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 Multiple influencesMultiple mediators
StressDurationType of stressContextAgeSexGenesNoradrenalineDopamineSerotoninCRHUrocortinsVasopressinOrexinDynorphinCorticosteroidsNeurosteroids
Any acta r ptentia distrbance f anindivida’s envirnent — a ‘stressr’ — isrecgnized r perceived by specific brainregins. The sbective state f sensingptentiay adverse changes in the envirn-ent is caed ‘stress’ and eads t the reeasef eces that we here ca ‘stress edia-trs’, which bind t receptr targets. Each f these ediatrs acts n specific nernappatins, resting in niqe dwnstreaeffects. Tgether, these effects cnstitte the‘stress respnse’, which enabes the ania tadapt t the changing envirnent
1–4
.A perpexing aspect f the stress respnseis its cpexity. Varis stress ediatrshave been described, incding ner-transitters (fr exape, nradrenaineand sertnin), peptides (fr exape,crtictrpin-reeasing hrne (CRH),ther ebers f the CRH faiy and vas-pressin) and sterid hrnes (fr exape,crtis in hans and crticsterne inrdents). What is the reasn fr the exist-ence f these tipe instrents? Is therent a staggering degree f redndancy?In this Perspective we initiay discss thecharacteristic spatia and tepra niches f key stress ediatrs and prvide eergingevidence that these niches verap, affrdingpprtnities fr interactins between edi-atrs. We then highight these interactins,shwing that the stress ediatrs act in cn-cert. We arge that the diversity f the instr-ents f stress, rather than being redndant,enabes bth ptia niches f actin freach ediatr and interactins betweenthe tipe ediatrs that rchestrate rbrains rearkabe abiity t respnd — andadapt — t a dynaic envirnent.
A eed fr multle medatrs
Stress signifies a ptentia r acta threat thatreqires iediate changes in behavir aswe as a dificatin f ftre behavirs.This is achieved thrgh the datin f nerna fnctining at severa eves f theCNS — eves that gvern decisin aking,earning and ery as we as hrna,atnic and etina respnses.Different types f stressrs reqire dif-ferent respnses
(FIG. 1)
. The stressr typeinfences the repertire f nerna ppa-tins that perceive a ptentia threat, as weas the nerns and stress ediatrs thatare engaged in the adaptive respnse. Frexape, physica stressrs sch as bd ss,traa and cd rapidy recrit the brainsteand hypthaaic regins
1,3
, whereas psy-chgica stressrs sch as scia ebarrass-ent, exainatins r deadines priariy engage stress ediatrs in brain regins thatsbserve etin (the aygdaa and theprefrnta crtex), earning and ery (thehippcaps) and decisin aking (the pre-frnta crtex)
2,4,5
. These are nt segregatedsystes, becase physica stressrs ften havepsychgica aspects and vice versa.The dratin f the stressr as greaty infences the natre f the nernarespnses
(FIG. 1)
. Acte stressrs — frexape, a rapidy appraching car — casea rapid srge f nertransissin, ner-na activatin and hrne reease. This isfwed by rapid retrn t baseine eves,athgh the teprary activatin f, frexape, hippcapa and hypthaaicnerns can tiatey ead t ateratins
opinion
The neuro-symphony of stress
Marian Joëls and Tallie Z. Baram
Abstact | The impact of stess on bain function is inceasingly ecognized. Vaioussubstances ae eleased in esponse to stess and can influence distinct neuonalcicuits, but the functional advantages of having such a divesity of stess mediatosemain unclea. Individual neuotansmitte, neuopeptide and steoid stessmediatos have specific spatial and tempoal niches, but these niches also ovelap.In addition, the effects of individual mediatos on neuonal function and plasticityae integated, and emeging evidence suggests that thee is cosstalk betweenthem. Togethe, this esults in the stess instuments poducing an ochestated‘symphony’ that enables fine-tuned esponses to divese challenges.
Figue 1 |
Dffnt t q dffntpn.
Many factos influence the pattenand magnitude of the esponse to stess, includ-ing the duation of stess exposue (acute vesuschonic), the type of stess (physical vesus psy-chological), the stess context (fo example, timeof day), the developmental stage of the animal(newbon, adult o aged) and the animal’s sex andgenetic backgound. The panoply of unique stesssituations and neuonal populations that espondto them to affect neual and behavioual plasticityon a timescale fom seconds to yeas is not wellseved by a single mediato — hence the need fomultiple instuments, so that each combination of mediatos addesses the specific aspects of astesso. The molecules that convey the stess sig-nal to the CNS and that contibute to the esultingfunctional changes in the CNS (stess mediatos)include monoamines, neuopeptides and steoidhomones, examples of which ae shown on theight. Each mediato has a pefeed activitydomain in space and time.
PErSPECTIVES
NATuRE REVIEWS
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NeuroscieNce 
VolumE 10
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juNE 2009
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 459
focus on stress
© 2009 Macmillan Publishers Limited. All rights reserved
 
in gene expressin, which in trn changesbseqent nerna respnses. By cntrast,chrnic stress (typicay defined as stress thatasts a week r re) prvkes sstainedand/r prgressive changes in the expressinf particar genes, strctra ateratinsin nerns and changes in nerna firingpatterns thrght the brain
4,6
. If schchanges persist they can rest in prngeddeviatins fr the rigina fnctining f the netwrk 
3
.In additin, the characteristics f therespnding brain deterine the pattern andagnitde f its respnse t a stressr. Frexape, the age f the ania infencesthe ikeihd f a signa being perceivedas a stressr. It as infences the edia-trs that are reeased by stressrs, and theircnseqences
3,7,8
. Fr exape, in rdentsthe ecar cascades that are activated by stress in the hypthaas
9,10
and the hip-pcaps
9,11
dring adthd differ frthse that are activated by stress in the infantand change again
 
with aging
7,12
. In additin,sex and genetic factrs interact with ifeevents, sch as envirnenta enrichentr isatin, t cntribte t the diversity f the stressrs and their ipacts n anindivida’s brain.Taken tgether, the arge array f stresstypes and cntexts, the genetic backgrnd,age and sex f the stressed ania, as weas additina factrs sch as the pint in thecircadian rhyth at which the stressf eventtakes pace, create a rich and cpex atrixf stressrs. Each niqe stress sitatinreqires an efficient respnse fr ner-s nerna ensebes thrght theCNS, a prcess that reqires astte rches-tratin. This rchestratin ccrs thrghthe depyent f a repertire f signaingeces that can bring abt the tepra,spatia and cntext specificity f eachindivida stress respnse.
The dversty f stress medatrs
Each stress ediatr has its characteristic,‘cassic’ spatia and tepra dains. Bewwe eabrate n the preferred spatia andtepra dains f the three ain cassesf stress ediatrs and their individacntribtin t the brain’s stress respnse, asa preabe t discssing their crdinatedand interactive effects.
 Monoamines.
Shrty after a stressf event,the reease f naines, incdingnradrenaine, dpaine and sertnin,is increased in specific nerna ppa-tins
13–16
. This reease is triggered by braincircits that are invved in the evaatin f the stressf event r is triggered indirecty,thrgh activatin f the sypathetic nerv-s syste
1,5
. The extent t which n-ainergic systes are activated depends nany factrs, incding sex (fr exape,see
reF. 17
), the tie f day 
18
and the cn-trabiity r recrrence f the stressr
13
.Fr instance, activatin f raphe nerns(which prdce sertnin) by shck exp-sre is ny prinent when the sitatin isncntrabe
13,19
.An enhanced reease f nainesafter stress has been denstrated in thehippcaps, the aygdaa, the prefrntacrtex and the nces accbens, bt itprbaby as takes pace in any therbrain regins. Hwever, the spatia distri-btin f the cnseqences f this reeasedepends as n the affinity and distribtinf the naine receptr sbtypes. Ths,the cbinatin f reease site and receptrdistribtin and affinity prvides a singestress ediatr with tipe spatia nichesand different fnctins.Stress-indced nainergic reeaseand actins are fast. The reease is generay indced within intes after the nset f thestressr (athgh regin-specific differencesexist
20
) and sed tasts the dratinf stressr expsre. Becase nainesgeneray act thrgh G prtein-cpedreceptrs, which rapidy transfer their acti- vatin t dwnstrea effectrs, the rapidrise in their eve is qicky transated intatered fnctining f nerns that expressthese receptrs.Each naine cntribtes t spe-cific behavira aspects f the iedi-ate respnse t the stressr. Fr instance,increased eves f nradrenaine sppsedy case a shift fr fcsed prcessing f sensry infratin t a re genera scan-ning f the envirnent, which ay prvidebetter stins fr chaenging cndi-tins
21
. Dpaine, which is reeased dringderate stress in the prefrnta crtex
15
,is thght t iprve risk assessent anddecisin strategies, and sertnin is instr-enta in redcing pst-stress anxiety 
22
.Ths, naines cectivey prteiprtant behavira strategies that hepthe ania face and srvive the initia phasef a stressf event.
 Neuropeptides.
A nber f nerpeptidesare reeased by stress in specific ner-na ppatins and cntribte, ften by activating tipe receptrs, t the stressrespnse
11,23–26
. Athgh severa f thesestress-indced nerpeptides as act nperiphera receptrs, we fcs here n theirreease and actins in the brain
(TABLe 1)
.
Table 1 |
Examles f stress-actvated euretdes  the bra
Pptdrlalatn rpt(and ptlatn)Fntnlatd tt
CrHCental amygdala
30,34,35
CrHr1 (basolateal amygdala)
30,34,38,78
 CrHr2
 
(reF. 74)
Stess/emotional memoy, anxiety
30,33,35,80
 Temination of stess-elated anxiety
31–33
Locus coeuleus
28
CrHr1 (locus coeuleus)
60,78
Inteaction with noadenaline systems
28
Hippocampal inteneuons
27,56
CrHr1 (pyamidal cells)
11,39,48,56,78
Stess-elated leaning and memoy
3,36,39
BnST
26,81
CrHr1
 
(reFs 48,81)
(nucleus accumbens)
81
andCrHr2
 
(reFs 74,78,81)
Stess-elated anxiety
26,30
UocotinNon-ganglionicEdinge–Westphal nucleus
41
CrHr1 and CrHr2 Inteaction with CrH systems duing acuteand chonic stessUocotin 2 and 3CrHr2
 
(reF. 41)
role in stess not establishedVasopessinHypothalamic denditesBnST and amygdala
25,26,43
V1A (septum, hippocampus, BnST and otheaeas) and V1BStess-elated and social memoy, andpehaps emotionality
25,26,43
OexinLateal hypothalamic aea
26
OX1 and OX2Stess-elated enegy and sleep homeostasisDynophinHippocampal dendites
82
Seveal opioid eceptos
26
Stess-elated dysphoia
26
BnST, bed nucleus of the stia teminalis; CrH, coticotopin-eleasing homone; CrHr,
 
CrH ecepto; OX, oexin ecepto; V1, vasopessin ecepto 1.
PersPectives
 460
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juNE 2009
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VolumE 10
www.nat.m/vw/n
 
PersPectives
© 2009 Macmillan Publishers Limited. All rights reserved
 
 
β
1R CRHR1CRHR2MR GR MedialprefrontalcortexCA1CA3Lat.septumBnSTPVNCeAMABLALCNTSDR DG
We cnfine the discssin t CRH and vas-pressin, athgh ther peptides as edi-ate the effects f stress (rexin, ghrein anddynrphin) r cnteract the stress respnsender specific cntexts (xytcin and ner-peptide Y); additina peptides ay regatestress-reated anxiety and dysphria (frexape, gaanin and sbstance P)
26
.The cannica stress-activated ner-peptides incde the CRH faiy and vaspressin, which were first discvered inthe hypthaas
24,25
. CRH is reeasedin respnse t stress fr axn terinas inthe hypthaaic edian einence and actsn receptrs in the pititary 
24
. Hwever, it isnw knwn t as be expressed in nernappatins in the aygdaa
24,26
, the hipp-caps
27
and the cs ceres
28
. Actingcay, the peptide exerts nerdatry effects n target nerns within secndsafter its reease
9,29,30
, thrgh tw G prtein-cped receptrs, CRHR1 and CRHR2.CRH receptr ccpancy infences ner-na firing patterns
9,29,30
, gene expressin
11,26
 and behavir
11,26,31–33
, in a CRH dse- andcntext-dependent anner. Fr exape,reease f CRH in the centra nces f the aygdaa dring acte stress enhancesery cnsidatin
34,35
, and CRHreeased by dest stress fr hippcapainternerns
11,56
pries ng-ter ptentia-tin
36
and iprves ery 
37
. By cntrast,hippcapa reease f arge ants f CRH in respnse t severe stress
38,39
can eadt hyperexcitabiity and seizres
9,40
and trapid ss f dendritic spines in CA3pyraida ces
39
. CRH ight ascntribte t the strctra changes inhippcapa pyraida ces that are pr- vked by chrnic stress in bth adt anddeveping brains
4,12,38
. other ebersf the CRH nerpeptide faiy, incdingthe rcrtins (uCN1, 2 and 3), can bindt CRH receptrs and act in distinct spatiadains. Ths, uCN1-expressing nernsin the nn-preganginic Edinger–Westphances in the brainste ight cntribte tstress adaptatin
41
.In the hypthaas, vaspressin inter-acts with CRH, prting adrencrtic-trpic hrne (ACTH) reease fr thepititary in respnse t stress
42
. In the brainas a whe, vaspressin acts n a wide array f nerns
25,43
 
(TABLe 1)
: in the aygdaa,the excitatry actins f vaspressin, per-haps reeased fr dendrites
25
, ight cn-tribte t the behavira stress respnse.Vaspressin ight as date etinaery and anxiety 
26
.The ‘activating’ actins f stress-indcedCRH reease are ediated priariy thrghbinding t CRHR1
(reFs 11,28,33,39)
, andthe panpy f effects described abve takepace in a tie frae f secnds t intes.In additin, stdies in knckt ice sg-gest that CRHR2 binding cd exert effectsat nger tiescaes and ight fnctin tsht dwn the stress respnse
31,32
. The yin–yang fnctins f the tw CRH receptrsdescribed abve are rearkaby siiar tthe res f the tw crticsterid receptrsin ediating the eary and ate effects f stress-indced crticsterid reease nnerns, as described bew.
Steroids.
Crticsterids are secreted ina psatie and circadian fashin; stresstriggers the reease f a arge brst f cr-ticsterids that is speripsed n theserhyths
44
. Crticsterids’ access t thebrain is regated by p-gycprteins
45
 (hwever, see
reF. 46
), bt the circadianpattern and the stress-indced srge f crticsterid eves are aintained in thebrain (as was recenty denstrated frthe hippcaps
47
), awing peripheraand centra aspects f the stress respnset be integrated. A brain ces, incdinggia, are in principe expsed t crtic-sterid hrnes — this cntrasts withthe spatiay restricted pathways thrghwhich naines and peptides exert theiractins.
 
Nevertheess, the sites in the brainwhere crticsterids are effectiveare restricted by the distribtin f crticsterid receptrs.In the aaian brain, crticsteridhrnes priariy act thrgh inera-crticid and gccrticid receptrs(mRs and GRs, respectivey). mRs have ahigh affinity fr crticsterids, s they aresty ccpied even when circating cr-ticsterid eves are w
2
. GRs have tenfdwer affinity; cnseqenty, these recep-trs are ny partiay ccpied nder basacnditins and bece re ccpied ascrticsterid eves increase — fr exape,after stress. The tw receptr types are dif-ferentiay distribted in brain
2
. mRs arehighy expressed in nerns f the hipp-capa fratin and the atera septand deratey expressed in sbncei f theaygdaa, the hypthaaic paraventric-ar nces (PVN) and the cs ceres
(FIG. 2)
. These regins define a circit thatis invved in the cgnitive, etina andnerendcrine prcessing f stressfevents
5
. The distribtin f mRs ths ver-aps with the distribtin f CRHR1
(reF. 48)
.GRs are biqitsy expressed in the brain,bt they are enriched in the hippcaps,the atera sept and the PVN.on binding f the hrne, crtic-sterid receptrs transcate t the nces,where they act as regatrs f gene tran-scriptin
49
. Therefre, sterid effects nnerna fnctin say reqire at eastan hr t devep and ast hrs t days.In the hippcaps, mR activatin is aprereqisite fr aintaining the nginginfratin fw
6
, whereas activatin f 
Figue 2 |
‘Ht pt’ f pt f ky t mdat.
The
β
1-adenoceptos fo noadena-line (
b
1rs), CrH ecepto 1 (CrHr1), CrHr2 and the minealocoticoid and glucocoticoid eceptos(Mrs and Grs, espectively) cluste in ‘hot spots’ in the bain. These hot spots include the pefontalcotex, specific amygdala nuclei, the hippocampus (CA1, CA3 and the dentate gyus (DG)), the pa-aventicula nucleus of the hypothalamus (PVN), the dosal aphe nuclei (Dr) and the locus coeuleus(LC). In these aeas, eceptos fo at least two classes of mediatos ae highly expessed. The hot spotsae stategic hubs that connect netwoks involved in divese aspects of the bain’s stess esponse,including leaning and memoy, decision making and homonal, autonomic and emotional esponses.BLA, basolateal amygdala; BnST, bed nucleus of the stia teminalis; CeA, cental amygdala; CrH,coticotopin-eleasing homone; lat. septum, lateal septum; MA, medial amygdala; NTS, nucleustactus solitaii. Data fom
reFs 48,74–78
.
PersPectives
NATuRE REVIEWS
|
 
NeuroscieNce 
VolumE 10
|
juNE 2009
|
 
 461
focus
 
on stress
© 2009 Macmillan Publishers Limited. All rights reserved
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