, J. R., (2006). Day-
care attendance, stress, and mental health. Canadian Journal of Psy-
chiatry, 51, 607-615.
Goldstein, S., Field, T., & Healy, B. (1989). Concordance of play be-
havior and physiology in preschool friends. Journal of Applied De-
velopmental Psychology, 10 , 337-351.
Gottman, J. M., Coan, J., Carrère, S., & Swanson, C. (1998). Predicting
marital happiness and stability from newlywed interactions. Journal
of Marriage and the Family, 60, 5-22. doi:10.2307/353438
Gottman, J. M., & Levenson, R. W. (1992). Marital processes predic-
tive of later dissolution: Behavior, physiology, and health. Journal of
Personality and Social P s y chology, 63, 221-233.
Gottman, J. M., & Levenson, R. W. (2002). A two-factor model for
predicting when a couple will divorce: Exploratory analyses using
14-year longitudinal data. Family Process, 41, 83-96.
Gottman, J. M., Levenson, R. W., Swanson, C., Swanson, K., Tyson, R.,
& Yoshimoto, D. (2003). Observing gay, lesbian and heterosexual
couples’ relationships: mathematical mod el in g o f co nf li ct in te raction.
Journal of Homosexu ality, 45, 65-91.
Gump, B. B., Polk, D. E., Kamarck, T. W., & Shiffman, S. M. (2001).
Partner interactions are associated with reduced blood pressure in the
nat u ral envi ronment: A mbulatory mo nitoring eviden ce fro m a health y,
multiethnic adult sample. Psychosomatic M e dicine, 63, 423-433.
Heimann, M., Laberg, K. E., & Nordoen, B. (2006). Imitative interac-
tion increases social interest and elicited imitation in non-verbal
children with autism. Infant and Child Dev e lopment, 15, 297-309.
Heron, W. (1961). Cognitive and physiological effects of perceptual
isolation. In P. Solomon (Ed.), Sensory deprivation. Cambridge,
Massachusetts: Harvard University Press.
Hofer, M. (1984). Relationships as regulators: A psychobiologic per-
spective on bereavement. Psychosomatic Medicine , 46, 183-197.
Hofer, M. (1996). On the nature and consequences of early loss. Psy-
chosomatic Medicine, 58, 570-581.
Holt-Lunstad, J., Uchino, B. N., Smith, T. W., Olson-Cerny, C., &
Nealey-Moore, J. B. (2003). Social relationships and ambulatory
blood pressure: Structural and qualitative predictors of cardiovascu-
lar function during everyday social interactions. Health Psychology,
22, 388-397. doi:10.1037/0278-6133.22.4.388
Jacobson, N. S., & Gottman, J. M. (1999). When men batter women.
New York: Simon & Schuster.
James, W. (1950). The principles of psychology (Vol. 1). New York:
Jean, A. D., & Stack, D. M. (2009). Functions of maternal touch and
infant’s affect during face-to-face interactions: New directions for
the still-face. Infant Behavior & Development, 32, 123-128.
Klein, K. E., & Wegmann, H. M. (1974). The resynchronization of
human circadian rhythms after transmediterranean flights as a result
of flight direction and mode of activity. In L. E. Scheving, F. H albe rg,
& J. F. Pauly (Eds.), Chronobiology (pp. 564-570). Tokyo: Igaku
Lester, B. M., Tronick, E., Nestler, E., Abel, T., Kosofsky, B. et al.
(2011). Behavioral epigenetics. Annals of the New York Academy of
Sciences, 1226, 14-33. doi:10.1111/j.1749-6632.2011.06037.x
Levenson, R. W., Carstensen, L. L., & Gottman, J. M. (1994). The
influence of age and gender on affect, physiology, and their interrela-
tions: A study of long-term marriages. Journal of Personality and
Social Psychology, 67, 56-68. doi:10.1037/0022-3514.67.1.56
Levenson, R. W., & Gottman, J. M. (1983). Marital interaction: Physio-
logical linkage and affective exchange. Journal of Personality and
Social Psychology, 45, 587-597. doi:10.1037/0022-3514.45.3.587
Levenson, R. W., & Gottman, J. M. (1985). Physiological and affective
predictors of change in relationship satisfaction. Journal of Person-
ality and Social Psychology, 49, 85-94.
Loving, T. J., Crockett, E. E., & Paxson, A. A. (2009). Passionate love
and relationship thinkers: Experimental evidence for acute cortisol
elevations in women. Psychoneuroendocrinology, 34, 939-946.
Mason, W. A., & Berkson, G. (1975) Effects of maternal mobility on
the development of rocking and other behaviors in rhesus monkeys:
A study with artificial mothers. Developmental Psychobiology, 8,
197-221. doi:10.1002/dev.420080305
McClintock, M. K. (1983) Pheromonal regulation of the ovarian cycle:
Enh ancement, suppression, and synchrony. In J. G. Vandenberg (Ed.),
Pheromones and reproduction in mammals (pp. 113-149). New York:
Academic Press.
McGowan, P. O., Suderman, M., Sasaki, A., Huang, T. C., Hallett, M.
Copyright © 2012 SciRes.
Copyright © 2012 SciRes. 479
et al. (2011). Broad epigenetic signature of maternal care in the brain
of adult rats. PLoS On e, 6, e14739.
Meltzoff, A. N., & Moore, M. K. (1977). Imitation of facial and manual
gestures by human neonates. Science, 198, 75-78.
Monk, T. H., Burk, L. R., Klien, M. H., Kupfer, D. J., Soehner, A. M.,
& Essex, M. J. (2010). Behavioral circadian regularity at age 1
month predicts anxiety levels during school-age years. Psychiatry
Research, 178, 370-373. doi:10.1016/j.psychres.2009.09.020
Monk, T. H., Houck, P. R., & Shear, M. K. (2005). The daily life of
complicated grief patients—What gets missed, what gets added?
Death Studies, 30, 77-85. doi:10.1080/07481180500348860
Montagner, H., Restoin, A., & Henry, J. C. (1982). Biological defense
rhythms, stress and communications in children. In W. W. Hartup
(Ed.), Review of child development research. Chicago: University of
Chicago Press.
Papousek, M. (2007). Communication in early infancy: An arena of
intersubjective learning. Infant Behavior & Development, 30, 258-
266. doi:10.1016/j.infbeh.2007.02.003
Paukner, A., Suomi, S. J., Visalberghi, E., & Ferrari, P. F., (2009).
Capuchin monkeys display affiliation toward humans who imitate
them. Science, 325, 880-883. doi:10.1126/science.1176269
Pelaez, M., Field, T., Diego. M., Deeds, O., & Delgado, J. (2011).
Insecurity, controlling, and loss of interest behaviors relate to
breakup distress in universit y students. College Student Journ al, 452.
Pelaez-Nogueras, M., Field, T., Hossain, Z., & Pickens, J. (1996a).
Depressed mothers’ touching increases infants’ positive affect and
attention in still-face interactions. Child Development, 67, 1780-
1792. doi:10.2307/1131731
Pelaez-Nogueras, M., Gewirtz, J. L., Field, T., Cigales, M., Malphurs,
J., Clasky, S., & Sanchez, A. (1996b). Infant preference for touch sti-
mulation in face-to-face interactions. Journal of Applied Develop-
mental Psychology, 17, 199-213.
Powell, L. H., Lovallo, W. R., Matth ews, K. A., Meyer , P., Midg ley, A.
R., Baum, A. et al. (2002). Physiologic markers of chronic stress in
premenopausal, middle-aged women. Psychosomatic Medicine, 64,
Riz zol atti, G., Fadiga, L., Fogassi, L., & Gallese, V. (2002). From mirror
neurons to imitation: Facts and speculations. In A. N. Meltzoff, & W.
Prinz (Eds.), The imitative mind. Cambridge: Cambridge University
Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L. (1996). Premotor
cortex and the recognition of motor actions. Cognitive Brain Re-
search, 3, 131-141.
Robles, T. F., & Kiecolt-Glaser, J. K. (2003). The physiology of mar-
riage: Pathways to health. Physiology and Behavior, 79 , 409-416.
Roopnarine, J. L., & Field, T. M. (1984). Play behaviors of friends and
acquaintances in nursery school. In T. Field, J. Roopnarine, & M.
Segal (Eds.), Friendships in normal and handicapped children. Nor-
wood, NJ: Ablex.
Rusbult, C. E., Kumashiro, M., Kubacka, K. E., & Finkel, E. J. (2009).
“The part of me that you bring out”: Ideal similarity and the Michel-
angelo phenomenon. Journal of Personality and Social Psychology,
96, 61-82. doi:10.1037/a0014016
Sbarra, D. A., & Hazan, C. (2008). Coregulation, dysregulation, self-
regulation: An integrative analysis and empirical agenda for under-
standing adult attachment, separation, loss, and recovery. Personality
and Social Psychology Review, 12, 141-167.
Schanberg, S., & Field, T. (1987). Sensory deprivation stress and sup-
plemental stimulation in the rat pup and preterm human neonate,
Child Development, 58 , 1431-1447. doi:10.2307/1130683
Schwerdtfeger, A. & Friedrich-Mai, P. (2009). Social interaction mod-
erates the relationship between depressive mood and heart rate vari-
ability: Evidence from an ambulatory monitoring study. Health Psy-
chology, 28, 501-509. doi:10.1037/a0014664
Shahrokh, D. K., Zhang, T. Y., Diorio, J., Gratton, A., & Meaney, M. J.
(2010). Oxytocin-dopamine interactions mediate variations in ma-
ternal behavior in the r at. Endocrinology, 151, 2276-2286.
Shear, K., & Shair, H. (2005). Attachment, loss, and complicated grief.
Developmental Psychobiology, 47, 253-267. doi:10.1002/dev.20091
Singer, T., Seymour, B., O’Doherty, J., Kaube, H., Dolan, R. J. , & Frith,
C. D. (2004). Empathy for pain involves the affective but not sensory
components of pain. Science, 303, 1157-1162.
Soto, J. A., & Levenson, R. W. (2009). Emotion recognition across
cultures: The influence of ethnicity on empathic accuracy and phy-
siological linkage. Emotion, 9, 874-884. doi:10.1037/a0017399
Stern, D. N. (2004). The present moment in psychotherapy and every-
day life. New York: Norton.
Suomi, S. J., (2006). Risk, resilience, and gene x environment interac-
tions in rhesus monkeys. Annals of the New York Academy of Sci-
ences, 1094, 52-62. doi:10.1196/annals.1376.006
Szyf, M., & Meaney, M. J. (2008). Epigenetics, behavior, and health.
Journal of Allergy and Clinical Im mu n ol og y , 4, 37-49.
Trevarthen, C. (1979). Communication and cooperation in early infancy:
A description of primary intersubjectivity. In M. Bullowa (Ed.), Be-
fore speech: The beginning of human communication (pp. 321-347).
Cambridge: Cambridge University Press.
Tronick, E. Z. (2003). Things still to be done on the still-face effect.
Infancy, 4, 475-482. doi:10.1207/S15327078IN0404_02
Van Hasselt, F. N., Corneliesse, S., Yuang Zhang, T., Meaney, M. J.,
Velzing, E. H. et al. (2011). Adult hippocampal glucocorticoid re-
ceptor expression and dentate synaptic plasticity correlate with ma-
ternal care received by individuals early in life. Hippocampus, Epub
ahead of print.
Vermeer, H. J., & Van Ijzendoorn, M. H. (2006). Children’s elevated
cortisol levels at daycare: A review and meta-analysis. Early Child
Research Quarterly, 21 , 390-401. doi:10.1016/j.ecresq.2006.07.004
Wade, M. G., Ellis, M. J., & Bohrer, R. E. (1973). Biorhythms in the
activity of children during free play time. Journal of the Experimen-
tal Analysis of Behavior, 20, 155-162. doi:10.1901/jeab.1973.20-155
Warner, R. M. (1979). Periodic rhythms in conversational speech.
Language and Speech, 22, 381-396.
Weaver, I. C. G., Cervoni, N., Champagne, F. A., Alessio, A. C. D.,
Sharma, S. et al. (2004). Epigenetic programming by maternal be-
havior. Nature Neuroscience, 7, 847-854.
Weaver, I. C., Meaney, M. J., & Szyf, M. (2006). Maternal care effects
on the hippocampal transcriptome and anxiety-mediated behaviors in
the offspring that are reversible in adulthood. Proceedings of the Na-
tional Academy of Science of United States of America, 103, 3480-
3485. doi:10.1073/pnas.0507526103
Weller, L., & Weller, A. (1993). Human menstrual synchrony: A criti-
cal assessment. Neuroscience and Biobehavioral Reviews, 17, 427-
439. doi:10.1016/S0149-7634(05)80118-6
Wittstein, I. S. Thiemann, D. R., Lima, J. A. C., Baughman, Kt.,
Schulman, S. P., Gerstenblith, G. et al. (2005). Neurohumoral fea-
tures of myocardial stunning due to sudden emotional stress. The
New England Journal of Medicine, 352, 539-548.
Young, L. J., & Wang, Z. (2004). The neurobiology of pair bonding.
Nature Neuroscience, 7, 1048-1054. doi:10.1038/nn1327
Zhang, T. Y., & Meaney, M. J. (2010). Epigenetics and the environ-
mental regulation of the genome and its function. Annual Review of
Psychology, 61, 439-466.