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Resiliece refers t a pers’s ability t aapt sccess-flly t acte stress, traa r re chric frsf aversity. A resiliet iivial has ths bee testeby aversity 
1
a cties t estrate aaptivepsychlgical a physilgical stress respses, r‘psychbilgical allstasis’
2,3
. The sty f resiliece,r stress-resistace, rigiate i the 1970s with a grpf researchers wh irecte their atteti t the ivesti-gati f chilre capable f prgressig thrgh ralevelpet espite expsre t sigificat aversity 
4
.Fr ay years research fcse  ietifyig thepsychscial eteriats f stress resistace, sch aspsitive etis, the capacity fr self-reglati, scialcpetece with peers a a clse b with a priary caregiver, ag ther factrs
5,6
. Later sties tret erstaig the psychscial eteriats f resiliece i traa-expse alts
7,8
.It is ly i recet years that sigificat scietifica techlgical avaces have ae it pssible tbegi t ersta the erlyig bilgical prcessesassciate with resiliet phetypes
3,9
. Fiigs frrecet sties sggest that geetic ifleces  bilgi-cal respses — sch as eral respses t affectivestili, easre with brai iagig — are larger thageetic ifleces  cplex behaviral respses
10,11
.Exaiig stress respses at ltiple phetypic lev-els, iclig t ly behaviral a psychlgicaleasreets, bt als easreets f erchei-cal, erecrie a eral systes, cl thshelp t elieate a itegrative el f resiliece
11
.Aial sties are a key cpet i the search frbilgical eteriats f resiliece, a are begi-ig t ietify eral circits a leclar pathwaysthat eiate resiliet phetypes
1,12
.
This Review t-lies a attepts t itegrate recet evelpetsi resiliece research fr psychscial, evelpetal,geetic a erbilgical perspectives.
Psychosocial factors in resilience
Sties have ietifie a rage f psychscial factrsthat prte sccessfl aaptati t stress a thatight help t prevet the set f psychiatric isr-ers sch as pst-traatic stress isrer (PTSD),ar epressive isrer a thers. We are wbegiig t ietify the erbilgical echa-iss that erlie se f these traits
(BOX 1)
. These f active cpig strategies sch as prble slv-ig a plaig has bee like t iprve well-beig a a greater capacity t hale stressflsitatis i iverse pplatis, ragig frtraa-expse t eically ill iivials
13
. Activecpig with stress
 
reqires a iivial t face theirfears, a resiliet iivials exhibit lwer levels f eial, aviat cpig behavir a behaviralisegageet
8,14
. Resiliet iivials are als char-acterize by ispsitial ptiis a high psitiveetiality 
15,16
. Psitive etis prte aaptivecpig a peess t scial spprt
15
, a are ass-ciate with greater flexibility f thikig a expl-rati, a braee fcs f atteti a ecreaseatic activity 
17
. Resiliece has bee like tbeig able t perceive stressfl evets i less threate-ig ways, prtig aaptive cpig strategies
13
; schcgitive reappraisal allws iivials t re-evalater refrae averse experieces i a re psitivelight. Scial cpetece a the ability t haress
*Department of Psychiatry,Mount Sinai Schoo of Medicine;
Departments of Psychiatry,Neuroscience, and Pharmacoogy and SystemsTherapeutics, Mount Sinai Schoo of Medicine, New York,New York 10029, USA.Correspondence to A.F.e-mai:adriana.feder@mssm.edu
doi:10.1038/nrn2649
Psychobiology and moleculargenetics of resilience
 Adriana Feder*, Eric J. Nester 
and Dennis S. Charney
Abstract | Every individual experiences stressful life events. In some cases acute or chronicstress leads to depression and other psychiatric disorders, but most people are resilient tosuch effects. Recent research has begun to identify the environmental, genetic, epigeneticand neural mechanisms that underlie resilience, and has shown that resilience is mediated byadaptive changes in several neural circuits involving numerous neurotransmitter andmolecular pathways. These changes shape the functioning of the neural circuits that regulatereward, fear, emotion reactivity and social behaviour, which together are thought to mediatesuccessful coping with stress.
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© 2009 Macmillan Publishers Limited. All rights reserved
 
scial spprt have als bee like t better etalwell-beig a health. Icrease scial spprt hasbfferig effects  etal a physical illess afsters aaptive cpig strategies
13
. other psychscialcharacteristics assciate with stress resiliece iclea sese f prpse i life, a ral cpass, spirit-ality a the ability t fi eaig i the ist f traa
8,13,18,19
.Althgh ay f the abve psychlgical character-istics cat be easre i aials, se behaviraltraits assciate with resiliece have bee ietifie. Iers aial els (seeSppleetary ifra-ti S1(bx)), rets isplay a rage f respses tstress: at e extree are active r ‘fight–flight’ respses(fr exaple, attepts t escape a aggressi), aat the ther extree are passive respses (fr exa-ple, freezig a sbissi)
27
. Active-cpig aialsare fte csiere t be resiliet, base  er-s fctial e pits, whereas their re passivecterparts are t; hwever, bth types f respsesca be see as aaptive epeig  the particlar c-text. The availability f these aial els has aeit pssible t sty the erbilgical a leclarechaiss that erlie these behaviral traits, as isiscsse belw.
Resilient responses to stress
ners hres, ertrasitters a er-pepties are ivlve i the acte psychbilgicalrespses t stress. Differeces i the fcti, balacea iteracti f these factrs erlie iter-iivial variability i stress resiliece.
Hypothalamus-pituitary-adrenal (HPA) axis.
 Crtictrpi-releasig hre (CRH) is release by the hypthalas i respse t stress, leaig t acti- vati f the HPA axis a the release f crtisl. Early life stress has bee like t chrically high levels f CRH i ha a aial sties
20
(BOX 2)
. Althghthe shrt-ter actis f crtisl are prtective a pr-te aaptati, sstaie expsre t abrally highlevels f crtisl ca be harfl, leaig t hyperte-si, isppressi, carivasclar isease ather health prbles
21
. I the brai, excessive crtisl isassciate with cplex strctral effects i the hipp-caps a aygala i has a aials, icl-ig atrphic effects i certai types f ers
22,23
. Ths,rece CRH release a aaptive chages i CRHreceptr activity ight prte resiliece.I several aial els a i se ha sties,resiliece is assciate with rapi activati f the stressrespse a its efficiet teriati
24
. Resiliece isassciate with the capacity t cstrai stress-iceicreases i CRH a crtisl thrgh a elabrate eg-ative feeback syste, ivlvig ptial fcti abalace f glccrtici a ieralcrtici recep-trs
3,24,25
. Sties sggest that the HPA istrbaces thatare assciate with PTSD are ifferet fr thse that areassciate with ar epressi
24
. of te, aials thatapt active respses t eviretal threat shwlwer glccrtici respses tha thse that apt pas-sive respses, althgh the relatiship betwee cpigstrategies a HPA axis activity is prbably cplex (frexaple, see
REF. 26
). I has these tw persal-ity types have bee like with risk fr ifferet sets f 
Box 1 |
Psychosocial factors and possible neurobiological underpinnings associated with resilience
Facng fas an ac copng
Facing fears promotes active coping strategies such as planning and problem solving. The ability to face one’s fears mightbe facilitated by stress inoculation (exposure to tolerable levels of stress) during development, and might be linked to theoptimal functioning of fear extinction mechanisms. Active, or ‘fight–flight’, responses in animals have been linked tomore transient activation of the hypothalamus-pituitary-adrenal (HPA) axis
27
, although the relationship between HPAaxis activity and active or passive coping might not be straightforward, as positive associations have also been found
26
.Physical exercise, which can be viewed as a form of active coping, has positive effects on mood, attenuates stressresponses and is thought to promote neurogenesis
13
.
Opmsm an pos moons
Positive emotions might contribute to healthier cognitive responses
17,128
and decreased autonomic arousal
128
. Mesolimbicdopamine pathways might be more reward responsive and/or stress resistant in individuals who remain optimistic whenfaced with trauma
3
. Accordingly, resilience in animals has been related to specific molecular adaptations in themesolimbic dopamine system
41
.
Cogn appasa, pos famng an accpanc
Cognitive reappraisal involves reinterpreting the meaning of negative stimuli, with a resulting reduction in emotionalresponses. Resilient individuals might be better at reappraisal or might use reappraisal more frequently. Neurobiologicalmechanisms that underlie some of these processes include memory suppression, memory consolidation and cognitivecontrol of emotion
106,107
.
Soca compnc an soca sppo
Social competence and openness to social support promote resilience in children and adults
5,13
. Mutual cooperation isassociated with activation of brain reward circuits. Oxytocin enhances the reward value of social attachments andreduces fear responses. Future research might identify potential differences in these measures in resilient individuals.
Ppos n f, a moa compass, manng an spay
A sense of purpose and an internal framework of beliefs about right and wrong are characteristic of resilientindividuals
8,13
. Religious and spiritual beliefs and practices might also facilitate recovery and finding meaning aftertrauma
13
. Brain imaging studies are beginning to identify the neural correlates of human morality
129
.
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© 2009 Macmillan Publishers Limited. All rights reserved
 
isrers, estratig that the relatiship betweehealth a the fctiig f the stress respse sys-te is cplex
27
. I aiti, ehyrepiarstere(DHEA), which is als release i respse t stress, hasatiglccrtici effects i the brai. Higher DHEAslphate/crtisl ratis i iivials ergig rigr-s ilitary srvival traiig were assciate with lwerissciative sypts a better ilitary perfrace,pssibly iicatig higher resiliece t stress
28
. I a sty f ale veteras with PTSD, higher DHEA levels wereassciate with sypt iprveet
29
. DHEA hasaitial cetral effects i the brai, tably  theGABA (γ-aibtyric aci)-ergic syste, which clals play a part i resiliece
30
.
 Noradrenergic system.
Stress als leas t release f rarealie fr braiste clei, st iprtatly the lcs cerles. The reslt is icrease rare-ergic stilati f ers frebrai areas ipli-cate i etial behavir, sch as the aygala,the cles accbes, the prefrtal crtex (PFC)a the hippcaps (see belw). uchecke, chrichyper-respsiveess f the lcs cerles rare-ergic syste is assciate with axiety isrers acarivasclar prbles, a blckae f β-areergicreceptrs i the aygala ca ppse the evelpet f aversive eries i aials a has
31,32
. This sg-gests that rece respsiveess f the lcs cerlesrareergic syste cl prte resiliece.
Serotonergic and dopaminergic systems.
Serti e-rs prect wiely i the brai. Acte stress is assci-ate with icrease serti trver i several brairegis, iclig the aygala, the cles accbesa the PFC. Serti lates eral respsest stress, with bth axigeic a axilytic effects(epeig  the brai regi a receptr sbtypeivlve)
3
. Serti fcti is als clsely like t reglati. Dpaie ers are activate irespse t rewar r the expectati f rewar ageerally are ihibite by aversive stili, as etailebelw. Dpaie sigallig facilitates fear exticti,bt its rle i resiliece
 per se
is clear.
 Neuropeptide Y (NPY).
 nPY, a erpeptie that iswiely istribte i the brai, has axilytic-like effectsi rets a is thght t ehace cgiti erstressfl citis. nPY als cteracts the axi-geic effects f CRH i the aygala, the hippcaps,the hypthalas a the lcs cerles, a resilieceight ivlve aitaiig a balace betwee nPY aCRH levels
 
rig stress
33
. I a sty f special frcessliers, wh are csiere t be highly stress resiliet,higher nPY levels rig rigrs ilitary traiig wereassciate with better perfrace
34
. Ather sty f higher plasa nPY levels i cbat-expse vet-eras witht PTSD tha i thse with PTSD
35
. Thesefiigs i has are csistet with recet sties irats: cetral aiistrati f nPY i rats ihibits theevelpet, a prtes the exticti, f fear c-itiig, with nPY atagists exertig the ppsiteactis. These effects are eiate at least i part by theaygala
36
. mrever, itra-aygala nPY aiistra-ti prtes resiliet respses t stress, i the frf rece axiety-like behavirs i respse t acterestrait
37
.
Brain-derived neurotrophic factor (BDNF).
 BDnF, aiprtat erve grwth factr that is expresse at highlevels i the brai, is best kw fr its rle, i retels, i prtig the fctiig f the alt hip-pcaps, iclig the srvival f ewly br gra-le cell ers thrght alt life. I rets, stressecreases BDnF expressi i the hippcaps, aeffect that is reverse by chric atiepressat treat-et
38
. Siilar fiigs have bee bserve i hahippcaps exaie pst-rte. Hwever, BDnFexerts very ifferet effects i ther brai regis.Chric stress icreases BDnF expressi i the retcles accbes, a this has bee like t pr-epressi-like effects i several behaviral assays
39,40
.Iterestigly, this icti f BDnF is casally relatet the egree t which rets are vlerable verss
Box 2 |
Development of resilience
eay f sss an naby
Early physical and sexual abuse is associated with long-lasting interrelated hormonal,neurotransmitter and CNS changes
20,130,131
that are likely to mediate increasedvulnerability to psychiatric disorders into adulthood.Animal studies have shown that prolonged maternal separation in early life hasenduring adverse effects on stress responsivity
20
.
rsnc o ay f sss
Studies in children adopted away from institutional orphanages in Romania illustratethe capacity of adaptive systems to resist or recover from marked disturbances whenthey are healthy and functional
4,132
.Rodent studies have demonstrated that a positive, or more enriched, environmentduring development makes animals less vulnerable to drugs of abuse and to stress laterin life
133
, and can even reverse some of the behavioural impairments that are inducedby early prolonged maternal separation
134
.
rsnc facos
During development a range of factors are potentially protective, as identified instudies of children. These include a close relationship with a caring adult, socialcompetence and agreeableness, positive emotionality and the capacity for self-regulation
135–137
. In particular, studies have shown that proximity to the caregiver is animportant modulator of a child’s sense of safety when facing trauma, as recognized inthe theory of attachment
122,123
. Rodent studies have shown that high levels of licking,grooming and arched-back nursing produce offspring that are less fearful as adults andthat show attenuated hormonal responses to stress
66
. Cross-fostering experimentshave demonstrated that these effects are transmitted behaviourally, and recentresearch has suggested an epigenetic basis for this phenomenon
 
(see main text)
66,138
.
It is also likely that exposure to manageable stressors during development isassociated with more adaptive coping with stress during adulthood
139
. In studies of squirrel monkeys and rodents, early exposure to manageable stressors (‘stressinoculation’) was found to be associated with reduced behavioural and hormonalresponses to stress later in life
65,140
. Adaptive responses seem to be associated with thedegree of behavioural control an animal has over stress
141
.Finally, the theory of predictive adaptive responses posits that early life experiencecan programme a certain set of responses that may be adaptive given a particular earlyenvironment, but that may prove maladaptive later on if there is a mismatch betweenthis set of responses and the environment in adulthood
142
. In a recent rodent study, theadult offspring of low- as opposed to high-licking and grooming mothers demonstratedgreater experience-dependent structural plasticity and learning under some contexts,but lesser structural and behavioural plasticity in other contexts
143
.
REVIEWS
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|
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|
VoLumE 10
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