C HA P TE R

5 Affiliation and Stress

Shelley E. Taylor

Abstract
Affiliation with others is a basic human coping response for managing a broad array of stressful
circumstances. Affiliating with others is both psychologically and biologically comforting, and biologically
may depend upon oxytocin and brain opioid pathways. The origins of affiliative responses to stress
include early life experiences, genetic factors, and epigenetic processes that interact with the availability
of supportive others during times of stress. The beneficial consequences of affiliation for mental and
physical health are strong and robust. Future research will continue to clarify the underlying
biopsychosocial pathways that explicate why this is the case.
Keywords: affiliation, coping, fight-or-flight, social support, stress, tend-and-befriend

Affiliation with others is one of human beings’ most threatening times. In recent decades, convincing
basic coping responses to threat. Whereas other ani- evidence that affiliation and its consequences also
mals have weapons, such as sharp teeth or claws, and affect biological responses to stress and ultimately
defensive resources, such as speed or thick skin, pri- physical health has emerged. Thus, social relation-
mates, including human beings, depend critically on ships, especially in times of stress, have benefits at
one another for survival. Correspondingly, social isola- both the psychological and biological levels across
tion and rejection from a social group are among the the lifespan (Taylor, 2009).
most distressing experiences people report (Eisenberger,
Lieberman, & Williams, 2003), and social isolation is Fight or flight/tend and befriend
associated not only with risks to safety, but with long- In the past, when scientists have characterized stress
term mental and physical health risks as well (Cacioppo responses, they usually have done so in terms of
& Hawkley, 2003). This chapter explores the con- fight or flight, a response pattern first characterized
ceptual basis for understanding the relation of affilia- by Walter Cannon (1932). Fight or flight refers to
tion to stress, the origins of affiliative responses to the fact that in response to threat, an animal or
stress, psychological and biological mechanisms person can become aggressive and mount an antag-
underlying these responses, and consequences of these onistic response to the threatening circumstances,
responses for physical and mental health. or it can flee, either literally or metaphorically,
from the stressor. Among the responses that stress
Affiliative Responses to Threat researchers interpret as flight behavior are social
Social relationships have long been known to sus- withdrawal and substance use, especially drug and
tain human beings in non-threatening as well as alcohol abuse. Fight and flight represent valuable

86
individual responses for coping with stress, in that Functions of affiliation
either fighting or fleeing has the potential to pro- Affiliation serves several vital functions with respect to
tect oneself from threats. However, humans are stress or threat. First, affiliating with others serves to
profoundly social and never more so than when calibrate or shape the biological stress systems that
the environment is threatening. Accordingly, it is regulate responses to stress across the lifespan. As will
important to characterize these affiliative responses be addressed, caregiving relationships, especially those
to stress as well. To address the human tendency early in life, help to serve this function. Beginning in
to affiliate under stress, we developed the term the early environment, the quality of caregiving an
“tend and befriend” (Taylor, 2002; Taylor, Klein, infant receives can permanently affect that infant’s
Lewis, Gruenewald, Gurung, & Updegraff, 2000). biological, emotional, and social responses to stress-
In contrast to fight or flight, tending to offspring ful conditions. These effects can occur in the form
and affiliating with others represent social responses of how genes are manifested in phenotypes and can
to stress. exert permanent organizational effects on the regula-
The theory, tend and befriend, maintains that tory systems that shape responses to stress, an issue
there is a biological signaling system that comes addressed in more detail later in this chapter. Ultimately,
into play if one’s affiliations fall below an adequate these responses to stress also predict a broad array of
level, a condition that may occur in response to chronic health disorders as well as longevity.
stress. The affiliative neurocircuitry then prompts Social affiliation also affects the regulation of stress
affiliation in many animal species and in humans. responses on an acute basis. During daily interac-
As such, this system regulates social approach behav- tions, as a person copes with more or less stressful
ior and does so in much the same way as occurs for circumstances, affiliation influences the magnitude of
other appetitive needs. Once signaled, this appeti- stress responses. Contacts with others can increase
tive need is met through purposeful social behav- tension and exaggerate responses to stress, but more
iors, such as affiliation and protecting offspring. commonly, affiliation buffers an individual against
As will be noted, oxytocin and endogenous opioid the deleterious biological effects of stress. These prox-
peptides appear to play a role in this system. As imal functions of affiliation in response to stress
we will note later, the biological impetus to affil- interact with the more distal calibration of stress sys-
iate under stress, coupled with the psychological tems just described, such that people’s responses to
need for contact with others under stress, may rep- stress depend both on the early development of
resent redundant biobehavioral protective mecha- their biological stress regulatory systems as shaped by
nisms that ensure affiliation and corresponding early relationships, and also on current circumstances
safety when the environment is threatening. that moderate these biological responses to stress.
Tend and befriend has its origins in evolutionary Affiliation serves practical functions with respect
theory, and as such tending and befriending may be to stress. For example, other people transmit impor-
somewhat more characteristic of women than men tant knowledge about the environment in which
as responses to stress (Taylor et al., 2000). During stress occurs. This informational function may be
the time that human stress responses evolved, men direct, as when one person warns another about an
and women faced somewhat different adaptive impending stressor, or it may be indirect, such that
challenges due to the division of labor they assumed. how others respond to a threat provides useful infor-
Whereas men were primarily responsible for hunt- mation for the self. Other people can provide tan-
ing and for group protection, women were typically gible aid and assistance that better enables the
responsible for childcare and foraging. Conse- recipient to cope with stressful events. For example,
quently, women’s responses to stress are likely to in harsh economic times, a loan of money from
have evolved so as to protect not only self but also relatives or the opportunity to share living spaces
offspring during times of stress. Consistent with this may provide badly needed resources. Thus, social
position, women are more likely than men to respond relationships can act as a barometer of how stressful
to stress by turning to others (Luckow, Reifman, an environment is and provide assistance for man-
McIntosh, 1998; Tamres, Janicki, & Helgeson, 2002). aging a stressful environment (Taylor & Gonzaga,
However, men, too, show social responses to stress, 2006). Finally, affiliation in response to stress can
and the gender difference in affiliation in response reduce psychological distress. Those with whom one
to stress, although robust, is relatively modest in mag- affiliates or from whom one seeks contact may be
nitude. Thus, affiliation in response to stress occurs emotionally supportive and exert calming, soothing
among both men and women. effects on the person seeking contact.

taylor 87
Origins of affiliative responses to stress the directionality of the effect. Of note, in humans,
Affiliation is vital to the survival of human beings. the evidence to date suggests that oxytocin levels
As such, there are likely to be biobehavioral mecha- rise primarily in women in response to social stress.
nisms that are sensitive to social threat or to loss of If oxytocin and endogenous opioid peptides are
social contact, resulting in social distress and efforts related to social distress, then as part of the affilia-
to remedy the situation. A large literature on separa- tive neurocircuitry, they may provide an impetus
tion distress attests to such processes in young ani- for social contact to ameliorate stress. Indeed,
mals and human infants. When the young are numerous studies attest to the fact that exogenously
separated from the mother, separation distress can administered oxytocin can act as an impetus to
result, especially during particular developmental affiliation. Experimental studies with several ani-
periods. The experience of separation leads to dis- mal species have found that the administration of
tress vocalizations (e.g., crying in human infants) or oxytocin causes an increase in social contact and
active searching for the caregiver that may prompt in grooming, among other pro-social activities
the caregiver’s return (Panksepp, 1998). (Argiolas & Gessa, 1991; Carter, De Vries, & Getz,
This system appears to depend in part on brain 1995; Witt, Winslow, & Insel, 1992). For example,
opioids. Evidence consistent with this pathway social contact is enhanced and aggression is dimin-
includes the fact that brain opioids reduce separa- ished following central administration of oxytocin
tion distress, and opioid-based drugs such as mor- in estrogen-treated prairie voles (Witt, Carter, &
phine reduce distress vocalizations in response to Walton, 1990). Although human evidence for this
separation (Panksepp, 1998). There also appear to point is more limited, Uvnäs-Moberg (1996) found
be genetic bases for these processes that likewise that women who were breastfeeding (and therefore
depend on opioid-based processes. For example, very high in plasma oxytocin concentration) rated
mice that lack the μ-opioid receptor gene emit few themselves as more sociable than age-matched
distress vocalizations when separated from their women not breastfeeding or pregnant.
mothers, suggesting that endogenous opioid bind-
ing is a significant basis of infant attachment behav- Biological Effects of Affiliation
ior (Moles, Kieffer, & D’Amato, 2004). Biological responses to stress: Overview
Oxytocin also appears to be implicated in infant Researchers have focused heavily on potential phys-
bonding, separation, and reunification (Panksepp, iological, neuroendocrine, and immunological
1998). For example, in an experimental study with pathways by which affiliation in response to stress
rats, Nelson and Panksepp (1996) found that attrac- may achieve beneficial effects on stress regulation.
tion to the mother was blocked in animals who had What are these pathways? During times of stress,
received an oxytocin antagonist, suggesting that the body releases the catecholamines epinephrine
oxytocin is implicated in the neurocircuitry that and norepinephrine with concomitant sympathetic
underlies separation and reunification. Oxytocin is nervous system arousal. Stress may also engage the
also implicated in social distress in adults. Just as HPA (hypothalamic-pituitary-adrenocortical) axis,
infants and young children experience gaps in their involving the release of corticosteroids, including
social relationships, so adults may experience an cortisol. These responses have short-term protective
analog of separation distress, which may implicate effects under stressful circumstances because they
the same biological systems as in the young. Both mobilize the body to meet the demands of pressing
animal (Grippo et al., 2007) and human studies situations.
support this conclusion. For example, a study from However, with chronic or recurrent activation,
our laboratory found that women who experienced they can be associated with deleterious long-term
reduced contact with their mothers, with their best implications for health (e.g., Seeman & McEwen,
friends, with a pet, and with their social groups had 1996; Uchino, Cacioppo, & Kiecolt-Glaser, 1996).
especially high levels of oxytocin. Oxytocin levels For example, excessive or repeated discharge of
were also elevated in response to the absence of epinephrine or norepinephrine can lead to the sup-
positive relationships with a partner. Similar results pression of cellular immune function, produce
have been found by Turner and colleagues (Turner, hemodynamic changes such as increases in blood
Altimus, Enos, Cooper, & McGuiness, 1999). pressure and heart rate, provoke abnormal heart
Grippo, Carter, and colleagues (Grippo et al., 2007) rhythms such as ventricular arrhythmias, and pro-
isolated female prairie voles and found that social iso- duce neurochemical imbalances that may relate to
lation led to increases in oxytocin, thus confirming psychiatric disorders (McEwen & Stellar, 1993).

88 affiliation and stress

Intense, rapid, and/or long-lasting sympathetic McEwen, 1996; Uchino, Cacioppo, & Kiecolt-
responses to repeated stress or challenge have been Glaser, 1996). In turn, these benefits may affect
implicated in the development of hypertension and health in a positive direction.
coronary artery disease.
Stress can also suppress immune functioning in The Early Social Environment
ways that leave a person vulnerable to opportunistic Substantial evidence from both animal and human
diseases and infections. Corticosteroids have immu- studies indicates that nurturant affiliative contacts
nosuppressive effects, and stress-related increases in early life help to determine the parameters of
in cortisol have been tied to decreased lympho- these stress systems, and consequently have benefi-
cyte responsivity to mitogenic stimulation and to cial effects not only on responses to stress but also
decreased lymphocyte cytotoxicity. Such immuno- on mental and physical health across the lifespan.
suppressive changes may be associated with increased
susceptibility to infectious disorders and to destruc- Biological consequences of affiliative
tion of neurons in the hippocampus as well (McEwen contact in early life: Animal studies
& Sapolsky, 1995). An early study by Harlow and Harlow (1962) found
An immunosuppression model does not explain that monkeys who were raised with an artificial ter-
how stress might influence diseases whose central rycloth mother and who were isolated from other
feature is excessive inflammation (Miller, Cohen, & monkeys during the first 6 months of life showed
Ritchey, 2002); such diseases include allergic, auto- disruptions in their adult social contacts. They were
immune, rheumatologic, and cardiovascular disor- less likely to engage in normal social behavior, such
ders, among other disorders that are known to be as grooming, their sexual responses were inappro-
exacerbated by stress. Miller and colleagues (2002) priate, mothering among the females was deficient,
hypothesized that chronic stress may diminish the and they often showed either highly fearful or
immune system’s sensitivity to glucocorticoid hor- abnormally aggressive behavior toward their peers,
mones that normally terminate the inflammatory which, not surprisingly, led to social rejection. These
cascade that occurs during stress. They found a buff- findings suggest that social and emotional regula-
ering effect of social support on this process, such tion skills may be critically engendered by nurturant
that among healthy individuals, glucocorticoid contact in early life. Of interest, social deficiencies
sensitivity bore no relation to social support; how- that result from deficient mothering appear to
ever, among parents of children with cancer (a pop- involve precisely the skills that would interfere with
ulation under extreme stress), those who reported an adult offspring’s ability to enlist social contact in
receiving a high level of support from others had adulthood.
higher glucocorticoid sensitivity. Building on this work, Meaney and colleagues
Extensive evidence suggests that these (Francis, Diorio, Liu, & Meaney, 1999; Liu et al.,
systems—the HPA axis, the immune system, and 1997) linked nurturant maternal contact to the
the sympathetic nervous system (SNS)—influence development of stress responses in offspring and
each other and thereby affect each other’s function- showed that these contacts affect emotional and
ing. For example, links between HPA axis activity neuroendocrine responses to stress throughout the
and sympathetic nervous system activity suggest animals’ lives. In their paradigm, infant rats are
that chronic activation of the HPA axis could poten- removed from the nest, stroked, and then returned
tiate overactivation of sympathetic functioning to the nest. The response of the mother to this sepa-
(Chrousos & Gold, 1992). Proinflammatory cytok- ration and reunification is licking, grooming, and
ines, which are involved in the inflammatory pro- arched-back nursing, especially in species with a
cesses just noted, can activate the HPA axis and may genetic predisposition to these behaviors. These
contribute not only to the deleterious effects that contacts provide the pup with nurturant, soothing,
chronic activation of this system may cause, but also immediate stimulation, and in the short term reduce
potentially to depressive symptoms, which have SNS and HPA axis responses to stress in the pup
previously been tied to HPA axis activation (and in the mother as well).
(Capuron, Ravaud, & Dantzer, 2000; Maier & Over the long term, this maternal behavior
Watkins, 1998). To the extent, then, that social con- results in a better-regulated HPA axis response to
tact can help keep sympathetic nervous system or stress and better regulation of somatic growth and
HPA axis responses to stress low, it may have a ben- neural development, especially hippocampal syn-
eficial impact on other systems as well (Seeman & aptic development. Rat pups exposed to highly

taylor 89
nurturant mothering show less emotionality to levels of emotional disturbance, especially depres-
novel circumstances and more normative social sion, in infants who failed to receive nurturant,
behavior, including mothering in adulthood, com- stimulating contact from a caregiver (Spitz & Wolff,
pared to recipients of normal mothering. These 1946). More recent findings from Eastern European
pups show more open field exploration, suggesting abandoned infants confirm that without the affec-
lower levels of fear as well (Francis, Diorio, Liu, & tionate attention of caregivers, infants may fail to
Meaney, 1999; Weaver et al., 2004). thrive and many die (Carlson & Earls, 1997).
This compelling animal model indicates that Similarly, families characterized by unsupportive
nurturant stimulation by the mother early in life relationships have damaging outcomes for the
modulates the physiological, neuroendocrine, and mental, physical, and social health of their offspring,
behavioral responses of offspring to stress in ways not only in the short term but across the lifespan.
that have permanent effects on behavior and on Overt family conflict, manifested in recurrent epi-
the offspring’s developing HPA axis. Studies with sodes of anger and aggression, cold non-nurturant
monkeys have shown similar effects. For example, behavior, or neglect have been associated with a
Suomi (1987) reported that highly reactive mon- broad array of adverse mental and physical health
keys cross-fostered to nurturant mothers develop outcomes long into adulthood (Repetti, Taylor, &
good socioemotional skills and achieve high status Seeman, 2002; Repetti, Taylor, & Saxbe, 2007).
in the dominance hierarchy, whereas monkeys with The chronic stress of unsupportive families and/or
reactive temperaments who are peer-raised develop chronic stress unabated by supportive family con-
poor socioemotional skills and end up at the bottom tacts may produce repeated or chronic SNS activa-
of the dominance hierarchy. tion in children, which in turn may lead to wear and
An early nurturant environment can also induce tear on the cardiovascular system. Over time, such
lasting changes in the function of genes, which is alterations may lead to pathogenic changes in sym-
an additional mechanism by which early affilia- pathetic or parasympathetic functioning or both.
tive experience can induce long-term alterations These changes may contribute to adult chronic
in behavior. Specifically, the long-term behavioral health disorders such as hypertension and coronary
effects of early-life maternal care appear to result at heart disease.
least in part from epigenetic structural alterations Recurrent or chronic engagement of the HPA
(methylation) to the glucocorticoid receptor gene axis in response to stress can compromise the effi-
that occur in the first week after birth and affect cient functioning of this biological stress regulatory
its expression throughout the lifespan (Meaney & system as well. Specifically, in response to the stress
Szyf, 2005). Mothers expressing high levels of nur- of a harsh early childhood environment, function-
turant behavior exhibited greater increases in oxyto- ing of the HPA axis may be compromised in any of
cin receptors during pregnancy, which is thought several ways. Daily cortisol patterns may be altered.
to trigger maternal responsivity (Meaney, 2001), Normally, cortisol levels are high upon waking in
and have higher levels of dopamine release when the morning but decrease across the day (although
caring for their pups (Champagne, Chretien, peaking following lunch) until they flatten out at
Stevenson, Zhang, Gratton, & Meaney, 2004). The low levels in the afternoon. People under chronic
nurturant mothering that results triggers greater stress, however, can show elevated cortisol levels
increases in serotonin turnover in the pup, which long into the afternoon or evening (Powell et al.,
initiates a cascade leading to altered glucocorticoid 2002) or a general flattening of the diurnal rhythm.
receptor expression that beneficially affects adult In response to acute stress, an elevated flat response
reactivity to stress (Meaney & Szyf, 2005). to stress (Taylor, Lerner, Sage, Lehman, & Seeman,
2004), an exaggerated cortisol response, a protracted
Biological consequences of affiliative cortisol response, or poor recovery may be seen
contact in early life: Human studies (McEwen, 1998). Any of these patterns is suggestive
Similar processes and mechanisms have been identi- of compromises in the ability of the HPA axis to
fied in humans. Warm, nurturant, supportive con- respond to and recover from stress (McEwen, 1998;
tact with a caregiver early in life affects physiological Pruessner, Hellhammer, Pruessner, & Lupien, 2003).
and neuroendocrine stress responses in human Attachment is implicated in these processes. Specif-
infants and children (see Repetti, Taylor, & Seeman, ically, securely attached infants are less likely to show
2002, for a review). Early research on orphans, anal- elevated cortisol responses to normal stress than
ogous to the Harlow monkey studies, found high insecurely attached offspring (Gunnar, Brodersen,

90 affiliation and stress

Krueger, & Rigatuso, 1996; see also Nachmias, Overall, however, negative emotional states may be
Gunnar, Mangelsdorf, Parritz, & Buss, 1996). The more “contagious” than positive ones, suggesting
protective effects of secure attachment are espe- the possibility of the exacerbation of stress within
cially significant for socially fearful or inhibited close relationships rather than its amelioration.
children, temperamental characteristics that have a Such effects may depend on whether both members
genetic basis. of a couple are facing a particular stressor or whether
Early nurturant and supportive contacts are also only one person is.
important for the development of social and emo- Whether adults can influence each other’s biol-
tional regulation skills, especially those involving ogy on a chronic basis in the same ways as occur
responses to stress or threat. A broad array of evi- in the mother–infant relationship is unknown, but
dence supports the point that children from harsh the answer may be not to the same degree. Maternal
families are less likely than those from nurturant influences occur at the time that biological stress
families to develop effective emotion regulation skills regulatory systems are just developing, and so their
and social competencies (Repetti et al., 2002). effects may be more profound and long-lasting than
Is the calibration and regulation of stress is true in adult biological co-regulation. Nonetheless,
responses confined to early environment? Just as the idea that chronic cohabitation exerts ongoing
evidence increasingly points to the important role effects on the biological functioning of both parties,
that maternal nurturance plays in the biological resulting, in some cases, in biological synchrony,
stress responses of offspring, some research is begin- merits additional attention.
ning to uncover the ways in which adults’ affiliative
contacts may influence each other’s biology as well. Affiliation and genetic pathways
An early study (McClintock, 1971) found that Socioemotional skills that underpin affiliation may
roommates’ menstrual cycles become synchronized have an epigenetic basis in humans as well. This
over time, probably because of olfactory cues research is in its infancy, and so there is much still to
(McClintock, 2002). Research examining physio- be discovered, but to date, genes involved in the
logical concordance between clients and clinical regulation of monoamine oxidase-A (MAOA), sero-
psychologists suggests that such concordance is tonin, and dopamine appear to be implicated.
tied to ratings of therapist empathy (Marci, Ham, MAOA is an enzyme that breaks down neurochem-
Moran, & Orr, 2007). These processes may be icals such as serotonin and dopamine (Shih, Chen,
especially significant in close relationships, and, to a & Ridd, 1999). The MAOA gene that regulates the
degree, partners may co-regulate or synchronize their enzyme has been implicated in antisocial behavior
physiological and affective states (Diamond, 2001; (e.g., Eisenberger, Way, Taylor, Welch, & Lieberman,
Sbarra & Hazan, 2008; Pietromonaco, Barrett, & 2007). For example, in epidemiological studies,
Powers, 2006). Substantial evidence indicates men with the low expressing alleles of the MAOA-
reciprocity of negative affective processes and con- uVNTR are more likely to engage in aggressive and
comitant physiological arousal in marital couples antisocial activity than men with high expressing
(e.g., Gottman, Coan, Carrere, & Swanson, 1998; alleles; of interest, these effects appear to be espe-
Levenson & Gottman, 1983); that is, one partner’s cially likely when those with the genetic risk have
hostility is likely to arouse the other’s. In happier also been exposed to maltreatment in childhood
marriages, arousal in conflict situations is more (Caspi et al., 2002; Kim-Cohen et al., 2006).
often not in synchrony, possibly because one part- The harshness or nurturance of the early family
ner may be attempting to calm the more agitated environment also influences the expression of the
partner (Saxbe, 2009). Hofer (1984) suggested that serotonin transporter gene (5-HTTLPR). People
cohabiting partners influence each other’s regula- with two copies of the 5-HTTLPR short allele
tory symptoms and routine so much that some (short/short) who have experienced childhood mal-
of the consequences of bereavement, such as dis- treatment are more likely to be diagnosed with
turbed sleep, reduced appetite, and social with- major depressive disorder than individuals with one
drawal, might result from the loss of this biological or two copies of the long allele who have experi-
regulatory influence. Until recently, physiological enced similar environments (Caspi et al., 2003;
underpinnings of these processes had not been Kaufman et al., 2004), although these effects do not
addressed. There is now some evidence that couples’ always replicate (Risch et al., 2009). A study from
HPA axis activity may be coordinated (Berg & our laboratory (Taylor, Way, Welch, Hilmert,
Wynne-Edwards, 2002; Schreiber et al., 2006). Lehman, & Eisenberger, 2006), which may help to

taylor 91
explain these inconsistencies, indicates that the psychological and biological effects of acute stress
short allele may not function as a risk allele for as well. For example, experimental studies demon-
depression in the face of an adverse environment, strate that the presence of a supportive person when
but as a general sensitivity allele, providing pro- one is going through a stressful task can reduce
tection from symptoms of depression when the cardiovascular and HPA axis responses to stress;
environment is nurturant. We found a significant these benefits can be experienced whether the sup-
gene-by-environment interaction, such that indi- portive person is a partner, a friend, or a stranger
viduals with two copies of the short allele had greater (e.g., Christenfeld et al., 1997; Gerin, Pieper, Levy,
depressive symptomatology if they had experi- & Pickering, 1992; Gerin, Milner, Chawla, &
enced early familial adversity compared to partici- Pickering, 1995; Kamark, Manuck, & Jennings,
pants with the short/long or long/long genotypes, 1990; Kors, Linden, & Gerin, 1997; Lepore, Allen,
but significantly less depressive symptomatology if & Evans, 1993; Sheffield & Carroll, 1994; see
they reported a supportive early environment. Lepore, 1998 for a review).
Notably, the adverse early family environments Oxytocin may play a role in these processes.
studied were fairly mild, consisting of some conflict, In response to stress, animals and humans experi-
moderate household chaos, and/or cold, unaffec- ence a cascade of hormonal responses that begins, at
tionate, and distant behaviors, rather than explicit least under some stressful conditions, with the rapid
maltreatment in the form of physical or sexual release of oxytocin. Consistent evidence suggests
abuse. Thus, nurturant, affiliative contacts in early that oxytocin is released in response to stress and
life can shape the expression of genes in ways that that oxytocin is associated with reduced SNS and
can have lifelong effects on social behavior (such as HPA axis responses to stress (see Taylor, Dickerson,
aggression) and on susceptibility to stress in the & Klein, 2002). For example, oxytocin is associ-
social environment. ated with parasympathetic (vagal) functioning that
Certain genes in the dopamine system may plays a counterregulatory role in fear responses to
show a similar pattern. Researchers have found that, stress (e.g., Dreifuss, Dubois-Dauphin, Widmer, &
when exposed to non-nurturant parenting, people Raggenbass, 1992; McCarthy, 1995; Sawchenko &
with the long allele of the polymorphism DRD4 Swanson, 1982; Swanson & Sawchenko, 1980).
are at higher risk for externalizing behaviors than In experimental studies, oxytocin enhances seda-
individuals with other alleles (e.g., Bakermans- tion and relaxation, reduces anxiety, and decreases
Kranenburg & van IJzendoorn, 2006). However, sympathetic activity (Altemus, Deuster, Galliven,
recent evidence indicates that the long allele may Carter, & Gold, 1995; Uvnäs-Moberg, 1997).
increase sensitivity to positive as well as negative Exogenous administration of oxytocin in rats results
parental influences. In one study, when the environ- in decreases in blood pressure, pain sensitivity, and
ment was nurturant, individuals with the long corticosteroid levels, among other findings indica-
DRD4 allele had low levels of externalizing behav- tive of a reduced stress response (Uvnäs-Moberg,
ior, but when the environment was harsh, individuals 1997). Oxytocin appears to inhibit the secretion of
with the same allele had high levels of externalizing adrenocorticotropin hormone (ACTH) and cortisol
behavior. The behavior of individuals with the other in humans as well (Chiodera & Legros, 1981;
alleles was less responsive to parenting quality Legros, Chiodera, & Demy-Ponsart, 1982).
(Bakermans-Kranenburg & van IJzendoorn, 2007). Oxytocin may be implicated in the clinical ben-
Bakermans-Kranenburg and colleagues (2008) also efits of affiliation as well. A study by Detillion and
found that toddlers with the long allele of DRD4 colleagues (Detillion, Craft, Glasper, Prendergast,
were more responsive to a parental educational pro- & DeVries, 2004) reported a role for oxytocin in
gram designed to reduce externalizing behavior wound healing. In this study, Siberian hamsters
through increasing the attentiveness of parenting received cutaneous wounds and were then exposed
than those with other alleles. Findings such as these to immobilization stress. The stressor increased cor-
offer significant evidence that the social environment tisol concentrations and impaired wound healing.
early in life can powerfully shape expression of genes However, these effects occurred only in socially iso-
related to social behavior across the lifespan. lated and not in socially housed animals. Thus,
social housing acted as a stress buffer. The studies
Affiliative responses to acute stress went further to tie down the mechanism underpin-
A variety of empirical studies have shown that ning this effect. The researchers found that elimi-
affiliative contact can be protective against the nating cortisol via adrenalectomy eliminated the

92 affiliation and stress

impact of the stressor on wound healing, thereby support showed reduced neurocognitive reactiv-
implicating the HPA axis in the wound healing pro- ity to social exclusion, which, in turn, was tied to
cess. Of particular relevance for the role of oxytocin reduced neuroendocrine stress responses to labora-
in the wound healing process, treating the isolated tory challenges. This study, then, helps to document
hamsters with oxytocin eliminated the stress-in- the neural mechanisms underpinning the relation-
duced increases in cortisol and facilitated wound ship between social support and health-relevant
healing; treating socially housed hamsters with an outcomes and suggests a mechanism by which social
oxytocin antagonist, however, delayed wound heal- support may benefit health, namely by diminishing
ing. This evidence strongly implies that affiliation neural and physiological reactivity to stress.
can be protective against adverse effects of stress
through a mechanism that implicates oxytocin- Physical and Mental Health Consequences
induced suppression of the HPA axis. Moreover, it of Affiliation Under Stress
confirms a role for oxytocin in a clinically signifi- In response to their affiliative efforts, people com-
cant health-related outcome (wound healing). monly experience social support. Social support is
The potential roles of oxytocin in the down- defined as the perception or experience that one is
regulation of SNS and HPA axis responses to stress, loved and cared for by others, esteemed and valued,
in the tendency to turn to others, and in health- and part of a social network of mutual assistance
related outcomes at present are hypotheses with and obligations (Wills, 1991). Social support may
animal evidence to support them, but less evidence come from a partner, relatives, friends, coworkers,
from human studies. Consequently, these issues social and community ties, strangers, and even a
currently represent a direction for research rather devoted pet.
than an established biological pathway by which Mapping onto the functions of affiliation more
social contact may exert protective effects on health. generally, taxonomies of social support typically
Moreover, there may be roles for other hormones classify it into several specific forms. Informational
both in promoting social support initially and in support occurs when one person helps another to
regulating its biological effects, which include vaso- understand a stressful event better by providing
pressin, norepinephrine, serotonin, and prolactin information about the event. Instrumental support
(Nelson & Panksepp, 1998; Taylor, Dickerson, & involves the provision of tangible assistance, such as
Klein, 2002). services, financial assistance, and other specific aid
Research has also focused on the neural mecha- or goods. Emotional support involves providing
nisms whereby social contact affects physiological warmth and assistance to another person and reas-
processes that, in turn, affect health outcomes. A suring that person that he or she is a valuable person
three-part investigation (Eisenberger, Taylor, Gable, for whom others care. Social support may involve
Hilmert, & Lieberman, 2007) (1) had participants the reality of using the social network for benefits
complete a daily diary that recorded the supportive- such as these, but it can also involve simply the
ness of social interactions, (2) used fMRI to scan perception that such resources are available should
reactions to a social exclusion manipulation, and they be needed. In other words, just knowing that
(3) recorded physiological and HPA axis reactivity one is cared for and that one could request support
to laboratory-induced social stressors. The results from others is often comforting in its own right.
indicated that people who interacted regularly with The beneficial effects of affiliation and social
supportive people on a day-to-day basis showed support on mental and physical health are well
diminished cortisol reactivity to a social stressor. established. Social support reduces psychological
Moreover, both greater social support and a dimin- distress such as depression or anxiety during times
ished cortisol response were associated with lower of stress (e.g., Fleming, Baum, Gisriel, & Gatchel,
reactivity during the social exclusion task in two 1982; Lin, Ye, & Ensel, 1999; Sarason, Sarason, &
brain regions that have been previously tied to dis- Gurung, 1997). It promotes psychological adjust-
tress induced by social separation, namely the dorsal ment to chronically stressful conditions, such as
anterior cingulate cortex (dACC) and Brodmann coronary artery disease (Holahan, Moos, Holahan,
area 8 (BA 8). Mediational analyses revealed that & Brennan, 1997), diabetes, HIV (Turner-Cobb
individual differences in dACC and BA 8 reactivity et al., 2002), cancer (Penninx, van Tilburg, Boeke,
mediated the relationship between high daily social Deeg, Kriegsman, & van Eijk, 1998; Stone,
support and low cortisol reactivity to social stress; Mezzacappa, Donatone, & Gonder, 1999), rheuma-
that is, those people experiencing greater social toid arthritis (Goodenow, Reisine, & Grady, 1990),

taylor 93
kidney disease (Dimond, 1979), childhood leuke- In prospective studies controlling for baseline health
mia (Magni, Silvestro, Tamiello, Zanesco, & Carl, status, people with a higher quantity and quality of
1988), and stroke (Robertson & Suinn, 1968), social relationships have consistently been shown to
among other disorders. be at lower risk of early death (Herbst-Damm &
Social support has been tied to a variety of Kulik, 2005; Seeman, 1996), and in studies of
specific health benefits among individuals sustain- both humans and animals, social isolation has
ing health risks. These include fewer complications been found to be a major risk factor for early mor-
during pregnancy and childbirth (Collins, Dunkel- tality (House, Landis, & Umberson, 1988).
Schetter, Lobel, & Scrimshaw, 1993), less suscepti-
bility to herpes attacks among infected individuals When affiliation is not experienced
(VanderPlate, Aral, & Magder, 1988), lower rates as supportive
of myocardial infarction among individuals with Not all research shows beneficial effects of affiliation
diagnosed disease, a reduced likelihood of mortality in challenging circumstances, however. Sometimes
from myocardial infarction (Kulik & Mahler, 1993; the presence of a friend or stranger actually increases
Wiklund, Oden, Sanne, Ulvenstam, Wilhemsson, sympathetic reactivity among those undergoing
& Wilhemsen, 1988), faster recovery from coronary stress (e.g., Allen, Blascovich, Tomaka, & Kelsey,
artery disease surgery (King, Reis, Porter, & Norsen, 1991; Mullen, Bryant, & Driskell, 1997). Whereas
1993; Kulik & Mahler, 1993), better diabetes the presence of a partner typically reduces stress-
control (Marteau, Bloch, & Baum, 1987), better related physiological and neuroendocrine reactivity
compliance and longer survival in patients with among men, the presence of a male partner often
end-stage renal disease (Cohen, Sharma, Acquaviva, enhances reactivity among women (Kiecolt-Glaser &
Peterson, Patel, & Kimmel, 2007), and less pain Newton, 2001). The presence of a friend or partner
among arthritis patients (Brown, Sheffield, Leary, & may increase evaluation apprehension over whether
Robinson, 2003). Social support protects against important others’ perceptions of the self may decline,
cognitive decline in older adults (Seeman, Lusignolo, and so this apprehension may eliminate any beneficial
Albert, & Berkman, 2001), heart disease among effect of support (Lepore, 1998).
the recently widowed (Sorkin, Rook, & Lu, 2002), Sometimes efforts to provide social support are
and psychological distress in response to traumatic experienced as intrusive, or would-be support pro-
events, such as 9/11 (Simeon, Greenberg, Nelson, viders may give poor advice or fail to provide the
Schmeider, & Hollander, 2005). right kind of social support, thereby reducing the
Social support contributes to longevity (e.g., effectiveness of the effort (Bolger, Foster, Vinokur,
Rutledge et al., 2004). In a classic study that docu- & Ng, 1996; Burg & Seeman, 1994; Dakof &
mented this point, epidemiologists Lisa Berkman Taylor, 1990). Social support efforts may also be
and Leonard Syme (1979) followed nearly seven perceived as controlling or directive by the recipi-
thousand California residents over a 9-year period ent. For example, chronically ill patients sometimes
to identify factors that contributed to their long- report that a spouse’s efforts to co-manage the disor-
evity or early death. They found that people who der can lead to conflict in the couple (e.g., Fisher,
lacked social and community ties were more likely La Greca, Greco, Arfken, & Schneiderman, 1997).
to die of all causes during the follow-up period than Social support may reinforce symptom experiences
those who cultivated or maintained their social rela- if it becomes contingent on a person’s expression
tionships. Having social contacts predicted an aver- of psychological or physical distress (Itkowitz,
age 2.8 years increased longevity among women and Kerns, & Otis, 2003).
2.3 years among men, and these differences per- When people are under threat, they are especially
sisted after controlling for socioeconomic status, vulnerable to perceived or actual threats to the self.
health status at the beginning of the study, and In other words, although people are often receptive
health habits (Berkman & Syme, 1979). Of particu- to negative or threatening information when they
lar significance is the fact that the positive impact of are in a positive state of mind (see Fiske & Taylor,
social ties on health is as powerful, and in some 2008, for a review), under threat, people typically
cases more powerful, a predictor of health and lon- need to shore up a sense of self. As such, having to
gevity than well-established risk factors for chronic ask for help or solace or receiving obvious forms
disease and mortality, with effect sizes on par with of assistance may be perceived as threats to the self.
smoking, blood pressure, lipids, obesity, and physi- Consistent with this argument, Bolger and col-
cal activity (House, Landis, & Umberson, 1988). leagues have suggested that the most effective kinds

94 affiliation and stress

of social support are those that are invisible to the in response to specific stressful events and involves
recipient. In a series of studies with couples, they the elicitation of advice, instrumental aid, or emo-
showed that supportive efforts identified by a part- tional comfort. Implicit social support, by contrast,
ner but not perceived by the recipient had greater involves the emotional comfort that one can obtain
effects on the recipient’s emotional well-being from social networks without necessarily disclosing
than support efforts experienced by both the sup- or discussing one’s problems vis-à-vis specific stress-
portive person and the recipient as intended (Bolger ful events. Implicit support may take the form of
& Amarel, 2007; Bolger, Zuckerman, & Kessler, reminding oneself of close others, affiliating with
2000). Visible acts of social support can raise a sense close others without discussing problems, or simply
of obligation or indebtedness and lower self-esteem, perceiving social support to be available without
particularly when the recipient is under stress. actually making use of it.
Other factors may compromise the efficacy of In a series of studies (Kim, Sherman, & Taylor,
socially supportive efforts as well. In their “match- 2008; Taylor, Sherman, et al., 2004; Taylor et al.,
ing hypothesis,” Cohen and McKay (1984) suggest 2007), we found that Asians and Asian Americans
that to be supportive, the actions of a support pro- sought less social support than European Americans,
vider must meet the specific needs of the recipient. and when they were put in a position of needing to
For example, if a person needs emotional support ask for social support, experienced more psycho-
but receives advice instead, the misfired effort at logical distress and stronger arousal. They were,
support may actually increase psychological distress however, psychologically and biologically buffered
(Thoits, 1986). Consistent with this perspective, by the process of merely thinking about their close
Helgeson and Cohen (1996) examined the impact relationships. European Americans, in contrast,
of social contact on adjustment to cancer and found were more comfortable with seeking explicit social
that emotional support was most desired by patients support, namely asking others for help, but were
and appeared to have the greatest beneficial effects not benefitted by merely thinking about their
on adjustment. However, when that support was social relationships. On the surface, these findings
provided in a peer group setting, it did not, for the regarding European Americans would appear to
most part, have benefits; rather, educational groups contradict the findings on invisible support by
that provided information were perceived more Bolger’s research group; however, it may be that
positively. It may be that emotional support is best European Americans are comfortable with asking
provided by people close to the patient such as for social support on their own terms, but that
family and friends (Dakof & Taylor, 1990), and unsolicited social support from close others in times
that educational needs are better satisfied by educa- of threat creates a sense of indebtedness or a threat
tional interventions (Helgeson & Cohen, 1996). to self-esteem.
Recent research suggests that certain adverse As the research on unintended negative effects of
effects of social support may be more acutely expe- social support efforts suggests, there is a disjunction
rienced by East Asians than by European Americans. between findings concerning the benefits of affilia-
Although social support appears to be universally tion and those attesting to the risks of socially
beneficial for mental and physical health, there supportive efforts. Research consistently finds that
are cultural influences on how it is experienced. East strong social networks have a positive effect on
Asians and Asian Americans are more reluctant to mental and physical health in both stressful and
explicitly ask for social support from close others non-stressful times (Thoits, 1995). Research on
than European Americans, because they are more actual support transactions, however, suggests that
concerned about the potential negative relational under many conditions, efforts at support mis-
consequences of such behaviors (Taylor, Sherman, fire for a host of reasons. Although the difference
Kim, Jarcho, Takagi, & Dunagan, 2004). Instead, between the two types of studies may depend on
they are more likely to use and benefit from forms the particular type of evidence gathered and para-
of social support that do not involve explicit disclo- digms used, to the extent that it reflects a reality
sure of personal stressful events and disclosure about social contact, it implies that mere social con-
of distress. tact and the ability to affiliate with others under
Accordingly, one may distinguish between implicit stress may be more beneficial than extracting social
and explicit social support (Taylor, Welch, Kim, & support from others. If you think back to an occa-
Sherman, 2007). Explicit social support involves sion when you were ill, you may remember that it
the specific recruitment and use of a social network was comforting just to leave the bedroom door open

taylor 95
so you could hear other people moving about in the relationships represents redundancy within the
house. Similarly, spouses may experience much of biopsychosocial system, whereby either the psycho-
the benefit of their contact with each other simply logical impetus toward others or the biological
by knowing that the other is around and available impetus or both ensure that affiliative efforts are
and not through the specific social interactions undertaken in times of threat. Future research will
that occur. Carrying this argument one step further, clarify whether this conceptualization is theoreti-
what scientists construe as social support may be cally and empirically useful.
a basic biopsychosocial process that depends heavily
on proximity and/or awareness of others’ availabil- Conclusions
The tendency to affiliate with others under stressful
ity more than on the explicit social support trans-
conditions is one of the most basic responses that
actions that have been so widely studied.
human beings have for coping with a broad array of
Future directions stressful and threatening circumstances. Unlike the
Substantial empirical progress has been made in fight-or-flight response that has typically guided
understanding the biopsychosocial underpinnings research, tend and befriend characterizes the fact
of affiliation in response to stress. In the near future, that humans come together for mutual protection
we can expect to see additional insights regarding and solace and to protect offspring. These affiliative
the roles of oxytocin, vasopressin, and the opioid responses to stress have both biological and psycho-
system in eliciting and responding to affiliative con- logical origins and effects. Affiliating with others is
tact. We may also see additional clarity regarding inherently comforting under most conditions, and
genetic bases of social support needs and per- so people often choose to affiliate with others when
ceptions. On the social psychological side, the times are stressful so as to gain emotional comfort,
benefits of giving as well as receiving social support information about a stressor, tangible assistance,
will become increasingly understood (e.g., Brown, and reduced physiological reactivity. Biologically,
Nesse, Vinokur, & Smith, 2003). these effects may depend upon oxytocin and brain
Our current conceptualization of the role of opioid pathways that provide a signal to the organ-
affiliation in protection against stress may require ism that the social environment is lacking and that
some rethinking. Human biological systems are provide an impetus to seeking social contact. Part
marked by substantial redundancy. In other words, and parcel of this response is the fact that social iso-
activities that are vital to survival are often main- lation is experienced as aversive, and rising endoge-
tained by more than one biological process. There nous oxytocin levels in response to isolation may
are, for example, five different ways by which the prompt affiliative behavior.
stomach can produce hydrochloric acid for the The biological benefits of affiliation are clear.
digestion of food. Other more obvious examples of Studies of early life experience provide unequivocal
redundancy include the fact that people have two evidence that nurturant mothering helps to shape
eyes, two hands, two lungs, two kidneys, and so on. biological stress regulatory systems as well as craft
This is not to say that all vital biological systems are socioemotional skills that aid in the creation of
backed up through redundancy, the heart being an social networks and the seeking of social support
obvious counterexample. Nonetheless, it may be across the lifespan. Genetic factors and epigenetic
useful to think about psychological processes as processes are also implicated in these pathways. The
implicated in this redundancy. That is, vital pro- interplay of these early influences with the availabil-
cesses may be backed up not only through multiple ity of supportive others during times of acute stress
biological mechanisms, but through a combination leads reliably to ameliorative effects on both psycho-
of psychological and biological mechanisms as well. logical distress and biological responses to acute
In this viewpoint, the human impetus toward group stressors.
living as well as human beings’ tendencies to affiliate The consequences of affiliation under stress for
with others in stressful times may have multiple psy- mental and physical health are very well established.
chological and biological origins. Affiliation is psy- Although there are circumstances under which
chologically satisfying, and during times of stress, efforts at social support backfire and may actually
human beings experience a psychological need, as worsen the situation, social support nonetheless has
well as a biological impetus, toward affiliating with effects on health on par with smoking, lipids, and
others. It is possible that the psychological architec- other well-established biological risk factors. On the
ture that leads people toward comforting social whole, the perception that one has social support

96 affiliation and stress