VOLUME 70, No.

2 THE QUARTERLY REVIEW OF BIOLOGY JUNE 1995

FEAR AND FEARFULNESS IN ANIMALS

ALAIN BoissY
aux Milieux, INRA Centrede TheixClermont-Ferrand
Adaptationdes Herbivores
F-63122 Saint-Genes-Champanelle,
France
ABSTRACT
Persistence ofindividual differences inanimalbehavior in reactionstovarious environmental
challengescouldreflect basicdivergences intemperament, whichmight beusedtopredict details
ofadaptive response.Although studies havebeencarried outonfear andanxiety invarious species,
includinglaboratory, domestic andwildanimals, noconsistent definition
offearfulnessas a basic
traitoftemperament hasemerged.
After a classificationoftheevents thatmayproduce a stateoffear,thisarticle describes the
greatvariability in behavior and inphysiological patterns generallyassociated withemotional
Thedifficulties
reactivity. ofproposing fearfulness - thegeneral capacitytoreacttoa variety of
potentially
threatening situations - as a validbasicinternal variablearethen discussed.Although
therearemanystudiesshowing covariation amongthepsychobiological responsestodifferent
environmental challenges, other studies findno suchcorrelations and raisedoubtsaboutthe
interpretation
offearfulness as a basicpersonality trait.Aftera critical
assessment ofmethodologies
usedinfearandanxiety studies, it is suggested thatdiscrepancies among resultsaremainly due
tothemodulation ofemotional responses in animals,whichdepend on numerous genetic and
epigenetic
factors. It is difficult tocompare results obtained bydifferentmethods fromanimals
rearedunder various conditions andwithdifferent geneticorigins.
Theconcept offearfulness as aninner traitis best
supported bytwokinds ofinvestigations.First,
an experimental approach combining ethology andexperimental psychology produces undeniable
indicatorsofemotional reactivity. Second, genetic linesselectedforpsychobiologicaltraitsprove
usefulin establishing relationships between behavioral andneuroendocrine aspectsofemotional
It is suggested
reactivity. thatfearfulness couldbeconsidered a basicfeatureofthetemperament
ofeachindividual, onethat predisposes ittorespond similarlytoa varietyofpotentiallyalarming
challenges,butis nevertheless continually modulated during development bytheinteraction of
genetictraitsofreactivity withenvironmentalfactors, particularlyin thejuvenile period.Such
interactionmayexplainmuchoftheinterindividual observed
variability inadaptive responses.

The Quarterly
Reviewof Biology,June 1995, Vol. 70, No. 2
Copyright ? 1995 by The University of Chicago. All rights reserved.
0033-5770/95/7002-0002$1.00

165
166 THE QUARTERL Y REVIEW OF BIOLOGY
IT IS CLEAR thattherearebehavioraldif- subsequentlybeen challenged,or at least mod-
ferencesnot only among species but also
among individualsofthe same species(Plomin
et al., 1990). Several studies reveal that there
is considerable individual variabilityin many
aspects of behavior, even when animals are
reared under the same conditions. Demon-
stratedconsistencyofinterindividual variability
over time and in response to environmental
changes could indicate the existence of basic
dimensions ofpersonality,as has been argued
already forhumans (Zuckerman, 1991).
Among these psychologicalcharacteristics,
an individual's emotional reactivity-the ca-
pacityto perceive and react to potentiallyan-
xiogenic situations-is oftenhypothesizedto
be an intervening variablemodulating a large
range of fundamentalbehaviors arising from
major life-challengingcircumstances. For ex-
ample, studiesin laboratoryrodentsrelatedif-
ferencesin reactionsto threateningeventsbe-
tweenvirginand pregnantor lactatingfemales
to the capacity to demonstrate maternal be-
havior (Hard and Hansen, 1985; Ferreira et
al., 1989; Maestripieri and D'Amato, 1991).
Fleming and Luebke (1981) suggested that
emotional reactivityprevents virgin females
frombehaving maternally. Moreover, inter-
individualvariabilityin behaviormay be partly
related to differencesin emotional reactions
among individuals. In mice, forexample, fe-
males obtaining higher scores for maternal
defensein protectingoffspring against conspe-
cificswere less reactivein a previous stressful
testregardlessofreproductivestage (Maestri-
pieri and D'Amato, 1991). Such characteris-
tic patternsof reactivitycould be used to pre-
dict adaptive responses to a varietyof major
life-challengingcircumstances.
In the past, the concepts of fear and fear-
fulnesswere a focusofintenseinterestin com-
parativepsychology.These concepts,however,
were vague and lacked universally accepted
definition.With theriseofbehaviorism,these
concepts, as well as those of emotions in ani-
mals in general, were criticized as being too
anthropocentric(e.g., Skinner, 1953). Con-
sequently, it became more common to speak
descriptivelyof escape and avoidance behav-
ior, withoutany assumptions about underly-
ing unitary states or traits(e.g., Anisman et
al., 1978). This reductionisticbehaviorismhas
VOLUME 70
erated, by an infusionof biological concepts
and rapid scientificdevelopment in the areas
of behavioral ecology and neuroendocrinol-
ogy. A reexamination of the validity of the
conceptsoffearand fearfulnessis a goal ofthis
article. In particular,a more global relevance
mightbe demonstratedon the basis of com-
monalitiesin physiologicaland behavioral re-
sponses to dangers among and withinspecies,
forthere is evidence that genetics and devel-
opmental experience subserve individual dif-
ferencesin such responsivenessin predictable
ways.
According to Gray (1987), the studyoffear
involves two importantconcepts of psychol-
ogy: motivation and personality.Fear and anxiety
have often been considered motivators and
are defined here as emotional states that are
induced by the perception of any actual dan-
ger (fear state) or potential danger (anxiety
state) thatthreatensthe well-beingoftheindi-
vidual, and which are characterizedas a feel-
ing ofinsecurity.Fearfulness is consideredhere
as a personalityor temperamenttraitdefining
the general susceptibilityof an individual to
reactto a varietyofpotentiallythreateningsit-
uations.
The Darwinian mainstream of behavioral
ecology, based on the concept ofevolutionary
adaptations, points out that fear has definite
survivalvalue in wild animals. The lifeexpec-
tancy of an animal is obviously increased if
it can reactto avoid sources ofdanger. Defen-
sive reactionsincrease the chances of individ-
ual survival (by fightor flight,forinstance).
In nature, the most importantthreatsof in-
jury that an individual encounters during its
lifetimecome frompredators and competing
or attackingconspecifics.There has been con-
siderableinterestin recentdecades in theevolu-
tionofantipredatorand competitionstrategies.
These strategiesare regarded as the product
of strongselectionpressuresbecause inappro-
priate defensivebehaviors generallyproduce
rapid and disastrous consequences (Blanch-
ard and Blanchard, 1990). Studies in natural
environmentsprovide substantialinformation
regarding the social functionof fear and de-
fensive strategies.
An importantpart of the research on fear
expressions as social signals is based on the
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS
studyof alarm calls. Animals of various spe-
cies vocalize whentheydetectpredators:mam-
mals likevervetmonkeys,Cercopithecus aethiops
(Seyfarthet al., 1980) and California ground
squirrels, Spermophilus beecheyl
(Leger et al.,
1980), and birds like black-billed magpies,
Pica pica hudsonia(Stone and Trost, 1991) and
domestic fowl,Gallusdomesticus (Gyger et al.,
1987). Alarm calls may be defined as signals
thatcommunicatepossibilitiesofdangerto con-
specifics.For example, in free-rangingvervet
monkeys,flightresponses to recorded alarms
are identical to those induced by the presence
of predators (Seyfarthet al., 1980). Animals
are able to vary call structurein a graded fash-
ion to communicate informationabout spe-
cific predator context to other conspecifics,
as was shown in magpies (Stone and Trost,
1991). Such predator-evokedcalls serveto rep-
resent the type of predator encountered and
help to coordinatean effective and appropriate
response.By examiningthe reactionsto alarm
calls,Seyfarthand his coworkers(1980) showed
that distincttypes of alarm calls emitted by
vervet monkeys are associated with distinct
sets of responses fromconspecifics,responses
whichappear to be adaptive strategiesforcop-
ing withthehuntingbehavior ofthepredators
involved. In response to the recorded alarm
calls of an individual exposed to a leopard,
monkeysrun up into treeswhere theyappear
to be safestfromthe ambush styleof typical
attack of terrestrialpredators. The audition
of calls emittedfollowingthe detection of an
eagle causes them to look up and run into
cover, apparentlyto avoid an aerial predator's
stoop. Some acts relatedto fearmay therefore
be regardedas a means to communicatepossi-
bilities of danger to conspecifics,and conse-
quently to influencetheir behavior.
Natural predatorsare largelyabsent in cap-
tivity,and it could be argued that reduced
fearfulnessis a rnajorconcomitantofdomesti-
cation (Price, 1984). Populations of farmani-
mals in range environments,however, may
stillexperience severe predation by wild ani-
mals or dogs (Sheltonand Wade, 1979). More-
over, modern farming practice can impose
severaldeviationsfromwhatmightbe regarded
as the natural situation: A kind of artificial
predation is practiced by humans, especially
in intensivehousing, where most antipreda-
167
tor behavior is directed against environmen-
tal changes and against people. For instance,
in large mammals, the detectionof a person
who remains at a considerable distance from
the animal may elicitno response. Closer ap-
proach, however, which is oftennecessaryon
farms, often elicits a violent defensive reac-
tion (Seabrook, 1972). In poultry,tonic im-
mobility,characterizedby a reduced respon-
sivenessinduced by physicalrestraint(as when
a human grabs a chicken), appears to be a
defensivereactionagainst potentialpredators
because it simulatesa predatoryepisode (Mc-
Farland, 1987). In spiteof theircaptivitythen,
domesticanimals can express emotional reac-
tivitysimilarto thatoffree-livingpopulations
of wild animals. Fear and anxietyare gener-
ally considered to be undesirable emotional
states that may reduce welfare, growthand
reproductiveperformancein laboratory,zoo
and farm animals. In poultry,for instance,
reactions such as panic or violent escape are
often inappropriate in an intensive farming
system,and the induction of a chronic state
ofanxietyor stressmay cause damage to indi-
vidual organismsand adverselyaffectmilkor
egg production,growthrate, or disease resis-
tance (Craig and Adams, 1984; Jones, 1989;
Mills and Faure, 1990). Thus, the develop-
ment of studies aimed at reducing fear and
defensivebehavior in animals reared in cap-
tivitycould be ofeconomic and ethical signifi-
cance.
The purpose of this articleis firstto exam-
ine the statusof fear and anxietyin the study
of animal life and then to develop the rele-
vance ofthe conceptoffearfulnessin the anal-
ysis of mechanisms underlyinginterindivid-
ual variabilityin adaptive processes. Animal
fear can be assessed only if the fear-eliciting
stimuliand the magnitude ofthe correspond-
ing psychobiologicalresponsesare objectively
taken into account. This article,therefore,re-
views the natureofthe frightening stimuliand
the correspondingbehavioral responses and
neuroendocrine processes. Aftera brief de-
scriptionofthevarious experimentalmethods
and situations,theconsistencyamong indica-
torsofemotional reactivityis discussed. Inter-
individual variabilityin reactionsto challenge
is exploredin lightof theconceptof fearfulness
as a basic personalitytrait that is subject to
168 THE QUARTERLY REVIEW OF BIOLOGY
several geneticand epigeneticfactors.Finally,
I consider the possibilityof temperamentas-
sessment in predictingadaptive responses to
variousenvironmentalchallengesand vulnera-
diseases and pathologies.
bilityto stress-induced
IDENTIFICATION OF FEAR
NATURE OF FRIGHTENING STIMULI
Some years ago, Miller (1959) assertedthat
most stimulithat generatenegative emotions
acquire thispower as a resultof classical con-
ditioning. But there are substantial observa-
tions on a large range of eventsthat are capa-
ble of causing fear that is not conditioned.
Gray (1979) classifiesfear-producingstimuli
into fivesubdivisions. One consistsofdangers
thatare part ofthe evolutionaryhistoryofthe
species, a second refersto novelty, a third
resultsfromlearning, a fourthis the intensity
of stimuli, and the fiftharises from interac-
tions with conspecifics.
Animalsexhibitnegativeemotionalresponses
towards specificstimulithat typicallyrelate to
persistentdangers in the ecology of the spe-
cies. They may relateto physicaldangers such
as fear of heights,as is found in many mam-
mals, fearofdarkness,as in vision-dependent
species like humans, or fear of dead bodies
thatmay transmitdisease or indicate thepres-
ence of danger. Fear of potential predators
has led to antipredatorstrategies,which are
based mainly on associations between certain
featuresin theanimal'senvironmentand adap-
tivestrategiesforcoping. For example, as men-
tioned above, vervetmonkeysgive alarm calls
withdifferent acoustical featuresaccording to
the type of predator, eitherterrestrialpreda-
torssuch as leopards or snakes, or aerial pred-
ators such as eagles (Seyfarthet al., 1980).
Exposure of an animal to noveltyis one of
themostpotentexperimentalconditionslead-
ing to a negative emotional response. The re-
sulting behavioral arousal is similar to that
induced by a nociceptive stimulationsuch as
electricfootshock(Dantzerand Mormede,1983).
Novelty can be classified as a collative vari-
able because the recognitionof any stimulus
situation as being novel requires a compari-
son with events that have been experienced
in thepast. Faure (1979) observed thatbehav-
ioral reactions decrease with repeated expo-
sure to a previously novel environment.
VOLUME 70
A stimulus can elicit fear by being associ-
ated withotherthreateningevents as a result
of conditionedprocessesoflearning.
Learning plays
a role in emotional reactions by identifying
new sources of danger. Boissy (1990) condi-
tioned heifersto be frightenedby a visual ob-
ject, initially nonaversive, by associating it
with an electrical shock.
Animals may be frightenedby a stimulus
because of thephysicalcharacteristics of its pre-
sentation, such as its movement, intensity,
duration,suddenness,or proximity.According
to Russel (1979), thesestimuliare not species-
specificbut ratherare associated withthecon-
textof predation. For instance, a flyinghawk
leads more easily to a flightresponse in black-
billed magpies than the same predatorthatis
perched and not moving (Buitron, 1983). By
using video playback images to manipulate
the salientfeaturesofthepredator,Evans and
Marler (1992) showed thatthe velocityof the
predatorand thedistancefromthepredatorto
the chickenare criticalwithregardto eliciting
alarm calls in the prey.
Finally, and as already mentioned in the
introductoryparagraphs, signalsarisingfrom
interactions
withconspecifics can also induce re-
sponses related to negative emotions. These
triggeringsocial signals representparticular
cases of the previous types of fear-producing
stimuli. They may be characterized by nov-
elty: Contact with a foreignindividual may
provokea flightresponsein heifers(Bouissou,
1985). They may be innate, as in the case of
a few alarm signals: Exposure of chicks to
alarm calls recordedfromconspecificsexposed
to a predatormake them peep and run away,
whetheror not theyhave previouslyencoun-
tered a predator(Duncan and Filshie, 1979).
These signals may be acquired, as seen typi-
callyin most antipredatorstrategiesand dom-
inance hierarchiesoccurringwithinthe social
group. Learning from conspecifics, that is,
social learning, to avoid futuredangerous en-
counters with putative predators, has been
reportedin birds (Curio, 1988) and primates
(Mineka and Cook, 1988). In vervetmonkeys,
forinstance,while infantscan distinguishbe-
tweenrelativelygeneralpredatorclasses, with
increased age theysharpentheassociation be-
tween the predator species and the type of
alarm calls (Seyfarthet al., 1980). Responses
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS 169

of low-rankingheifersto threatsfromdomi- activityin whichtheanimal is engaged may be

nant conspecificsalso reflectthis process, al- enhanced: The administrationofweak electric
thoughthe role of social learning in domestic shocks to a rat leads to an increase in food
animals is open to question (Bouissou, 1985). intake. But when fearis intense,behavior can
In highlygregariousspecies, such as domestic be disturbedor totallyinhibited:Regular nox-
fowl,theinterruption ious stimulican inhibitaggressiveinteractions
of social contactis stress-
fulsince the social motivationofthe individu- between rats (Archer, 1976c). Intermediate
als is a potentfactorin learning (Mills et al.,degrees of fear usually lead to a conflictbe-
1993). tween the expression of fear and the activity
An adaptive response to real or potential in which the individual is engaged (feeding,
danger comprisestwo complementaryfacets: sexual, aggressive, exploratory). For exam-
psychobehavioralchanges thatneutralize the ple, File (1980) showed that modulation of
effectsofthetriggeringstimulusand neuroen- anxietyby pharmacological manipulation in-
docrineadjustmentsneeded to maintaininter- duces changes in the amount of social interac-
nal homeostasis.In animals, emotionalstates, tion. Conflict between an intense emotional
such as fear or anxiety, can be indirectlyin- stateand a positivemotivationmay resultin a
ferredonly fromthese observable and mea- displacementactivity.Dantzer and Mormede
surable phenomena. (198 lb) observed thathungrypigs developed
a compulsive behavior (nibbling of a chain)
FEAR-RELATED BEHAVIORAL PARAMETERS when feedwas associated witha painfulstim-
Behavioralresponsesto aversiveeventsvary ulation (conflictsituation). Conflictbetween
greatlydepending on whetherthethreatstim- motivationsmay also provoke an intermedi-
ate activitycharacterized by the alternation
ulus is present (fear state) or only potential
of two typesof behaviors, as, forinstance, in
(anxiety state). The behavioral patternscan
some aggressive or sexual displays.
even be contradictory:Active defense(attack,
threat)or active avoidance (flight,hiding, es- FEAR-RELATED BIOLOGICAL MARKERS
cape) and immobilityor movementinhibition
can all be viewed as expressing a fear state. There are obviouslymany diversepotential
Two types of motor inhibitionmay be ob- biological correlates of emotional reactivity
served. "Freezing" is of shortduration and is and associated behavioral explanations. This
to
usually accompanied by signs of activationof article is purposely restricted neuroendo-
the vegetative system,such as an increase in crine correlates and does not deal with all of
the complex mechanisms ofthecentralnervous
pulse rate (Archer, 1976b). "Tonic immobil-
ity,"which is mainly observed in response to systemthat are involved in emotional states,
manual restraint(Gallup, 1977), is longer and such as neural circuits,neuromodulators,and
not accompanied by physiologicalevents that neurotransmitters, whichare reviewedby sev-
are controlledby the autonomic nervous sys- eral authors (e.g., LeDoux, 1990; Holstege,
is now extensive literatureon
tem. Tonic immobilityhas been successfully 1992). There
the neuroendocrine changes that accompany
used as an index of fear in chickens (Jones,
1984). exposure to environmental challenges. The
is
Other responses considered as fear indica- purpose here to attemptto show that vari-
tors include expressive movements(piloerec- ous physiologicalsystemscan respond specifi-
tion, facial expressions), vocalizations, and cally to psychologicalconditions,and thatthe
the productionof smells(pheromones). Some neuroendocrinestateaffectsthe behavioral re-
of these responses, such as the alarm calls, actions to danger.
are a means ofcommunicationin social envi-
Neuroendocrine SystemsInvolvedin
ronments.
EmotionalReactivity
Fear-producingstimulimay also affectother
patternsof behavior. Archer (1979) observed SympatheticAdrenal MedullarSystemand
that the effectsvary and depend on the emo- Hypothalamo-Pituitary-AdrenalAxis
tional intensityof the response to a threaten- Traditionally the sympatheticadrenal me-
ing event. When the level of fear is low, the dullar systemand thehypothalamo-pituitary-
170 THE QUARTERLY REVIEW OF BIOLOGY
adrenocortical (HPA) axis are viewed as the
major systemsthatare highlysensitiveto en-
vironmental challenges. Claude Bernard, in
thelast century,was the firstto recognize that
the relativeconstancyofthe internalenviron-
ment is importantto the functionalintegrity
of the organism. Cannon (1935) noticed that
emotional reactions, such as fear and rage,
pose a threatto the integrityof the body. In
theemergencyconcept,Cannon describedhow
emotional reactions are characterizedin par-
ticular by the release of adrenal medullary
catecholamines. Besides the adrenal activa-
tion, emotional disturbances also elicit a re-
lease of catecholamines both of sympathetic
origin(Dodd and Role, 1991) and froma dense
neuronal networkin subcortical areas in the
brain (Le Moal and Simon, 1991). These re-
actions require immediate physiological ad-
justmentsformaintaininghomeostasis,mostly
via energymetabolismand cardiovascularad-
aptations that allow a rapid redistributionof
blood and energytowardmusclesand thebrain.
The cardiovascularand metabolicadjustments
have survival value in preparingthe body for
an active response to acute threat, such as
"fightor flight"(Kuchel, 1991). The measure-
mentofcirculatingcatecholaminesis extremely
difficult due to theirlow concentrations,short
duration of half-life,and high sensitivityto
foreignevents. Thus, the activationofthe au-
tonomicnervoussystemhas usuallybeen indi-
rectlyevaluated by theeffecton certainvegeta-
tivefunctions,suchas defecationfrequencyand
changes in cutaneous resistance, or on some
cardiovascular measure, such as heart rate or
blood pressure.
Since Selye (1936), numerous studies have
demonstratedthata varietyofpsychophysical
events cause release of adrenocorticotrophic
hormone (ACTH) fromthe pituitary,which
in turnactivates the adrenal cortex to release
glucocorticoid,which facilitatesenergyavail-
abilityover prolongedperiods. The conceptof
stresswas proposed to characterizethe arousal
of the HPA axis and was firstdefined as "a
non-specificresponse of the body to any de-
mand made upon it" (Selye, 1950). It took a
long time before it was recognized that the
profileof the activation of the HPA axis may
vary depending on the nature of the stressor
(Mason, 1971).
VOLUME 70
In spiteofmany differencesin theirspecific
effects,glucocorticoidsact in combinationwith
adrenal catecholamines to enable the organ-
ism to engage in rapid behavioral action by
mobilizing available resources. They inhibit
glucose uptake and fattyacid storage or pro-
tein synthesisat storage sites, and stimulate
the release of energy substratessuch as glu-
cose, amino acids, and freefattyacids (Mor-
mede, 1991). It has been demonstratedthat
thereare numerous interactionsbetween the
neurochemicalcontrolsofthesetwomajor neu-
roendocrine systems (Axelrod and Reisine,
1984; Plotskyet al., 1989). In addition, since
the discoveryof serotoninin the centralner-
vous system,there have been extensive data
supportingthenotionthatthereare close rela-
tionshipsbetweencentralserotonergicsystems
and the sympatheticnervous system or the
pituitary-adrenalaxis (Chaouloff, 1993).
Other
Neuroendocrine
Systems
Although this article focusesessentiallyon
the two major neuroendocrine systemslead-
ing to the ACTH-glucocorticoid and adrenal
catecholamine secretions, there is now evi-
dence indicatingthat numerous otherneuro-
endocrine systemsare altered under stressful
conditions,involvinggonadal steroids,a large
group of hypothalarno-pituitary neuropeptides
[prolactin,corticotropinreleasingfactor(CRF),
oxytocin,vasopressin], and another group of
peptides localized in brain, pituitaryand ad-
renal medulla (13-endorphins,enkephalins).
Many studies have shown that there are
differencesin fearand defensivereactionsbe-
tween the sexes. In response to challenges,
female rodents generally exhibit a lower be-
havioralreactivitythando males (Gray, 1987).
The same pattern has been observed in do-
mesticfowl(Jones, 1987b). Likewise, in dogs
and sheep, males are more reluctantthan fe-
males to approach and make physical contact
with a human or a novel object (Lore and
Eisenberg, 1986; Vandenheede and Bouissou,
1993a, respectively). This interpretationof
the emotional levels of males and femaleshas
been severelycriticizedbecause thereare many
physiologicaldifferences, such as body weight
or foodintake,thatcould accountforsex differ-
encesin testsofanxiety(Archer,1975;Johnston
and File, 1991). Studies in domesticungulates,
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS 171

however, presentevidence forimplicationsof to pain. Central 1-endorphins, which share

gonadal steroidsin fear-relatedreactions. Fe- a precursorwithACTH (the pro-opiomelan-
males treatedwithtestosteronepropionateex- ocortin),are released simultaneouslywiththis
hibitedlowerfearreactionsthantheiruntreated neuropeptide in response to stressfulevents
counterpartsin cattle (Boissy and Bouissou, (Guillemin et al., 1977). There is substantial
1994) and sheep (Vandenheede and Bouis- evidence that exposure to aversive events can
sou, 1993b). produce a reduction in pain reactivitymedi-
It is well establishedthatprolactinsecretion ated by theopioid system.For example, when
by the anteriorpituitaryis also increased fol- returnedto an environmentpreviouslyasso-
lowing a variety of challenges. The plasma ciated withelectricshock, ratsexhibita loss of
levels of prolactin rose in rats subjected to the pain sensitivity;this autoanalgesic effect
electricshock(MormZede,Dantzer, Montpied, disappears afterthe injection of naloxone, an
Bluthe, Laplante, and Le Moal, 1984) and in antagonistof opioid receptors(Fanselow, 1984).
sheep testedduringa period of social isolation In the same way, rats exposed to a novel envi-
(Parrot and Thornton, 1989). In addition, ronmentalso develop analgesia (Netto et al.,
changes in the plasma levels of prolactin are 1987), which is suppressed by the injection
linked to adrenal responses to aggression. In of naltrexone, another antagonist of opioid
thelactatingfemalerat,whichhas highplasma receptors(Siegfried et al., 1987). Moreover,
levels of prolactin,the pituitary-adrenocortical the administrationof an anxiolyticbeforeex-
reactivityis lower in an open-fieldtest (Stem posure to threateningevents reduces not only
and Levine, 1974; Hard and Hansen, 1985). the length of freezingbut also the length of
The rise in prolactin levels is even positively analgesia (Fanselow and Helmstetter,1988).
correlatedwith the increase in corticosteroid Ecologically relevant stimuli associated with
concentrationin rats placed in an open-field social aggressionand predationhave also been
test (Seggie and Brown, 1975). The plasma shownto activateendogenous antinociceptive
level of prolactin, however, is not always af- opioid mechanisms (Kavaliers and Colwell,
fectedby threateningevents. In primates,the 1991). Endogenous opioids seem to reduce
behavior oflower-rankingindividuals, which the experienced intensityof noxious stimula-
is very differentfrom that of dominant ani- tion and therebyrender the animal less re-
mals, does not seem to be related to an in- sponsive to the challenge. Evidence that opi-
creased prolactin level (talapoin, Miopithecus ate peptides can enterthe brain (Kastin et al.,
talapoin:Eberhartet al., 1983; marmoset, Cal- 1991) confirmsthe influenceof the peripher-
lithrixjacchusjacchus: Abbott et al., 1981). ally released opiates on the activityofthe cen-
Some otherpeptides also seem to be closely tral nervous system.
relatedtotheneuroendocrineresponsesofemo- According to these data, the brain appears
tional reactivity.Corticotophin-releasingfac- to be the most importanttargetorgan forhor-
tor (CRF), released into the hypothalamic- mones released in challenging situations,
pituitaryportal vessels, is the main regulator although peripheral sites, such as the neuro-
of adrenocorticotropinsecretionby the pitu- muscular and cardiovascular systems,are im-
itarygland (Dunn and Berridge, 1990). CRF, portanttargetsof the adrenal corticosteroids
centralvasopressin, and oxytocinregulatethe and catecholamines,whichstimulatetheadap-
sympathetic nervous system and stimulate tiveresponsesthatincrease immediate energy
ACTH release eitherdirectlyor by modulat- availability forthe brain and muscles.
ing theeffectsofneuropeptides(Gibbs, 1986).
The influenceof these neuropeptides on the Modulationof the Neuroendocrine
peripheralendocrineresponsesto environmen- PatternofReactivity
tal challenges, however, is complex (Ivanyi The magnitude of neuroendocrine arousal
et al., 1991). depends not only on the physical properties
The endogenous ligands of opioid recep- ofthetriggerstimulilike electricshock or heat
tors,the 13-endorphins and enkephalins,have but also on psychologicalfactors.Psychologi-
aroused considerable interestin the study of cal discomfort,which may resultfromuncer-
emotions because of theirrole in the reaction tainty,conflict,frustration,or a high degree
172 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 70

ofnovelty,is responsibleforHPA axis activa- Rats thathave the opportunityto controldis-

tion(Hennessy and Levine, 1979). For exam- play a more moderateblood pressureresponse
ple, exposure to a novel environmentleads to challenge than rats withoutcontrol(Buch-
to increases in the plasma levels of corticoste- holz et al., 1981).
roids in the mouse (Hennessy and Levine, The predictabilityof an aggressive act may
1978) and the squirrelmonkey,Saimirisciureus also reduce its impact. When uncontrollable
(Coe et al., 1982). Catecholamines are re- electricshocksare combined witha briefstim-
leased in situationsthatrequire attentionand ulus followingshocktermination(i.e., a feed-
vigilance. For example, rats placed in a cage back stimulus),rats show no more fearin this
where theyhad been previously subjected to contextthanthoseexposedto controllableshock
electricshock exhibithigher plasma levels of (Mineka et al., 1984). Repeated exposure to
catecholamines than do naive rats (McCarty noveltyprovokes a lower activationof the pi-
and Kopin, 1978a). tuitary adrenal axis only if the exposure is
There is evidence indicatingthatthedegree regular, that is, according to a predictable
of control that an animal can exert over its pattern(expectancy), in both rats (Muir and
threateningenvironmentby suitable behav- Pfister,1987) and mice (Shanks et al., 1990).
may also determine Henry(1980) representsthedifferences
ior, that is, controllability, in neu-
the pattern of neuroendocrine arousal. This roendocrine patterns schematicallyaccording
was demonstratedby the fundamentalwork to the subject's possibility of controllingor
of Weiss (1972), who used two rats yoked to- predictingthe threateningevent. He suggests
getherby shockelectrodesattachedto thesame thatthemedullosympatheticsystemwould be
source. One rat could interruptthe electric predominant as long as the organism is chal-
shock (ability to control) and the other could lenged in its controlof the environment.By
not (no ability to control), but both subjects contrast,the loss of controlor the perception
received the same quantity of electric shock of failureto meet expectations would lead to
as a result of the yoking. The rat that con- a preferentialactivation of the HPA axis.
trolledthe stimulationexhibiteda lower pitu- There is ample evidence, therefore,to indi-
itary-adrenalarousal compared to yoked sub- cate that the biological response to a threatis
jects that had no such possibility of action. not stereotypedbut is influencedby psycholog-
Since then, some other studies have shown ical factorsand by behavioral strategiesthat
that the extentto which the animal perceives have a direct impact on the threat.
the danger as under its controlis of the great- Influenceofthe NeuroendocrineState
est importance in determiningthe intensity on EmotionalReactivity
of the emotion experienced. The increase in
While the neuroendocrine responseto threat-
plasma levels of corticosteroneobserved in
ening events is modulated by the possibility
rats (Barnett and Cowan, 1976) and in mice
ofbehavioral action, theneuroendocrinestate
(Misslin and Cigrang,1986) exposed to a novel
that results froman interactionbetween the
environmentceases once the animals have free
availability of hormones and the functional
access to theirfamiliarenvironment.The be-
propertiesof theirreceptors,both in the pe-
havioral action of the subject does not even
ripheryand the brain, may affectthe way in
need to be related to the aggression to be effi- whichindividuals react to aversive situations.
cient: Chewing a nonedible object reduces the Indeed,by bindingto receptorspresentthrough-
adrenal activation in mice exposed to a novel out the brain, glucocorticoidsexert negative
environment(M. B. Hennessyand Foy, 1987), effectson theirown secretionand also act on
The possibility of moving, however, corre- otherfear-activatedneural circuits(Bohus et
sponds generallyto an active behavioral strat- al., 1987). Such influencesoccur by at least
egy of coping, which leads to a decrease of two mechanisms: a basic hormonal effectand
the HPA axis arousal consecutiveto theexpo- a retroactivehormonaleffect,as demonstrated
sureto a threateningsituation(Dantzer, 1986). through methods of adrenalectomy and ad-
The sympatheticadrenal medullarysystemis ministrationof exogenous glucocorticoid to
also highlyinfluencedby the animal's ability intactanimals (Leshner, 1979). When an aver-
to control the occurrence of aversive events. sive event occurs, the basal hormonal levels
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS
(basiceffect)
may affectthebehavioral response
by "preparing" the central nervous system.
For example, the duration of tonic immobil-
ity, considered as a specific fear-relatedre-
sponse in restrainedhens, is prolonged after
thebasal plasma level of corticosteroneis arti-
ficiallyincreased by a corticosteroneinfusion
at physiologicaldoses (Joneset al., 1988). And
adrenalectomy in rats decreases novelty-in-
duced locomotion(Veldhuis et al., 1982). The
glucocorticoidresponse to a threateningsitu-
ation in turnhas an effecton the centralner-
vous system (retroactive effect)
and modulates
the development of the behavioral response.
Mice exposed to trained attackers fightless
and exhibitsubmissivebehavior more rapidly
when injected withACTH just beforethe en-
counter (Leshner and Politch, 1979). This is
due to release of corticosteroidsin response
to ACTH injection (excitabilityof the gluco-
corticoidreceptors), since the behavior is not
observed in adrenalectomized animals whose
plasma corticosteronelevels are kept constant
by corticosteroneinfusion.
All of these observations suggest that the
neuroendocrine state of the brain may be the
ultimate mechanism for the organization of
emotional responses. Moreover, autonomic
and neuroendocrine patternsgive additional
informationabout the emotional state of the
animal.
At this level of the analysis, attentionhas
to focus on the fact that the identificationof
fear-inducingstimulidepends on the type of
responsestheyproduce. By contrast,thesere-
sponses, labeled as fear-relatedacts, depend
on the type of stimuli inducing them. Fear-
producing stimuliand fear-relatedresponses
are thusinextricably bound. Accordingto Hinde
(1985), an emotional state cannot be consid-
ered to be independent of the factorsthat in-
duce itnor oftheresponsesexpressingit. These
psychobiologicalresponsesare not stereotyped.
A major determinantoftheemotionalresponse
may be regarded as theresultofan interaction
between (1) the propertiesof the threatening
event, (2) the possibilitiesthat are offeredby
the environmentto the individual to control
the danger, thatis, cognitiveperception,and
(3) theneuroendocrinestateoftheindividual.
The most efficientapproach to the identifica-
tion of a fear or anxiety state in the animal
is to consider these aspects interactively.
173
STUDY OF FEAR-RELATED RESPONSES: THE
ASSESSMENT OF INTERINDIVIDUAL
DIFFERENCES
VARIOUS METHODS FOR STUDYING FEAR
Many kinds of laboratory situations have
been designed to studythe various behavioral
and physiologicalprocessesofemotional reac-
tivityby attemptingto mimic conditions en-
counteredby animalsin naturalhabitats.These
experimentaltestsfacilitatecomparisonofpsy-
chobiological reactivityamong individuals in
a standardized way that is difficultto attempt
under natural conditions. It is not our intent
to review all the experimental designs that
have been used in studies of fear defensive
reactions, but to focus on those most com-
monlyused in the scientificliteratureon both
laboratory and domestic animals.
Since the classic work of Hall (1934), the
"open-field"testhas been extensivelyused in
rodents (Archer, 1973b). This experimental
situation provides a number of threatening
factorssuch as novelty,absence of shelterand
landmarks, and bright lighting. Later, this
testwas used fordomestic fowl(Faure et al.,
1983) because of its methodological facility
(easy use, rapidity,automatization,standardi-
zation, and repeatability). More recently,it
has been applied to domestic mammals and
in particularto cattle (Kilgour, 1975; Koval-
cikova and Kovalcik, 1982; Dantzer et al.,
1983; Boissy, 1990), pigs (Mormede, Dant-
zer, Bluthe, and Caritez, 1984; Taylor and
Friend, 1986), and sheep (Moberg et al., 1980;
Lachaux et al., 1983).
Some other tests also have been used to
assess neophobia. The introductionofa novel
object into the familiarenvironmentand the
opportunityto leave thehome cage to explore
unfamiliar surroundings,that is, the "emer-
gence test,"have been used in fowl (Archer,
1976a; Murphy, 1977) and rodents (Barnett
and Cowan, 1976). Reactions to novel objects
have also been studiedin heifers(Boissy, 1990),
goats (Lyons et al., 1988) and pigs (Monnede,
Dantzer, Bluthe,and Caritez, 1984; Lawrence
et al., 1991).
Hall (1941) described othermethodsforas-
sessing fear and anxietyin rodents: handling
by humans, exposureto visual or acousticfear-
producing stimuli,movementin a maze, and
administrationof inescapable electric shock.
174 THE QUARTERL Y REVIEW OF BIOLOGY
Fear has also been measured by the decrease
in socialinteractionbetweenpairsofratsplaced
in a novel enclosure(File, 1980). Most ofthese
tests were later used in fowl Uones, 1987a).
Domestic ungulates have also been exposed
to these threateningsituations. Confinement
was testedin cattle(Stephensand Toner, 1975;
Veissier et al., 1987), exposure to a stimulus
associated withan unavoidable noxious event
was studied in pigs (Dantzer and Mormede,
1980), while exposure to humans was tested
in goats(Lyons and Price, 1987), cattle(Boissy
and Bouissou, 1988), and pigs (Lawrence et
al., 1991). Presentation ofa natural predator
(dog) was used in sheep (Torres-Hernandez
and Hohenboken, 1979), and the response to
sound stimulationwas recordedin both sheep
(Ames and Arehart, 1972) and cattle (Boissy
and Le Neindre, 1990).
Another methodologywas also devised to
assess fearthatinvolvespassive avoidance con-
ditioning (avoidance of an unpleasant event
by the inhibitionofa previouslyrewarded be-
havior) and active avoidance conditioning(es-
cape fromthe unpleasant event by displaying
a particularbehavior,e. g., two-waytest)(Selig-
man, 1975). In addition to experimentswith
rodentsand fowl,theseconditioningtestshave
been used in pigs (Dantzer and Mormede,
1981a).
Many other experimental situations have
been designed.As Archer(1973b) pointedout,
however, these testsdo not take into account
thebiological significanceofthebehavior pro-
duced, and oftenhad littleor no relationto the
behavioral repertoireof the species studied.
CHARACTERIZATION OF
FEAR-RELATED RESPONSES
RelationbetweenEnvironmental
Challengeand EmotionalReactivity
In orderto assess the effectivenessof study-
ing emotional reactivityin animals, attention
has long focusedon correlations.One attempt
to achieve an objectiveevaluationofemotional
reactivityassociated with fear is to measure
response afterexperimentallyvaryingthe de-
gree of threat. The degree of threat can be
graded by changing the triggerevent from
slight disturbances, such as gentle handling
oftheanimal, to major physicaleventssuch as
restraintor electricshock, and psychological
VOLUME 70
challenges such as exposure to novelty(Kopin
et al., 1989). It also can be graded by modi-
fyingthe alarm-causing characteristicsof the
same threateningevent.
Some resultssuggestthat the response can
be reliably related to the degree of environ-
mentalchallenge. In rodentssubjectedto elec-
tric shock, behavioral responses (Natelson et
al., 1987), plasma catecholamine levels (Na-
telson et al., 1981), and HPA axis reactions
(Wiener and Levine, 1983) increase withthe
intensityof the stimulation.In a series of ex-
perimentsusing various species, it was dem-
onstratedthatifthe gradientofnoveltyvaries
withchanges in thestimuluselements,thereis
a correlatedgraded psychobiologicalresponse
according to the degree of differencefromthe
normal environmentof the organism. Faure
(1975, 1979) andJones (1977b) reportedthat
the duration of tonic immobility(i.e., reac-
tion induced by physical restraint)decreases
in chickens once the animals become accus-
tomed to the test. A similar result was ob-
tained in the same species when familiarob-
jectswereintroduced intothepen Uones, 1977a).
The increase in the level ofnoveltyin the pen
increases the defecationrate in rats (Ivinskis,
1970), the plasma level of corticosteroidsin
mice (M. B. Hennessy and Levine, 1978, M.
B. Hennessy and Foy, 1987) and rats (Arm-
ario et al., 1986), the duration of freezing
in chicks Uones and Faure, 1982), and the
frequencyofmovementsin calves(Dellmeier et
al., 1985). Likewise, exposure to increasingly
unfamiliarsurroundingsincreases the ambu-
lation rate in sows (L. Taylor and Friend,
1986) and calves (Dellmeier et al., 1985), in
which the level of plasma cortisol also rose
(Dantzer et al., 1983). However, correlations
are not always found between the level of the
disturbanceand subsequentreactions.For ex-
ample, the adrenal response of rats subjected
to electricshock is not systematicallyrelated
to the intensityof the stimulus (Natelson et
al., 1981, 1987).
Differences
Assessmentof Interindividual
variationin thebehav-
A greatinterindividual
ioral and neuroendocrinereactivityto threat-
eningchallengeshas oftenbeen described.The
importance of this individual reactivityhas
led to examination of whether:(1) the behav-
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS 175

ioralpatternscould be linkedto particularneu- rate Uones et al. , 1981). For confinedrabbits,

roendocrine traits,(2) the scores obtained in tonic immobilityis longer when the plasma
differentenvironmental challenges correlate levels of corticosteroneare high (Carli et al.,
withinindividuals, and (3) thepsychobiologi- 1979).
cal responses to an alarming event are consis- Behavioral reactivityand endocrine char-
tent over time. acteristics are not always related, however.
The negative correlationbetween defecation
between
Relations BehavioralReactivity and ambulation in rodents subjected to an
andNeuroendocrine Traits open-fieldtestis sometimesnonsignificant (Har-
The significanceofinterrelationships is stud- rington, 1972; Ley, 1975; Misslin et al., 1976).
ied from behavioral and endocrine parame- And the magnitude of fear-relatedbehaviors
tersrecorded during the same environmental cannot be systematicallylinked to physiologi-
challenge. Abundant evidence shows thatbe- cal parameters. In ratstestedin an open field,
havioralcharacteristics are linkedto differential the duration of freezingis independentof the
physiologicaland neuroendocrineresponsesto increase in heart rate (Candland et al., 1967)
threateningsituations.Defecation rate in ro- and corticosteroidplasma levels (Stern et al.,
dents, the most frequentlyused index of fear 1973; Restrepo and Armario, 1987). In re-
in open-fieldtestssincetheworkofHall (1934), sponse to an acoustic startlestimulus,Svens-
is negativelycorrelatedwithambulation(Tachi- son and coworkers(1991) reporteda dissocia-
bana, 1982; Gamallo et al., 1986; Dishman tion between behavioral and cardiovascular
et al., 1988) and positivelycorrelatedwiththe reactivityin rats. In squirrelmonkeysexposed
increase in heart rate (Candland and Nagy, to novelty, there is interindividualvariation
1969; Blizard, 1971), plasma catecholamines in the magnitude of behavioral disturbance
(McCarty and Kopin, 1978a), and the initial but no differencein adrenocorticalresponses
plasma levels of corticosterone(Gamallo et (Coe et al., 1982). The relationsbetweenhor-
al., 1986). monal and behavioral responses accompany-
Such correlationsalso existin domesticani- ing fearare not more marked in domestic un-
mals. When chickensare subjectedto an open- gulates. Behavioral response to a threatening
field test, the duration of freezing varies in event is not related to heart rate in goats (Ly-
proportion to their adrenal response Uones ons and Price, 1987) nor to plasma levels of
and Merry, 1988). In sheep testedin a novel glucocorticoidsin cows (Lefcourtet al., 1986).
environment,Lankin (1976) found a positive Most testsusing novel environmentsthatare
correlationbetween the ambulation rate and performedon pigs (Dantzer and Mormede,
the subsequent increase in the plasma level 198lb), sheep (Moberg and Wood, 1982), and
ofcortisol.In Chinese pigs exposed to a novel calves (Arave et al., 1980; Dantzer et al., 1983)
environment,a high behavioral reactivityis have shown a dissociationbetweenlocomotor
negatively correlated with low plasma levels reactivityand activationof the pituitary-adre-
of ACTH and adrenaline (Mormede, Dan- nal axis. Furthermore,the differentphysio-
tzer, Bluthe, and Caritez, 1984). In the other logical indices seldom show high intercorrela-
experimentalchallenges, several correlations tions (Lacey, 1967).
between behavioral and physiological values
are also reported as significant.In rats ex- RelationsbetweenResponsesto DifferentChallenges
posed to electric shock, for example, the in- The interestin individual differenceshas
crease in behavioral reaction depends closely led researchersto ask whetherindividuals are
on the rise in the plasma levels of circulating consistentin theirresponses to differentchal-
catecholamines(McCarty and Kopin, 1978b). lenges, and many studies indicate that they
Exposure to an unexpected acoustic stimula- are. Brush and coworkers(1985) reportedthat
tionproduces an inverserelationshipbetween ratsexhibitinglow performanceduringactive
the amplitude of the behavioral reaction and avoidance conditioninghave a higherdefeca-
the increase of corticosteronelevels (Glowa tion rate in a novel environment.The defeca-
et al., 1992). Behavioral reactionsofhens ex- tion rates of rats in conditioned feartestsand
posed to humans are correlated with heart open-fieldtestsare positivelycorrelated(Ley,
176 THE QUARTERL Y RE VIEW OF BIOLOGY VOLUME 70

1975). Correlationsare foundamongseveral pa- tionalityto describe the behavioral reactions

rametersmeasured in open-field,emergence,
and tonic immobilitytestsand in response to
a frighteningstimulus in chicks Jones and
Mills, 1983), hens Uones, 1987c, 1988), and
Japanese quails, Coturnixcoturnixjaponica(Mills
and Faure, 1986). Good correlationsamong
responses to a fewkinds offrighteningstimuli
have also been obtained in hens (Craig et al.,
1983), dogs (Goddard and Beilharz, 1984), and
cattle(Boissy, 1990).
A limitednumber ofstudiesshow thatthere
is no strikingcorrelation among the values
recorded in various experimental challenges.
In rats (Overstreet et al., 1992) and in chick-
ens (Archer,1976a), behavioralreactionsmea-
sured in the open field are not significantly
correlatedwith any parameter recorded dur-
ing the emergence test.
ofEmotional
Consistency ResponsesoverTime
Psychobiological is definedby those
reactivity
individual characteristicsthatare consistently
displayed, not only in differentsituationsbut
also over time. Measurements of flightreac-
tions in response to threateninghumans have
illuminated the issue of fear consistencyover
time because several studies in domestic ani-
mals have looked at the same individuals over
long periods. For example, Lyons and cowork-
ers (1988) found that goats, when tested at
several ages, show high stabilityin theirreac-
tivitytoward humans. In heifers,flightreac-
tion in response to a standardized approach
of a human remained fairlyconstant up to
seven months of age (Kerr and Wood-Gush,
1987), and in poultry,individuals are consis-
tent in their tonic immobilityresponse over
time(Jones,1988). Websterand Hurnick(1990)
found thatthe distressresponses measured in
chickens in an open-fieldtest at 17 weeks of
age are related to their behavioral reactivity
recorded at age 2 days.
SEARCH FOR A UNIFYING
CONCEPT OF FEARFULNESS
(mainlythereductionofactivity)and thephysi-
ological changes (higherdefecationscores,for
example) observedin a ratexposed to an open-
fieldtest.Later, thenumerouscross-testcorre-
lationsobservedamong variousfear-related re-
sponses suggested thatthese responses might
be mediatedby the same psychobiologicalpro-
cesses. Gray (1987) interpretsfearas a hypo-
theticalstateofthe brain and neuroendocrine
systemthat occurs under certain conditions
and resultsin certainformsofbehavior. Fear-
fulnessmay thus be considered an inner trait
of the individual, an intermediarybetween
perceived stimulations(or independent vari-
ables) and psychobiologicalresponses (or de-
pendentvariables)(Ivinskis,1970; Gray, 1979).
Accordingly,fearfulnessmay be definedas a
basic constitutionaltrait that determinesthe
extentto which an individual becomes fright-
ened in potentiallyalarming situations. We
can expect, therefore,that when an animal
exhibitsa high degree of emotional reactivity
in responseto one challenge, itwillmostlikely
display high reactivityin responseto another,
similar situation. With this notion of a single
scale to representemotional reactivity,it be-
comes possible to classifysubjects by the im-
portanceof certaincharacteristicresponsesto-
ward a few challenges.
Not all tests,however, support the notion
ofconsistencyin reactionsto diverse environ-
mental challenges, and some authors, in par-
ticularArcher(1973b) and Hinde (1985), have
questioned the unitaryconstructas a means
of definingfearfulness.Archer (1973b) said
that Hall (1934) used emotionalityas "a con-
venient concept for describing a complex of
factors"assumed to express sympatheticactiv-
ity.Taking thevarietyoffear-related responses
as a basis, Archer (1979) proposed a more
flexiblemodel in whichreactionsare governed
by multifactorialinfluencesratherthan by a
single, central state.
ORIGINS OF INTERLABORATORY DISCREPANCIES

IS FEARFULNESS A UNITARY TRAIT The conflictingfindingsreportedabove raise

OR A COMPLEX OF FACTORS? questions about the sources ofinterindividual
Attemptshave long been made to interpret differences in emotionalreactivity.Among the
the differencesin individual reactions to the possiblesourcesofvariationthatmay be identi-
same environmentalchallengein orderto pre- fied are variation in experimentaldesign and
dict psychobiologicalresponses to other chal- interactionbetween genetic and ontogenetic
lenges. Hall (1934) firstused the term emo- factors.
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS
Diversityof EffectsOwing to
ProceduralVariations
Thevariety ofprocedures. The varietyofmeth-
ods used in studies of fear and anxiety may
partlyexplainthediscrepanciesin results(Walsh
and Cummins, 1976). Maintenance condi-
tions could be one source of difference.Har-
rington and Blizard (1983) showed that the
resultsofopen-fieldtestsare not directlycom-
parable ifanimals are previouslymaintained
under radicallydifferent conditions.
light-cycle
Defecation scores are substantiallyhigherfor
rats maintained under a continuous 24-hour
lightdiurnal cycle than forthose maintained
in a light-darkdiurnalcycle.The physicalcon-
ditionsofthe experimentalsituationmay also
account for differencesamong studies. For
example, in rodentsthat are mainly active at
night,increasinglightintensityduring expo-
sure to an open-fieldtest increases the level
ofthreat.The changein thebrightnessgradient
is sufficientto cancel thesignificant
correlations
betweenambulation and defecationscoresob-
served when the same test is performedwith
a mean lightintensity(Tachibana, 1982). Be-
cause physicalconditions,ofbothmaintenance
and experimentation,differfrom one study
to another, theirinfluenceis all the more im-
portant. The area of the device used to test
cattle in a novel environmentmay vary be-
tween 12m2 (Canali et al., 1986) and lOOm2
(Kovalcikova and Kovalcik, 1982), and itsform
can be square (Boissy and Bouissou, 1988),
rectangular(Dellmeier et al., 1985), circular
(Warnicket al., 1977), or even T-shaped (Veis-
sier et al., 1987).
The psychophysical conditionspresentwhen
an alarming event occurs may also influence
the emotional response. Chickens exposed to
a novel environmenthave differentresponses
to the same sound stimulus, depending on
whetherthe sound is emittedby an object that
is localizable in the immediate environment
(Archer, 1976b). While fear and anxiety are
both induced by threat, they can be distin-
guished based on how the threatis presented.
The frighteningevent may be actual (fear-
state associated) or anticipated based on the
presentationof cues (anxiety-stateassociated).
Blanchardand Blanchard(1990) providedstrong
supportforsuch a distinction,indicatingthat
verydifferent behavioral patternsoccur in di-
177
rect response to a predator (avoidance and
attackreactions),as opposed to thoseoccurring
in response to olfactorycues indicating the
potential threatof a predator (approach pat-
terns).
The social context.Because it can alter the
individual's response to stressfulevents ("so-
cial buffering"),the social context is also a
potentsource ofvariation among data. A vast
amountofdata on antipredatorstrategiesshow
that alarm calls are sensitive to the caller's
social context. For example, alarm calls in
female vervet monkeys, Cercopithecus aethiops,
are potentiated by the presence of offspring
(Cheney and Seyfarth,1985). The vocal be-
havior of domestic chickensvaries according
to thenatureofthesignaler'saudience: Chick-
ens give more aerial alarm calls in response
to overhead hawk models when they are in
the presence of conspecificsthan when they
are alone (Evans and Marler, 1992). Several
laboratorystudieshave investigatedthe effect
of an audience on otheremotional behaviors.
In rats (G. T. Taylor, 1981), fowl(Jones and
Merry, 1988), and monkeys(Coe et al., 1982),
exposure to noveltyproduces less behavioral
disturbance when animals are tested with a
social partner than when they are alone. In
fact,the animal does not even need to be in-
volved in a social interactionwithitscompan-
ions forthereactivityto be reduced. In a study
withheifers,themere presence ofconspecifics
is sufficientto diminishthe threateningeffect
of an unexpected event (Boissy and Le Nein-
dre, 1990).
Inappropriateexperimentalconditions
forthespe-
ciesstudied.Testing animals in inappropriate
environments,which is likelyto resultin ab-
normal and maladaptive behavior, can also
lead to an inaccurate estimationof emotional
reactivityand explain the lack of correlations
among studies. Conditioned avoidance tests,
forinstance, have been extensivelyvalidated
as a means of assessing fear responses in ro-
dents (Gray, 1987). The same type of test,
however, does not always seem to be accurate
in evaluating fearin fowl.While a conditional
stimulusdifferentiates hens according to their
strainwhen theymust respond activelyto the
signal to avoid the aversive event (i.e., active
avoidance), the same stimulusdoes not differ-
entiatebetweentwo strainsifthe animals must
178 THE QUARTERL Y REVIEW OF BIOLOGY
refrainfrommoving to avoid the unpleasant
event (passive avoidance) (Rutter and Dun-
can, 1988). This suggeststhatfowlare distin-
guished during the active avoidance test by
theirabilityto exhibitan active response and
not, as was assumed, by the magnitude of an
absolute fear response. Moreover, it is not
well known whethertests measure the same
motivations in males and females, and the
validation of a test for one sex cannot be as-
sumed to necessarilyapply to the other(John-
ston and File, 1991).
Smallsamplesizes.Small sample sizes, which
are not suitable formost statisticalanalyses,
may also be responsible for a lack of signifi-
cant correlationsamong thedata (Gray, 1987).
Tachibana (1982) and thenJones(1987c) showed
how difficultit is to obtain statisticallysignifi-
cant resultsforas complex a phenomenon as
fear from a limited amount of data and too
small a sample.
Diversityof EffectsOwing to Preexisting
IndividualCharacteristics
Adaptive responses to environmentalchal-
lenges are affectedby preexistingcharacteris-
ticsofreactivitythatare based on interactions
between an individual's geneticbackgroundand
past environmental on developmental
influences
and learning processes.
Genetic
Background
As already mentioned,the sex ofan animal
is a major factorin interindividualvariability
in defensiveresponses.Adaptive processesare
also, to a certainextent,under geneticcontrol
(Bouchard et al., 1990; Plomin, 1990). A ge-
netic component accounting for part of the
interindividualvariabilityin reactions to hu-
mans has been foundin several domestic spe-
cies. In a studycomparing dam-reared goats
withhuman-rearedgoats, Lyons and cowork-
ers (1988) found that among pairs of twins,
a goat's rank within the dam-reared group
predictsitssibling'srank in thehuman-reared
group. A consistentheritabilityof reactivity
also has been foundby studyingdefensivere-
actions to humans in dairy cattle (Dickson
et al., 1970), pigs (Hemsworth et al., 1990),
poultry(Jones, 1986), and dogs (Goddard and
Beilharz, 1984). The influenceof geneticfac-
tors on psychobiologicaltraitsof reactivityis tion and classical conditioning,interactswith
VOLUME 70
reported even more often at the population
level than at the individual level. Large differ-
ences in the behavioral and neuroendocrine
reactionsto aversiveeventsare foundbetween
breeds or strainsof rodents(Olivero and Cas-
tellano, 1990). For instance, in mice exposed
to uncontrollablefootshock,themagnitude of
the increase in corticosteroneconcentration
and in the time required for it to returnto
basal values vary with strains(Shanks et al.,
1990). Similarly, exposure to an unexpected
acoustic stimulationelicits larger behavioral
responses in Lewis rats than in Fisher rats
(Glowa et al., 1992). Breed-dependentdiffer-
ences exist also in domestic mammals. For
example, compared with European breeds,
Chinese pigs displaya low behavioralreactivity
in responseto a novelenvironment(Mornmede,
Dantzer, Bluthe, and Cartitez, 1984).
These findingssuggest that genetic vari-
abilitymay be partlyresponsible forthe dis-
crepancies among laboratories in which sub-
jects ofdifferentgeneticoriginshave been used.
It is not surprisingto findthatvariation in the
expressionofemotional reactivityis relatedto
genetic variability. On the other hand, lim-
ited genetic variability can affectthe likeli-
hood offindingdifferences in reactivityamong
individualsofthe same population. Since lab-
oratoryand domesticanimalshave been highly
selected,theinterindividualvariabilitywithin
each strainis considerablyreduced.From seven
inbred strainsof rats tested in an open field,
Van Der Staay and his coworkers (1990) showed
thatthe variabilityamong individuals within
each strainwas clearlysmallerthanthevariabil-
ity among individuals fromdifferentstrains.
By studying correlations over strain means
(genetic correlations)where the strainsserve
the role ofindividuals, these authorsreported
strongcorrelationsbetweendifferent measures,
both withinthe open-fieldtestand across dif-
ferenttests(open-fieldand emergence tests).
Accordingly,itmay be harder to demonstrate
correlationsbetweenvalues measured in sub-
jects belonging to the same population than
those recorded from individuals of different
strains.
PastEnvironmentalInfluences
Previouslearning,characterizedby habitua-
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS
the genetic background of each individual to
modulate emotional reactivity.In poultry,for
example, repeated exposure to human beings
(i.e., habituation) or association of a food re-
ward withhuman contact (i.e., classical con-
ditioning)decreases subsequentbehavioral re-
activity(Jones, 1986; Murphy and Duncan,
1976, respectively).On the otherhand, prior
negativeexperiencecan dramaticallyincrease
emotionalreactivity. For example,chronicstress
(generallyinescapable electricshockpretreat-
ment) predisposes individuals to react more
fearfully to subsequentalarmingevents,as was
shown in fowl (Jones et al., 1988) and rats
(Tejedor del Real et al., 1991).
In addition, isolation or separation from
conspecifics,as well as repeated social stress,
such as chronicsocial defeator social instability
and subordinationrelationships,determinein-
dividual neuroendocrine reactivity(Henry,
1982). For instance,dailyrotationofratsamong
differentsocial groups, which causes social
instability,activates the sympatheticnervous
system(Mormede et al., 1990) and may dif-
ferentiallyaffectindividual reactivityto aver-
sive challenges.These social stress-related dif-
ferencesare not found only between animals
with distinct social status, that is, between
dominants or subordinates. For example, the
differencein the neuroendocrine profilesof
free-rangingolive baboons, Papio anubis, in
response to a physical threatis not so much
between dominants and subordinates as it is
between certain dominant individuals when
the hierarchy is unstable (Sapolsky, 1990):
Certain dominants exhibit a release of corti-
costeroid in response to physical threatsthat
is similarto the hormonal patternof the sub-
ordinates.
Abundant evidence is available suggesting
that increased environmentalmanipulations
in early lifeleads to marked increases in later
reactivity.Early environmentalinfluencesact
especially during sensitive periods of brain
development. For example, rats or fowlsthat
received substantial stimulation in infancy,
such as environmentalenrichmentor regular
handling,were generallyless reactivein adult-
hood (Chevins, 1990; Jones and Waddington,
1992, respectively).Early environmentalen-
richmentand handlingmay also influenceneu-
roanatomical development by increasing the
179
number ofhippocampal glucocorticoidrecep-
tors,which are implicated in both behavioral
and endocrine regulations (Renner and Ro-
senzweig, 1987; Meaney et al., 1989, respec-
tively).
The influencesofprevious experiencesand
early environmentare partly responsible for
divergentresultsbetweenstudieson emotional
reactivity.For example, the fact that Jones
(1977b) but not Archer(1973a) notes thatthe
repetitionofthe open-fieldtestincreasesloco-
motor activityin chickensmay simplybe due
to differencesin social housing methods. Un-
like the animals testedby Archer, those used
byJoneshad been rearedin a group and there-
forewere faced not only withnoveltybut also
with separation fromconspecificsduring the
test. Thus, their increased activitywith re-
peated testingmight reflectan active search
forconspecificsstimulatedby progressivere-
duction ofemotionallyinduced locomotorin-
hibition.
Differencesin developmental maturityamong
animals may affectthe reliabilityof results.It
is indeed known thatage influencesthe acute
response to alarming events, although these
effectshave not received much attention.For
example, adult deer flee danger while young
fawns adopt the characteristicfreezing pos-
ture(Espmark and Langvatn, 1979). Because
thephenotypeand environment interactthrough-
out life, one would not expect perfectconsis-
tency over long periods of time. Therefore
it is not surprising that correlations among
resultsrecorded at different ages seldom show
large coefficientsof variation. Goddard and
Beilharz (1986) foundin dogs thatthepredict-
ability of an individual's fearfulnessdimin-
ishes withtime fromthe initialmeasurement,
particularlywhen behavioral assessment be-
gins at a young age.
To summarize,discrepanciesin resultsfrom
different observationsare partlyrelatedto nu-
merous variations in procedural conditions
that tend to affectthe degree of stressfulness
ofthesituationand limitthepossibilityofdirect
comparisonsamongstudies.In addition,genetic
predispositionsand developmentalexperiences
shape individualtendenciesto be anxious, fear-
ful,or secure, and thusdifferentiate individu-
als on the basis of their reactions to adverse
environmentalchallenges. Because emotional
180 THE QUARTERL Y REVIEW OF BIOLOGY
dispositionhas so much effectupon responses
to environmentalchallenges, traditionalindi-
catorsoffearand anxietymay provide contra-
dictoryresultsifstudiesdo not properlytake it
into account. This concept of interindividual
diversityin emotional reactivityis illustrated
in programs of genetic selection.
GENETIC MODELS OF
PSYCHOBIOLOGICAL REACTIVITY
The existence of robust strain-dependent
differencesin adaptive responses to aversive
stimulationhas suggestedthatthis character-
isticcan be geneticallymanipulated. Bidirec-
tional genetic selection for a large range of
behavioral and neuroendocrinereactivityhas
been successfulin rodents(Brush, 1991). For
example, strains of mice have been selected
on the basis of their behavioral reactivityin
open-fieldtests (De Fries et al., 1978). Ge-
netic selection has been carried out in rats
according to theirbehavioral responses to en-
vironmental challenge. Roman rats, for in-
stance, were originally selected for extreme
differencesin two-wayactive avoidance per-
formance(Bignami, 1965). Maudsley ratswere
selectivelybred for differencesin open-field
defecation rate (Blizard, 1971; Broadhurst,
1975). Wild Norwayratswereselectedthrough
many generations, either for reduced or for
high aggressive reactivitywith respectto hu-
mans (Naumenko et al., 1989). Divergent
strainsof poultryhave also been successfully
developed. For instance, hens were selected
over several generationson the basis of high
or low activityin the open-field test (Faure
and Folmer, 1975), and Japanese quails were
selectivelybred forexaggeratedor reduced ad-
renocorticaland behavioralresponsesto immo-
bilizationstress(Satterleeand Johnson, 1988;
Mills and Faure, 1991, respectively).A heri-
tabilityindex of0.5 forthe reactionsofdefen-
sive dogs has led to breeding of individuals
according to theirbehavioral reactivityin re-
sponse to an environmentalchallenge (God-
dard and Beilharz, 1984, 1986).
In selectionprograms,even though strains
were selected according to one particularbe-
havioral or endocrinecharacteristicmeasured
in a particular test, there are many recent
studies reportingthat the animals also differ
in other psychobiologicaltraitsobserved in a
VOLUME 70
wide varietyofenvironmentalchallenges. For
instance, Roman rats geneticallyselected for
a low degree of active avoidance behavior ex-
hibit higher levels of corticosteroneand pro-
lactin followingexposure to an open-fieldtest
than do rats displayinghigh active avoidance
behavior (Walker et al., 1989; Castanon and
Mormede, 1994). Maudsley rats, selectedfor
theirhigh reactivityin an open field,are also
more reactivein an escape-avoidance conflict
(Commissaris et al., 1986) and spend less time
in an open arm comparedto a closedone (Over-
streetet al., 1992).
Similar resultshave been obtained in poul-
try. Hens selected over several generations
for low locomotor activityin an open field
exhibited lengthened tonic immobilityreac-
tions, marked responsivenessto startlingvi-
sual or acoustic stimuli,a longer waiting pe-
riodbeforeventuringinto an unfamiliararea,
and decreasedacceptanceofnovel food(Faure,
1981). InJapanese quails, chicksfroma strain
bred selectivelyfortheirhigh tonic immobil-
ityin response to handling by humans exhib-
ited higherreactionsof fearin open-fieldand
emergence tests Uones et al., 1991; Jones et
al., 1992). Such wide-rangingeffectssuggest
thatgeneticmanipulationmightexerta marked
effect on fearand defensivepsychobiological re-
sponses.
The association between neuroendocrine
status and behavioral responses to threaten-
ing stimuli may result from a genetic link.
Such coselection is demonstrated by recent
studies. For example, by making nonsegre-
gatingcrosses (parental lines and F1) and seg-
regating crosses (F2 and backcrosses) of the
Roman lines, Castanon and her coworkers
(1991) foundthatavoidance performanceand
prolactinreactivityare geneticallycorrelated.
Such results suggest that the behavioral and
neuroendocrine responses to environmental
challengesmay be intimatelyinterrelatedand
regulated by a common central mechanism
thatis geneticallymodulated. Rather thanbe-
ing genetically related systematically,how-
ever, thebehavioral and endocrinecharacters
ofemotionalreactivitymay insteadresultfrom
fortuitouscoselection.And selectionin defen-
sive responses may partlyexplain divergence
among the resultsreviewed above. As an ex-
ample, Hendley and her collaborators(1986)
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS
initiated a recombinant inbreeding program
to separatehypertensiveand hyperactivetraits
that are associated in the SHR strain, a line
derived fromtheWistar-Kyotorat. They pro-
duced a new strainof ratsthatwere behavior-
allyhyperreactiveto environmentalchallenge
like the original SHR strain,but withouthy-
pertension.Such psychobiogenetically selected
strains provide an extremelyuseful tool for
investigatingthe biological bases ofinterindi-
vidual differences in emotionalreactivity.This
new approach oughtto furtheran understand-
ing of how geneticfactorsinfluencebrain or-
ganization subserving individual variability,
particularlyindividual susceptibilityto being
frightened.
FEARFULNESS AS A COMPLEX INTERMEDIATE
VARIABLE IN BEHAVIOR MECHANISMS
As suggestedthroughoutthisarticle,psycho-
biologicalreactionsto emotionalchallengesare
only indicators of fear, and cannot be direct
measures ofthe emotional state. Fear mustbe
evaluated by studyingnot onlytheintensityof
a unique response but also the strategyof the
response. The different mechanisms underly-
ing fear-relatedresponses probably depend
on othermotivationalsystemsthatmay modu-
late these responses. For instance, differences
in locomotor activityrecorded in a particular
testbetween two strainsof rats are consistent
with the high or normal activity for which
the animals are selected,whereas the opposite
response is observed in another threatening
situation (Rogers et al., 1988). Therefore, it
is difficultto attribute a given behavior to
any singleemotion or motivation.To say that
behavior recorded in a given environmentis
a fearindicatordoes not necessarilymean that
fear is the only cause of this behavior. And
variations in the patternof the fear response
do not necessarilyimplydifferencesin the de-
gree of fear. Because of the complexityof the
phenomena that can affectemotional behav-
ior, it is not possible to relyon resultsisolated
fromcontext. A measurement used as a fear
indicator in one situation cannot be directly
extrapolatedto others,and it is impossible to
assess the magnitude ofconcepts like fearand
anxiety on the basis of a single objective and
perfectmeasurement. It is likelythatthevari-
ety of fear-relatedresponses representdiffer-
ent coping strategies.
181
The above analyses illustratethe complexity
of fear and anxietyconcepts, and emphasize
recognitionof the importance of interactions
among various factorsin modulating individ-
ual responses to aversive environmentalchal-
lenges. Although a certain consistencydoes
existin individualemotionaldispositions,fear-
relatedstrategiesdepend indeed on numerous
interactionsbetween: (1) these individualten-
dencies of reactivitywhich are shaped by ge-
netic background (species, strain and sex),
experiences (early experiences and learning
processes) and the stateoftheneuroendocrine
systems,and age or maturation, and (2) the
characteristicsof the experimental environ-
ment: social context, properties of stressors
(includingsize, lighting,color, substrate,nov-
elty,and procedure), controllability,and pre-
dictability.Thus the variation among results
is mainly due to this continuous modulation
of psychobiological reactivity.If experimen-
tal designs were carried out in a more stan-
dardized way and if care were taken when
extrapolatingfromone resultto another, di-
vergenceamong resultsshould be diminished.
Clearly thereare at least twolines ofexperi-
mental data that emphasize the relevance of
the concept of fearfulnessto a better under-
standing of the interindividualvariabilityin
adaptive behavior. First, there are many re-
sultsshowingcovariationbetween behavioral
and neuroendocrine traitsof fear, both at in-
dividual and at group levels, such as among
breeds or strains. Second, the existenceof ge-
netic relationshipsbetween some behavioral
and neuroendocrinetraitsof reactivityallows
investigatationof the biological bases of fear-
fulness.
Consequently, most argumentsagainst the
concept offearfulnessas a basic characteristic
may arise from the difficultyof comparing
resultsobtainedwithdifferent approaches. The
wide variabilityof factorsand responses re-
lated to an emotional stateis not put forward
here as a reason forabandoning the concept
of fearfulness.All this variability,however,
makes itnecessaryto relativizethe interpreta-
tion of this concept. Fearfulness can then be
definedas a basic characteristicofthe individ-
ual that predisposes it to react in a similar
manner to a large range of potentiallychal-
lengingevents. This profileofgeneral reactiv-
182 THE QUARTERL Y REVIEW OF BIOLOGY
ityis obviouslyadaptable, since itresultsfrom
the dynamicinteractionbetweengeneticback-
ground and epigenetic factorssuch as early
influencesand previous experiences.
FEARFULNESS AS AN INDEX OF VULNERABILITY
TO STRESS AND STRESS-RELATED DISEASES
An imbalance between environmentalde-
mand on the one hand, and psychobiological
reactionsand neuroendocrineemotionalstates
on theother,may account forvarious psycho-
somatic diseases. The role of neuroendocrine
systemsas etiologic factorsin mental disor-
ders or pathological outcomes, such as hyper-
tension and immune suppression, has often
been hypothesized (De Wied, 1979; Henry,
1988; Karasek and Theorell, 1990). Given
this complex framework,questions arise not
only about the originsand correlatesof inter-
individual differencesin emotional reactions,
but also about consequences ofthisvariability
in long-termadaptive processes. Could indi-
vidual differencesin the developmentofstress
responses or stress-inducedphysiopathology
be predicted by a particular set of emotional
traits? The study of emotional reactivityis
likelyto bring considerable benefitsshould a
set of fearfulnesstraitsbe identifiedthat pre-
dict the likelihood of developing stress and
stress-relatedpathologies. A few studies sug-
gest thatthe development of stresscan be in-
fluencedby the susceptibilityto be more easily
frightened.For instance,it is observedin poul-
try and rats that the more intense the fear
reactionsare, thegreaterare thepsychobiologi-
cal consequences fora chronicstressor(Jones,
1989; Tejedor del Real et al., 1991, respec-
tively). A betterunderstanding of interindi-
vidual variability in emotional reactivityis
thus essential to opening new avenues of re-
search in the human clinical and applied ani-
mal sciences.
Given their possible relevance for human
pathologies, animal models of psychobiologi-
cal reactivitymay be useful for developing
noninvasive experimental tools for studying
the physiopathologicalmechanisms underly-
ing vulnerabilityto anxiety-relatedor stress-
related disorders. For example, the clinical
study of drug addiction has indicated that a
major factorinfluencingpsychoactivedrug in-
take in humans is an individual'svulnerability
VOLUME 70
to thereinforcing effects
ofthedrug(O'Brien et
al., 1986). Recent researchin rodentsshowed
thatvulnerabilityto amphetamineself-admin-
istration,used as an experimental model of
drug addiction, may be predictedin individu-
als by assessing theiremotional reactivityto-
ward a novel environment(Piazza et al., 1991).
The higherthe locomotor and corticosterone
responses of rats to open-fieldexposure are,
the greater is their vulnerabilityto psycho-
stimulants.
One problem with animal fear as a model
forhuman emotionis thatfearin humans often
concernspsychosocialthreatratherthan psy-
chophysicalthreat.Indeed, as shownthrough-
out this article, the study of emotion in ani-
mals is oftenbased on pain conditioning,conflict
between punishment threat and hunger, or
the fear of extreme novelty or open spaces.
The question is whetherthese animal models
are the best strategies for investigatingthe
biological bases of the psychosocial reactivity
in humans. It may be suggested that animal
models using psychosocialcues would be use-
ful for investigatingthe human personality.
Indeed withinanimal colonies, emotional re-
action of individuals is often observed as a
response to threatarising fromtheir conspe-
cificgroup members, or at least is influenced
by the social context(Brain, 1990). Regard-
ing their linkages with human anxiety sys-
tems, such animal models mightbe useful in
providing homologies to a varietyof human
psychopathological conditionsarisingfromma-
jor life-challengingcircumstances.
Investigation of emotional reactivitymay
also be particularlyrelevantto assessment of
welfarein animal husbandry, since the well-
being of an individual depends on whetherit
can effectivelycope withenvironmentalchal-
lenge (Broom, 1988). Artificialselection for
improved zootechnical performancehas been
accompanied by selectionforadaptabilityto in-
tensivehousing(Price, 1984). However, farm-
ing practice has changed too frequentlyand
too rapidly for animal adaptive processes to
evolvesufficientlyas correlatedcharacters.More-
over, in intensivehusbandry,housing condi-
tionsprofoundlyrestrictthe degree of control
the animals have. As we saw earlier, thisloss
of control is often associated with increased
HPA axis activitythat may lead to various
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS
psychosomatictroubles. A large range of ab-
normal and undesirable behaviors, such as
aggression,overeating,stereotypiesand with-
drawal, occurs in modern farming(Dantzer
and Mormede, 1983). A fewstudies associate
lower productivitywithan increased suscepti-
bilityto being frightened.For instance, goats
thatare experimentallyratedas more reactive
present a higher degree of milk ejection im-
pairment(Lyons, 1989). The findingsreported
throughoutthisarticlesuggestthatemotional
reactivityin domestic animals may be open
to experimentalmanipulation geared toward
reducingtheincidenceofsome psychobiologi-
cal troubles. Because emotional reactivityis
to a certain degree under genetic control, a
selection program to reduce emotional reac-
tivitymay be undertaken in domestic mam-
mals, as ithas in rodentsand poultry.Because
experiencesduringparticularlysensitiveperi-
ods are also important, changes in human-
animal relationshipsduringtheseperiodsmay
be recommended(Boissy and Bouissou, 1988;
Boivin et al., 1992). The development of re-
search for assessing in domestic animals the
patternsof psychobiologicalreactivitymight
improveour understandingofthe factorsand
mechanismsgoverningthe elicitationof stress,
and offernew strategiesforimprovingthewell-
being of animals, and improvingproduction
efficiencyas well.
The conceptofemotionalreactivityis there-
fore importantand should be considered in
nonhuman animal studies. Moreover, animal
models are needed to establish the biological
bases ofhuman personality,because theyoffer
an experimentalapproach thatis impossibleto
employ in humans. Nevertheless, as shown
throughoutthisarticle,anthropomorphism of-
ten influencesthe definitionof emotion-induc-
ing events.The question is whethertraditional
animal models,essentiallybased on pain condi-
tioningand conflict,are best forinvestigating
emotions.It is suggestedthatsome approaches
realizedin semi-naturalistic
environmentsmay
be more useful, and that reactions in these
settingsbettermimick responses to threatsin
natural settings.Indeed, laboratory animals
exposed to natural situationsassociated with
nonpainfulthreats(predators, partial preda-
torystimuliand contextualstimuliassociated
with predators) display a broad spectrumof
183
emotional behaviors (Blanchard et al., 1990).
Moreover, the vast amount of data on the
contributionofsocialcues to antipredatorstrat-
egies, which are studied in free-rangingani-
mals, suggest a new alternativeforthe study
of emotions in the laboratory: inducing fear
or anxietythroughthe emotional reactionsof
conspecifics.As compared withtraditionalin-
vestigations,whichstudyreactionsoftheindi-
vidual directlyexposed to a challenge,models
based on thesocial communicationoffearmay
avert subjective interpretationand anthropo-
morphism.
CONCLUSION
Emotional reactionshave an importantim-
pact on the relationshipof an animal with its
environment.The psychobiologicalresponses
to environmental challenges depend on the
geneticbackground and earlyor previous ex-
periences of the individual. A complex inter-
action of these factorsis responsible for the
large range ofvariationin fear-relatedor anx-
iety-relatedresponses. Personality,tempera-
ment or individual behavior exists in nonhu-
man animals, and considerable progresshas
to be made in the understandingof interindi-
vidual differences.Fearfulnesshas to be con-
sidered as a componentof personalityand we
cannot dismiss the validity of fearfulnessas
an intermediatevariable that partlyexplains
the interindividualvariabilityobserved in an-
imal behavior. Furtherstudies are needed to
better understand the modifiabilityof emo-
tional traitsand the relative contributionsof
heredity,early environmentalinfluences,and
learningin the genesis ofinterindividualvari-
abilityin fear-relatedand anxiety-relatedre-
sponses. The developmentofnew approaches
and technologiesis now essential forprovid-
ing appropriate strategiesfor the investiga-
tion of fear and adaptive processes. Social
signals fromanimal communication that un-
equivocally induce fear will allow us to study
psychobiologicalpatternsthatmightbe func-
tionally interpretedas emotional reactions.
As Brain (1990) says, such developments"may
enable us to make more sense of what is cur-
rentlya ratherconfused literature."In addi-
tion to the interestin predictingthe adaptive
responses of individuals to various environ-
184 THE QUARTERL Y REVIEW OF BIOLOGY
mentalchallenges,the studyof fearfulness can
be used as a new approach to investigatethe
processesthatunderliethevariabilityin vulner-
abilityto stressand to stress-relateddiseases.
Such approaches are sure to have consider-
able relevance forhuman clinical and applied
animal sciences.
REFERENCES
Abbott, D. H., A. S. McNeilly, S. F. Lunn, M. J.
Hulme, and F. J. Burden. 1981. Inhibition of
ovarian functionin subordinate femalemarmo-
set monkeys(Callithrixjacchusjacchus). J. Reprod.
Fertil.,63:335-345.
Ames, D. R., and L. A. Arehart. 1972. Physiologi-
cal response of lambs to auditory stimuli. J.
Anim. Sci., 3:994-998.
Anisman, H., D. de Catanzaro, and G. Reming-
ton. 1978. Escape performancefollowingexpo-
sure to inescapable shock: deficitsin motor re-
sponse maintenance.j Exp. Psychol. Anim.Behav.
Processes,4:197-218.
Arave, C. W., J. L. Walters, and A. J. Svejda.
1980. Responses to open field testing of Hol-
stein heifers reared under four differentsys-
tems. J. Dairy Sci., 63:145.
Archer,J. 1973a. The influenceoftestosteroneon
chick behavior in novel environments. Behav.
Biol., 8:93-108.
. 1973b. Tests for emotionalityin rat and
mice: a review. Anim. Behav., 21:205-235.
. 1975. Rodent sex differencesin emotional
and related behavior. Behav.Biol., 14:451-479.
. 1976a. Emergence tests in testosterone-
treated chicks. Physiol.& Behav., 16:513-514.
. 1976b. Testosterone and fearbehavior in
male chicks. Physiol.& Behav., 17:561-564.
. 1976c. The organizationof aggressionand
fear in vertebrates. In P. P. G. Bateson and
P. Klopfer (eds.), Perspectives in Ethology,Vol.
2, pp. 231-298. Plenum Press, New York.
. 1979. Behavioural aspects of fear. In
W. Sluckin (ed.), Fear in Animalsand Man, pp.
56-85. Van Nostrand Reinhold, New York.
Armario, A.,J. L. Montero, andJ. Balasch. 1986.
Sensitivity of corticosterone and some meta-
bolic variables to graded levels of low intensity
stresses in adult male rats. Physiol. & Behav.,
37:559-561.
Axelrod, J., and T. D. Reisine. 1984. Stress hor-
mones: theirinteractionand regulation. Science,
224:452-459.
Barnett, S. A., and P. E. Cowan. 1976. Activity,
exploration, curiosityand fear: an ethological
study. Interdiscip.Sci. Rev., 1:43-62.
VOLUME 70
ACKNOWLEDGMENTS
I am gratefulto M. F. Bouissou,J. P. Signoret,
and P. Le Neindre fortheirhelpfulcomments on
the earlier version of the manuscript. I am greatly
indebted to D. A. de Catanzaro forhaving offered
many useful suggestions, including correctingthe
English of the paper.
Bignami, G. 1965. Selection for high rates and
low rates of avoidance conditioning in the rat.
Anim. Behav., 13:221-227.
Blanchard, R. J., and D. C. Blanchard. 1990.
Anti-predatordefenseas models of animal fear
and anxiety.In P. F. Brain, S. Parmigiani,R. J.
Blanchard, and D. Mainardi (eds.), Fear and
Defence,pp. 89-108. Harwood Academic Pub-
lishers, Chur.
Blanchard,R. J., D. C. Blanchard,J. Rodgers,
and S. M. Weiss. 1990. The characterization
and modelling ofantipredatordefensivebehav-
ior. Neurosci.Biobehav.Rev., 14:464-472.
Blizard, D. A. 1971. Autonomic reactivityin the
rat: effectsofgeneticselectionforemotionality.
J. Comp. Physiol.Psychol.,76:282-289.
Bohus, B., R. F. Benus, D. S. Fokkema, J. M.
Koolhaas, C. Nyakas, G. A. van Oortmerssen,
A. J. A. Prins,A. J. H. de Ruiter,A. J. W.
Scheurink, and A. B. Steffens.1987. Neuroen-
docrine states and behavioral and physiological
stressresponses. In E. R. de Kloet, V. M. Wie-
gant, and D. De Wied (eds.), Progressin Brain
Research,pp. 57-70. Elsevier Science Publish-
ers, Amsterdam.
Boissy, A. 1990. Les reactions emotives chez les
Bovins domestiques femelles (Bos taurusL.):
quantification et variations sous l'influencede
facteursenvironnementauxet hormonaux. PhD
thesis, University of Paris XIII, Paris.
Boissy, A., and M. F. Bouissou. 1988. Effectsof
early handling on heifers'subsequent reactivity
to humans and to unfamiliar situations. Appl.
Anim. Behav. Sci., 20:259-273.
, and . 1994. Effects of androgen
treatmenton behavioral and physiological re-
sponses of heifers to fear-elicitingsituations.
Horm. Behav., 28:66-83.
Boissy, A., and P. Le Neindre. 1990. Social influ-
ences on the reactivityof heifers: implications
for learning abilities in operant conditioning.
Appl. Anim. Behav. Sci., 25:149-165.
Boivin, X., P. Le Neindre, J. M. Chupin, and
J. P. Garel. 1992. Influence of breed and early
management on handling facilityand open-field
behaviour of heifers. Appl. Anim. Behav. Sci.,
32:3 13-323.
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS
Bouchard, T. J.,D. T. Lykken,M. McGue, N. L.
Segal, and A. Telleguen. 1990. Sources of hu-
man psychological differences:the Minnesota
study of twins reared apart. Science,250:223-
228.
Bouissou, M. F. 1985. Contribution a l'etude des
relations interindividuelleschez les Bovins do-
mestiques femelles(Bos taurusL.). PhD thesis,
University of Paris VI, Paris.
Brain, P. F. 1980. Adaptive aspects of hormonal
correlates of attack and defence in laboratory
mice: a studyin ethobiology. In P. S. McCon-
nell, G. J.Boer, H. J.Romijn, N. E. Van De
Poll, and M. A. Corner (eds.), Progress in Brain
Research,AdaptiveCapabilitiesof theNervousSys-
tem,pp. 391-414. Elsevier Science Publishers,
Amsterdam.
. 1990. A historical look at the concepts
of fear and defence and some conmments on
psychobiology. In P. F. Brain, S. Parmigiani,
R. J.Blanchard, and D. Mainardi (eds.), Fear
andDefence,pp. 1-21. Harwood Academic Pub-
lishers, Chur.
Broadhurst, P. L. 1975. The Maudsley reactive
and non-reactive strains of rats: a survey. Be-
hav. Genet.,5:299-319.
Broom, D. M. 1988. The scientificassessment of
animal welfare.Appl.Anim.Behav.Sci., 20:5-19.
Brush, F. R. 1991. Genetic determinantsof indi-
vidual differencesin avoidance learning: be-
havioral and endocrine characteristics. Expe-
rientia,47:1039-1050.
Brush, F. R., S. Baron, J. C. Froehlich, J. R.
Ison, L. J. Pellegrino, D. S. Phillips, P. C.
Sakellaris, and V. N. Williams. 1985. Genetic
differences in avoidance learningby Rattus nor-
vegicus: escape/avoidance responding, sensitiv-
ity to electric shock, discrimination learning
and open-fieldbehavior. J. Comp. Psychol.,99:
60-73.
Buchholz, R. A., J. E. Lawler, and G. F. Barker.
1981. The effects ofavoidance and conflictsched-
ules on the blood pressure and heart rate of
rats. Physiol.&Behav., 26:853-863.
Buitron, D. 1983. Variability in the response of
black-billed magpies to natural predators. Be-
haviour,87:209-236.
Canali, E., M. Verga, M. Montagna, and A. Baldi.
1986. Social interactions and induced behav-
ioural reactionsin milk-fedfemale calves. Appl.
Anim. Behav. Sci., 16:207-215.
Candland, D. K., and Z. M. Nagy. 1969. The
open-field: some comparative data. Ann. N. Y.
Acad. Sci., 159:831-851.
Candland, D. K., K. D. Pack, and T. J. Mat-
thews. 1967. Heart rateand defecationfrequency
as measures of rodent emotionality.J. Comp.
Physiol.Psychol.,64:146-150.
185
Cannon, W. B. 1935. Stresses and strains of ho-
meostasis. Am. J. Med. Sci., 189:1-14.
Carli, G., F. Farabollini, and C. Lupo Di Prisco.
1979. Plasma corticosteroneand its relation to
susceptibilityto animal hypnosisin rabbits.Neu-
rosci.Lett., 11:271-274.
Castanon, N., and P. Mormede. 1994. Psychobio-
genetics-adapted tools forthe study of the cou-
pling between behavioral and neuroendocrine
traits of emotional reactivity. Psychoneuroendo-
crinology, 19:257-282.
Castanon, N., C. Sandi, J. Dulluc, M. Le Moal,
and P. MormZede.1991. Genetic analysis ofthe
relationshipsbetween behavioral and neuroen-
docrine traits in Roman low and high avoid-
ance lines of rats. Endocr.Soc., 73:498.
Chaouloff, F. 1993. Physiopharmacological inter-
actions between stress hormones and central
serotonergicsystems.BrainRes. Rev., 18:1-32.
Cheney, D. L., and R. M. Seyfart. 1985. Vervet
monkey alarm calls: manipulation through
shared information?Behaviour,94:150-166.
Chevins, P. F. D. 1990. Early environmentalinflu-
ences on fear and defence in rodents. In P. F.
Brain, S. Parmigiani, R. J. Blanchard, and
D. Mainardi (eds.), Fear and Defence,pp. 269-
288. Harwood Academic Publishers, Chur.
Coe, C. L., D. Franklin,E. R. Smith, and S. Le-
vine. 1982. Hormonal responses accompa-
nyingfearand agitationin the squirrelmonkey.
Physiol.& Behav., 29:1051-1057.
Commissaris, R. L., G. M. Harrington, A. M.
Ortiz, and H. J. Altman. 1986. Maudsley reac-
tive and non-reactive rat strains: differential
performance in a conflicttask. Physiol. & Be-
hav., 38:291-294.
Craig,J. V., and A. W. Adams. 1984. Behaviour
and well-being of hens (Gallus domesticus)in al-
ternativehousing environments. World'sPoult.
Sci.J., 40:221-240.
Craig, J. V., T. P. Craig, and A. D. Dayton.
1983. Fearful behavior by caged hens of two
genetic stocks. Appl. Anim.Ethol., 10:263-273.
Curio, E. 1988. Cultural transmission of enemy
recognitionin birds. In T. R. Zentall and B. G.
Galef (eds.), SocialLearning.Lawrence Erlbaum
Associates, Hillsdale.
Dantzer, R. 1986. Behavioral, physiological and
functional aspects of stereotyped behavior; a
review and a reinterpretation. J. A nim.Sci., 62:
1776-1786.
Dantzer, R., and P. Mormede. 1980. Hormonal
influences on conditioned fear in pigs. Appl.
Anim. Ethol., 6:92-93.
, and . 1981a. Influence du mode
d'elevage sur le comportementet l'activite hy-
pophyso-corticosurrenaliennedu porcelet. Re-
prod. Nutr. Dev., 21:661-670.
186 THE QUARTERLY REVIEW OF BIOLOGY
, and . 1981b. Pituitary-adrenalcor-
relates of adjunctive activities in pigs. Horm.
Behav., 16:78-92.
, and . 1983. Stressin farmanimals:
a need forreevaluation. J. Anim.Sci., 57:6-18.
Dantzer, R., P. Mormede, R. M. Bluthe, and
J. Soissons. 1983. The effectof differenthous-
ing conditions on behavioural and adrenocorti-
cal reactions in veal calves. Reprod.Nutr.Dev.,
23 :501-508.
De Fries,J. C., M. C. Gervais, and A. E. Thomas.
1978. Response to 30 generations of selection
for open-field activityin laboratory mice. Be-
hav. Genet.,8:3-14.
Dellmeier, G. R., T. H. Friend, and E. E. Gbur.
1985. Comparison of fourmethods of calf con-
finement.II. Behavior. J. Anim. Sci., 60:1102-
1109.
De Wied, D. 1979. Schizophrenia as an inborn
error in the degradation of f-endorphin: a hy-
pothesis. TrendsNeurosci.,2:79-82.
Dickson, D. P., G. R. Barr, L. P. Johnson, and
D. A. Wieckert. 1970. Social dominance and
temperament of Holstein cows. J. Dairy Sci.,
53:904-907.
Dishman, R. K., R. B. Armstrong,M. D. Delp,
R. E. Graham, and A. L. Dunn. 1988. Open-
fieldbehavior is not related to treadmillperfor-
mance in exercising rats. Physiol.& Behav., 43:
541-546.
Dodd, J., and L. W. Role. 1991. The autonomic
nervous system. In E. R. Kandel, J. H.
Schwartz, and T. M. Jessell (eds.), Principles
ofNeuralScience,3rd ed., pp. 761-775. Elsevier,
New York.
Duncan, I. J. H., and J. H. Filschie. 1979. The
use of telemetrydevices to measure tempera-
ture and heart rate in domestic fowl. In C. J.
Amlaner and D. W. MacDonald (eds.), A Hand-
bookonBiotelemetry and Radio Tracking,pp. 579-
588. Pergamon Press, Oxford.
Dunn, A. J., and C. W. Berridge. 1990. Physio-
logical and behavioral responses to corticotro-
pin-releasing factor administration: Is CRF a
mediator of anxiety or stress responses? Brain
Res. Rev., 15:71-100.
Eberhart,J. A., E. B. Keverne, and R. E. Meller.
1983. Social influences on circulating levels of
cortisol and prolactin in male talapoin mon-
keys. Physiol.& Behav., 30:361-369.
Espmark, Y., and R. Langvatn. 1979. Cardiac
responses in alarmed red deer calves. Behav.
Processes.,4:179-186.
Evans, C. S., and P. Marler. 1992. Female ap-
pearance as a factor in the responsiveness of
male chickens during anti-predatorbehaviour
and courtship. Anim. Behav., 43:137-145.
VOLUME 70
Fanselow, M. S. 1984. Shock-induced analgesia
on the formalin test: effectsof shock severity,
naloxone, hypophysectomy, and associativevari-
ables. Behav. Neurosci.,98:79-95.
Fanselow, M. S., and F. J. Helmstetter. 1988.
Conditional analgesia, defensive freezing,and
benzodiazepines. Behav. Neurosci., 102:233-
243.
Faure, J. M. 1975. Etude des liaisons entre com-
portement en open-field et emotivite chez le
jeune poussin. Ann. Genet.Sel. Anim., 7:197-
204.
1979. Effetde l'habituation sur le compor-
tement en open-field du jeune poussin (Gallus
domesticus). Biol. Behav., 4:241-248.
1981. Bidirectionalselectionforopen-field
activityin young chicks. Behav. Genet.,11:135-
144.
Faure,J. M., andJ. C. Folmer. 1975. Etude gene-
tique de l'activiteprecoce en open-fielddu jeune
poussin. Ann. Genet.Sel. Anim., 7:123-132.
Faure, J. M., R. B. Jones, and W. Bessei. 1983.
Fear and social motivation as factorsin open-
field behaviour of the domestic chick. A theo-
retical consideration. Biol. Behav., 8:103-116.
Ferreira, A., S. Hansen, M. Nielsen, T. Archer,
and B. G. Minor. 1989. Behavior ofmotherrats
in conflicttests sensitiveto antianxietyagents.
Behav. Neurosci.,103:193-201.
File, S. E. 1980. The use of social interaction as
a methodfordetectinganxiolyticactivityofchlor-
diazepoxide-like drugs. J. Neurosci.Methods,2:
219-238.
Fleming A. S., and C. Luebke. 1981. Timidity
preventsthevirginfemaleratfrombeing a good
mother: emotionalitydifferencesbetween nul-
liparous and parturientfemales. Physiol.& Be-
hav., 27:863-868.
Gallup, G. G., Jr. 1977. Tonic immobility: the
role of fear and predation. Psychol.Rec., 27:
41-61.
Gamallo, A., A. Villanua, G. Trancho, and
A. Fraile. 1986. Stress adaptation and adrenal
activity in isolated and crowded rats. Physiol.
& Behav., 36:217-221.
Gibbs, D. M. 1986. Vasopressin and oxytocin:
hypothalamicmodulatorsof the stressresponse:
a review. Psychoneuroendocrinology, 11: 131-140.
Glowa, J. R., M. A. Geyer, P. W. Gold, and
E. M. Sternberg. 1992. Differentialstartleam-
plitude and corticosterone response in rats.
Neuroendocrinology, 56:719-723.
Goddard, M. E., and R. G. Beilharz. 1984. A
factoranalysis of fearfulnessin potential guide
dogs. Appl. Anim. Behav. Sci., 12:253-265.
, and . 1986. Early predictionofadult
behaviour in potential guide dogs. Appl. Anim.
Behav. Sci., 15:247-260.
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS
Gray,J. A. 1979. Emotionalityin male and female
rodents. A reply to Archer. Br. J. Psychol.,70:
425-440.
1987. The PsychologyofFear and Stress,2nd
ed. Cambridge University Press, Cambridge.
Guillemin, R., T. Vargo, J. Rossier, S. Minick,
N. Ling, C. Rivier, W. Vale, and F. Bloom.
1977. 13-endorphin and adrenocorticotropinare
secretedconcomitantly.Science,197:1367-1368.
Gyger, M., P. Marler, and R. Pickert. 1987. Se-
mantics ofan avian alarm call system: the male
domestic fowl(Gallus domesticus). Behaviour,102:
15-40.
Hall, C. S. 1934. Emotional behavior in the rat.
I. Defaecation and urination as measures of
individual differencesin emotionality.J. Comp.
Psychol.,18:385-403.
. 1941. Temperament: a survey of animal
studies. Psychol.Bull., 38:909-943.
Hard, E., and S. Hansen. 1985. Reduced fear-
fulness in the lactating rat. Physiol.& Behav.,
35:641-643.
Harrington,G. M. 1972. Straindifferences in open-
fieldbehavior ofthe rat. Psychon.Sci., 27:51-53.
Harrington,G. M., and D. A. Blizard. 1983. Open-
field behavior in the Maudsley Reactive and
Nonreactive strains: procedural variations. Be-
hav. Genet.,13:91-94.
Hemsworth, P. H., J. L. Barnett,D. Treacy, and
P. Madgwick. 1990. The heritabilityofthe trait
fearofhumans and the association between this
traitand subsequent reproductiveperformance
of gilts. Appl. Anim. Behav. Sci., 25:85-95.
Hendley, E. D., D. J. Wessel, andJ. Van Houten.
1986. Inbreeding of Wistar-Kyoto rat strain
with hyperactivitybut without hypertension.
Behav. NeuralBiol., 45:1-16.
Hennessy, M. B., and T. Foy. 1987. Nonedible
material elicitschewing and reduces the plasma
corticosterone response during novelty expo-
sure in mice. Behav. Neurosci.,101:237-245.
Hennessy, M. B., and S. Levine. 1978. Sensitive
pituitary-adrenalresponsiveness to varying in-
tensities of psychological stimulation. Physiol.
&Behav., 21:295-297.
Hennessy, J. W., and S. Levine. 1979. Stress,
arousal, and thepituitary-adrenalsystem:a psy-
choendocrine hypothesis.Prog.Psychobiol. Phys-
iol. Psychol.,8:133-178.
Henry, J.P. 1980. Present concept of stress the-
ory. In E. Usdin, R. Kvetnansky, and I. J.
Kopin (eds.), Catecholamines andStress:RecentAd-
vances,pp. 557-571. Elsevier North Holland,
New York.
. 1982. The relation of social to biological
processes in disease. Social Sci. & Med., 16:
369-380.
187
. 1988. Emotions et hypertensionpsycho-
sociale. Recl. Med. Vet., 164:751-766.
Hinde, R. A. 1985. Was "the expression of the
emotions" a misleading phrase? Anim. Behav.,
33:985-992.
Holstege, G. 1992. The emotional motor system.
Eur. J. Morphol., 30:67-79.
Ivanyi, T., V. M. Wiegant, and D. De Wied.
1991. Differentialeffectsof emotionaland physi-
cal stresson the centraland peripheralsecretion
of neurohypophysial hormones in male rats.
Life Sci., 48:1309-1316.
Ivinskis, A. 1970. A study of validityof open-field
measures. Aust.J. Psychol.,22:175-183.
Johnston, A. L., and S. E. File. 1991. Sex differ-
ences in animal tests of anxiety. Physiol.& Be-
hav., 49:245-250.
Jones, R. B. 1977a. Open-field responses of do-
mestic chicks in the presence or absence of fa-
miliar cues. Behav. Processes,2:315-323.
. 1977b. Repeated exposure ofthedomestic
chick to a novel environment:effectson behav-
ioural responses. Behav. Processes,2:163-173.
. 1984. Experimental noveltyand tonic im-
mobility in chickens (Gallus domesticus).Behav.
Processes.,9:255-260.
. 1986. The tonic immobility reaction ol
the domestic fowl: a review. World'sPoult. Sci.
J., 42:82-96.
. 1987a. The assessment of fear in the do-
mestic fowl. In R. Zayan and I. J. H. Duncan
(eds.), Cognitive Aspectsof Social Behaviourin thz
Domestic Fowl, pp. 40-81. Elsevier, Amsterdam.
. 1987b. The social and environmental as-
pects of fear in the domestic fowl. In R. Zayan
and I. J. H. Duncan (eds.), Cognitive Aspectsoj
SocialBehaviourin theDomesticFowl, pp. 82-149.
Elsevier, Amsterdam.
. 1987c. The assessment of fear in adull
laying hens: correlational analysis of methods
and measures. Br. Poult. Sci., 28:319-326.
. 1988. Repeatability of fear ranks amonQ
adult laying hens. Appl. Anim. Behav. Sci., 19:
297-304.
. 1989. Chronic stressors,tonic immobility
and leucocytic responses in the domestic fowl.
Physiol.& Behav., 46:439-442.
Jones, R. B., G. Beuving, and H. J. Blokhuis.
1988. Tonic immobilityand heterophil/lympho-
cyteresponses ofthedomestic fowlto corticoste-
rone infusion. Physiol.& Behav., 42:249-253.
Jones, R. B., I. J. H. Duncan, and B. 0. Hughes.
1981. The assessment of fear in domestic hens
exposed to a looming human stimulus. Behav.
Processes,6:121-133.
188 THE QUARTERL Y REVIEW OF BIOLOGY
Jones, R. B., andJ. M. Faure. 1982. Open-field
behaviour of male and female domestic chicks
as a functionof housing conditions, test situa-
tions and novelty. Biol. Behav., 7:17-25.
Jones, R. B., and B. J. Merry. 1988. Individual
or paired exposure ofdomesticchicksto an open-
field: some behavioural and adrenocorticalcon-
sequences. Behav. Processes,16:75-86.
Jones, R. B., and A. D. Mills. 1983. Estimation
of fearin two lines of the domestic chick: corre-
lations between various methods. Behav. Pro-
cesses,8:243-253.
Jones, R. B., A. D. Mills, andJ. M. Faure. 1991.
Genetic and experiential manipulation of fear-
related behavior in Japanese quail chicks (Co-
turnixcoturnixjaponica). J Comp. Psychol.,105:
15-24.
Jones, R. B., D. G. Satterlee, and F. H. Ryder.
1992. Fear and distressinJapanese quail chicks
of two lines geneticallyselected forlow or high
adrenocorticalresponseto immobilizationstress.
Horm. Behav., 26:385-393.
Jones, R. B., and D. Waddington. 1992. Modifi-
cation of fear in domestic chicks, Gallus gallus
domesticus, via regular handling and early envi-
ronmentalenrichment.Anim. Behav., 43:1021-
1033.
Karasek, R., and T. Theorell. 1990. HealthyWork:
Stress,Productivity,
and theReconstructionof Work-
ingLife. Basic Books, New York.
Kastin, A. J., M. A. Pearson, and W. A. Banks.
1991. EEG evidence that morphine and an en-
kephalin analog cross the blood-brain barrier.
Pharmacol.Biochem.Behav., 40:771-774.
Kavaliers, M., and D. D. Colwell. 1991. Sex dif-
ferencesin opioid and non-opioidmediatedpred-
ator-induced analgesia in mice. BrainRes., 568:
173-177.
Kerr, S. G. C., and D. G. M. Wood-Gush. 1987.
The developmentofbehaviourpatternsand tem-
perament in dairy heifers. Behav. Processes,15:
1-16.
Kilgour, R. 1975. The open-fieldtestas an assess-
ment of the temperamentof dairy cows. Anim.
Behav., 23:615-624.
Kopin, I. J., G. Eisenhofer, and D. Goldstein.
1989. Adrenergic response following recogni-
tion of stress. In S. Breznitz and 0. Zinder
(eds.), MolecularBiologyofStress,pp. 123-132.
A. R. Liss, New York.
Kovalcikova, M., and K. Kovalcik. 1982. Rela-
tionshipsbetween parameters of the open-field
test of cows and their milk production in loose
housing. Appl. Anim. Ethol., 9:121-129.
Kuchel, 0. 1991. Stress and catecholamines. In
G.Jasmin and M. Cantin (eds.), StressRevisited:
1 Neuroendocrinology of Stress,pp. 80-103. Kar-
ger, Basel.
VOLUME 70
Lacey, J. I. 1967. Somatic responsepatterning
and stress:somerevisionsofactivationtheory.
In M. H. Appleyand R. Trumball(eds.), Psy-
chologicalStress:
IssuesinResearch, pp. 14-44. Ap-
pleton-Century-Crofts, New York.
Lachaux, M., M. F. Bouissou,J. C. Berges,and
P. Orgeur. 1983. Etude du comportement en
open-field de beliersIle-de-France soumisa dif-
f6rentesconditionsd'elevage.Biol. Behav.,3:
257-269.
Lankin,V. S. 1976. Differences in the response
ofthepituitary-adrenal systemtopsychological
stressin sheepwithtwotypesofbehaviour.Isv.
Sib. Otd.Akad.Nauk.SSSR Ser.Biol.Nauk.,15:
105-108.
Lawrence,A. B., E. M. C. Terlouw,and A. W.
Illius. 1991. Individualdifferences in behav-
iouralresponsesofpigs exposedto non-social
and social challenges.Appl.Anim.Behav.Sci.,
30:73-86.
LeDoux, J. E. 1990. Fear pathwaysin thebrain:
implications fora theoryoftheemotionalbrain.
In P. F. Brain,S. Parmigiani,R. J. Blanchard,
and D. Mainardi (eds.), FearandDefence, pp.
163-178.HarwoodAcademicPublishers, Chur.
Lefcourt, A. M., S. Kahl, and R. M. Akers.1986.
Correlationof indicesof stresswithintensity
of electricalshockforcows.J. DairySci., 69:
833-842.
Leger,D. W., D. H. Owings,and D. L. Gelfand.
1980. Single-notevocalizationsof California
groundsquirrels:Gradedsignalsand situation-
specificityofpredatorand sociallyevokedcalls.
Z. Tierpsychol.,52:227-246.
LeMoal, M., andH. Simon.1991.Mesocorticolim-
bic dopaminergic network: functionaland regu-
latoryroles.Physiol.Rev., 71:155-234.
Leshner,A. I. 1979.Kinds ofhormonaleffects on
behavior:a newview. Neurosci. Biobehav. Rev.,
3:69-74.
Leshner,A. I., andJ.A. Politch.1979.Hormonal
controlofsubmissiveness in mice: irrelevance
oftheandrogensand relevanceofthepituitary-
adrenalhormones.Physiol.& Behav.,22:531-
534.
Ley, R. 1975. Open-fieldbehavior,emotionality
duringfearconditioning and fear-motivated in-
strumental performance. Bull.Psychon. Soc.,6:
598-600.
Lore, R. K., and F. B. Eisenberg.1986. Avoid-
ance reactionsof domesticdogs to unfamiliar
male and femalehumansin a kennelsetting.
Appl.Anim.Behav.Sci., 15:261-266.
Lyons,D. M. 1989.Individualdifferences intem-
peramentof dairygoatsand the inhibitionof
milkejection.Appl.Anim.Behav.Sci., 22:269-
282.
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS 189

Lyons, D. M., and E. 0. Price. 1987. Relation- Mineka, S., M. Cook, and S. Miller. 1984. Fear
ships between heart rates and behavior of goats conditioned with escapable and inescapable
in encounters with people. Appl. Anim. Behav. shock: effectsof a feedback stimulus. J. Exp.
Sci., 18:363-369. Psychol.Anim. Behav. Processes,10:307-323.
Lyons, D. M., E. 0. Price, and G. P. Moberg. Misslin, R., R. Bouchon, and P. Ropartz. 1976.
1988. Individual differencesin temperamentof Signification de certains parametres compor-
domestic dairy goats: constancy and change. tementaux chez la souris placee dans un open-
Anim. Behav., 36:1323-1333. field. Physiol.& Behav., 17:767-770.
Maestripieri, D., and F. R. D'Amato. 1991. Anxi- Misslin, R., and M. Cigrang. 1986. Does neopho-
etyand maternal aggression in house mice (Mus bia necessarily imply fear or anxiety? Behav.
musculus):a look at interindividualvariability. Processes,12:45-50.
J. Comp. Psychol.,105:295-301. Moberg, G. P., C. 0. Anderson, and T. R. Un-
Mason,J. W. 1971. A re-evaluation ofthe concept derwood. 1980. Ontogeny of the adrenal and
of non-specificityin stress theory.J. Psychiatr. behavioralresponsesoflambs to emotionalstress.
Res., 8:323-333. J Anim. Sci., 51:138-142.
McCarty, R., and I. J. Kopin. 1978a. Changes Moberg, G. P., and V. A. Wood. 1982. Effect
in plasma catecholamines and behavior of rats of differentialrearing on the behavioral and
during the anticipation of footshock.Horm.Be- adrenocortical response oflambs to a novel en-
hav., 11:248-257. vironment. Appl. Anim. Ethol., 8:269-279.
, and . 1978b. Sympatho-adrenal Mormede, P. 1991. Du stressa la physiopathologie
medullary activityand behavior during expo- de l'adaptation. Rev. Med. Fonct.,23:273-303.
sure to footshockstress: a comparison of seven Mormede, P., R. Dantzer, R. M. Bluthe, and
rat strains. Physiol.& Behav., 21:567-572. J. C. Caritez. 1984. Differences in adaptive
McFarland, D. 1987. The OxfordCompaniontoAni- abilities ofthreebreeds ofChinese pigs. Behav-
malBehaviour.Oxford UniversityPress, Oxford. ioural and neuroendocrine studies. Genet.Sel.
Meaney, M. J., D. H. Aitken,S. Sharma, V. Viau, Evol., 16:85-102.
and A. Sarrieau. 1989. Postnatal handling in- Mormede, P., R. Dantzer, P. Montpied, R. M.
creases hippocampal type II glucocorticoid Bluthe, E. Laplante, and M. Le Moal. 1984.
receptorsand enhances adrenocorticalnegative- Influence of shock-induced fightingand social
feedback efficacyin the rat. Neuroendocrinology, factorson pituitary-adrenalactivity,prolactin
50:597-604. and catecholamine synthesizing enzymes in
Miller, N. E. 1959. Liberalization of basic S-R rats. Physiol. &Behav., 32:723-729.
concepts: extensionsto conflictbehavior, moti- Mormede, P., V. Lemaire, N. Castanon,J. Dul-
vation and social learning. In S. Koch (ed.), luc, M. Laval, and M. Le Moal. 1990. Multi-
Psychology:A Studyofa Science,pp. 196-292. Mc- ple neuroendocrine responses to chronic social
Graw-Hill, New York. stress: interaction between individual charac-
Mills, A. D., andJ. M. Faure. 1986. The estima- teristicsand situational factors. Physiol.& Be-
tion of fear in domestic quail: correlations be- hav., 47:1099-1105.
tween various methods and measures. Biol. Be- Muir, J. L., and H. P. Pfister. 1987. Time course
hav., 11:235-243. ofthe corticosteroneand prolactin response fol-
and . 1990. Panic and hysteria in lowing predictable and unpredictable novelty
domestic fowl: A review. In R. Zayan and stress in Rattus norvegicus. Physiol.& Behav.,
R. Dantzer (eds.), SocialStressinDomesticAnimals, 40: 103-107.
pp. 248-277. Kluwer Academic, Dordrecht. Murphy, L. B. 1977. Responses of domestic fowl
, and . 1991. Divergent selection for to novel food and objects. Appl. Anim. Ethol.,
duration of tonic immobility and social rein- 3:335-349.
statementbehavior in Japanese Quail (Coturnix Murphy, L. B., and I. J. H. Duncan. 1976. At-
coturnixjaponica) chicks.]. Comp. Psychol.,105: temptsto modifythe responses ofdomestic fowl
25-38. towards human beings. The effectof early ex-
Mills, A. D., R. B. Jones, J. M. Faure, and J. B. perience. Appl. Anim. Ethol., 4:5-12.
Williams. 1993. Responses to isolation injapa- Natelson, B. H., D. Creighton,R. McCarty, W. N.
nese quail geneticallyselected forhigh and low Tapp, D. Pitman, andJ. E. Ottenweller. 1987.
sociality. Physiol.& Behav., 53:183-189. Adrenal hormonal indices of stress in labora-
Mineka, S., and M. Cook. 1988. Social learning tory rats. Physiol.& Behav., 39:117-126.
and the acquisition of snake fear in monkeys. Natelson, B. H., W. N. Tapp,J. E. Adamus,J. C.
In T. R. Zentall and B. G. Galef (eds.), Social Miller, and B. E. Levin. 1981. Humoral indi-
Learning.Lawrence Erlbaum Associates, Hills- ces of stress in rats. Physiol. & Behav., 26:
dale. 1049-1054.
190 THE QUARTERL Y REVIEW OF BIOLOGY
Naumenko, E. V., N. K. Popova, E. M. Nikulina,
N. N. Dygalo, G. T. Shishkina, P. M. Boro-
din, and A. L. Markel. 1989. Behavior, adre-
nocortical activity, and brain monoamines in
Norway rats selected for reduced aggressive-
ness towards man. Pharmacol.Biochem.Behav.,
33:85-91.
Netto, C. A., B. Siegfried,and I. Izquierdo. 1987.
Analgesia induced by exposure to a novel envi-
ronmentin rats: effectof concurrentand post-
trainingstressfulstimulation.Behav.NeuralBiol.,
48:304-309.
O'Brien, C. P., R. N. Ehrman, andJ. N. Terns.
1986. Classical conditioning in human opioid
dependence. In S. R. Goldberg and I. P. Stolr-
man (eds.), BehavioralAnalysisof Drug Depen-
dence,pp. 329-338. Academic Press, London.
Olivero, A., and C. Castellano. 1990. Genetic ap-
proaches to fear and defence. In P. F. Brain,
S. Parmigiani, R. J. Blanchard, and D. Main-
ardi (eds.), Fear and Defence,pp. 144-162. Har-
wood Academic Publishers, Chur.
Overstreet, D. H., A. H. Rezvani, and D. S. Ja-
nowsky. 1992. Maudsley reactiveand nonreac-
tive ratsdifferonlyin some tasksreflectingemo-
tionality. Physiol.& Behav., 52:149-152.
Parrot, R. F., and S. N. Thornton. 1989. Opioid
influenceson pituitaryfunctionin sheep under
basal conditionsand duringpsychologicalstress.
Psychoneuroendocrinology, 14:451-459.
Piazza, P. V.,J. M. Demini?ere,S. Maccari, M. Le
Moal, P. Mormede, and H. Simon. 1991. Indi-
vidual vulnerabilityto drug self-administration:
action of corticosteroneon dopaminergic sys-
tems as a possible pathophysiological mecha-
nism. In P. WillnerandJ. Scheel-Kruger (eds.),
TheMesolimbicDopamineSystem:FromMotivation
to Action,pp. 473-495. Wiley & Sons, New
York.
Plomin, R. 1990. The role ofinheritancein behav-
ior. Science,248:183-188.
Plomin, R., J. C. De Fries, and G. E. McClearn.
1990. BehavioralGenetics:A Primer.W. H. Free-
man, New York.
Plotsky, P. M., E. T. Cunningham, and E. P.
Widmaier. 1989. Catecholaminergic modula-
tionofcorticotropin-releasing factorand adreno-
corticotropinsecretion. Endocr. Rev., 10:437-
458.
Price, E. 0. 1984. Behavioral aspects of animal
domestication. Q. Rev. Biol., 59:1-32
Renner, M. J., and M. R. Rosenzweig. 1987.
Enrichedand Impoverished Environments. on
Effects
BrainandBehavior.Springer-Verlag,New York.
Restrepo, C., and A. Armario. 1987. Chronic stress
alters pituitaryadrenal functionin prepubertal
male rats. Psychoneuroendocrinology,
12:393-398.
VOLUME 70
Rogers, L. J., H. S. Sink, and J. W. Hambley.
1988. Exploration, fear, and maze learning in
spontaneously hypertensiveand normotensive
rats. Behav. NeuralBiol., 49:222-233.
Russel, P. A. 1979. Fear-evoking stimuli. In
W. Sluckin (ed.), Fear in Animalsand Man, pp.
86-124. Van Nostrand Reinhold, New York.
Rutter, S. M., and I.J. H. Duncan. 1988. Mea-
suringfearin domesticfowlusing aversionlearn-
ing. In International Congresson AppliedEthology
inFarmAnimals,pp. 108-114. Skara (Sweden).
Sapolsky, R. M. 1990. Adrenocortical function,
social rank, and personality among wild ba-
boons. Biol. Psychiatry, 28:862-878.
Satterlee, D. G., andW. A.Johnson. 1988. Selec-
tion ofJapanese quail forcontrastingblood cor-
ticosterone response to immobilization. Poult.
Sci., 67:25-32.
Seabrook, M. F. 1972. A study to determine the
influence of the herdman's personalityon milk
yield. J. Agric. Labour Sci., 1:1-45.
Seggie, J. A., and G. M. Brown. 1975. Stress
response patternsof plasma corticosterone,pro-
lactin and growthhormone in the rat following
handling or exposure to novel environment.
Can. J. Physiol.Pharmacol.,53:629-637.
Seligman, M. E. P. 1975. Helplessness:On Depres-
sion, Development, and Death. W. H. Freeman,
San Francisco.
Selye, H. 1936. A syndrome produced by diverse
nocuous agents. Nature,138:32-33.
. 1950. Stress:ThePhysiology and Pathology of
Exposureto Stress.Acta Medica, Montreal.
Seyfarth,R., D. L. Cheney, and P. Marler. 1980.
Monkey responsesto threedifferent alarm calls:
evidence ofpredatorclassificationand semantic
communication. Science,210:801-803.
Shanks, N., J. Griffiths,S. Zalcman, R. M. Za-
charko, and H. Anisman. 1990. Mouse strain
differencesin plasma corticosteronefollowing
uncontrollablefootshock.Pharmacol.Biochem.Be-
hav., 36:515-519.
Shelton,M., and D. Wade. 1979. Predatorylosses:
a serious livestockproblem. Anim. IndustryTo-
day, 2:4-9.
Siegfried,B., C. A. Netto, and I. Izquierdo. 1987.
Exposure to noveltyinduces Naltrexone-rever-
sible analgesia in rats. Behav. Neurosci., 101:
436-438.
Skinner, B. F. 1953. Scienceand Human Behavior.
MacMillan, New York.
Stephens, D. B., and J. N. Toner. 1975. Hus-
bandry influences on some physiological pa-
rametersofemotional responses in calves. Appl.
Anim. Ethol., 1:233-243.
Stern,J. M., M. S. Erskine, and S. Levine. 1973.
Dissociation ofopen-fieldbehaviorand pituitary-
adrenal function.Horm. Behav., 4:149-162.
JUNE 1995 FEAR AND FEARFULNESS IN ANIMALS
Stern, J. M., and S. Levine. 1974. Psychobio-
logical aspects of lactation in rats. Prog. Brain
Res., 41:433-444.
Stone, E., and C. H. Trost. 1991. Predators, risks
and contextformobbingand alarm calls in black-
billed magpies. Anim. Behav., 41:633-638.
Svensson, L., C. Harthon, and B. Linder. 1991.
Evidence fora dissociation between cardiovas-
cular and behavioral reactivityin the spontane-
ously hypertensive rat. Physiol. & Behav., 49:
661-665.
Tachibana, T. 1982. Open-field test forrats: cor-
relational analysis. Psychol.Rep., 50:899-910.
Taylor, G. T. 1981. Fear and affiliationin domes-
ticated male rats.J. Comp. Physiol.Psychol.,95:
685-693.
Taylor, L., and T. H. Friend. 1986. Open-field
testbehavior ofgrowingswine maintained on a
concretefloorand a pasture. Appl. Anim.Behav.
Sci., 16:143-148.
Tejedor del Real, P., J. Gibert-Rahola, I. Leon-
segui, andJ. A. Mico. 1991. Relationship be-
tween emotivitylevel and susceptibilityto the
learned helplessness model of depression in the
rat. In AnimalModels in Psychopharmacology: Ad-
vancesin Pharmacological Sciences,pp. 217-224.
BirkhaiuserVerlag, Basel.
Torres-Hemandez, G., and W. Hohenboken. 1979.
An attempt to assess traits of emotionality in
crossbred ewes. Appl. Anim. Ethol., 5:71-83.
Vandenheede, M., and M. F. Bouissou. 1993a.
Sex differencesin fearreactions in sheep. Appl.
Anim. Behav. Sci., 37:39-55.
, and . 1993b. Effectof androgen
treatmenton fear reactions in ewes. Horm. Be-
hav., 27: 435-448.
Van Der Staay, F. J., S. Kerbusch, and W. Raaij-
191
makers. 1990. Genetic correlations in validat-
ing emotionality. Behav. Genet.,20:51-62.
Veissier, I., P. Le Neindre, and G. Trillat. 1987.
The influenceof mother-youngrelationshipson
behavioural reactivityand learning in calves.
Biol. Behav., 12:222-238.
Veldhuis, H. D., E. R. De Kloet, I. Van Zosten,
and B. Bohus. 1982. Adrenalectomy reduces
exploratory activity in the rat: a specific role
for corticosterone. Horm. Behav., 16:191-198.
Walker, C. D., R. W. Rivest, M.J. Meaney, and
M. L. Aubert. 1989. Differentialactivation of
the pituitary-adrenocorticalaxis afterstressin
therat: use oftwo geneticallyselectedlines (RLA
and RHA) as a model. J Endocrinol.,123:
477-485.
Walsh, R. N., and R. A. Cummins. 1976. The
open-fieldtest: a critical review. Psychol.Bull.,
83:482-504.
Warnick, V. D., C. W. Arave, and C. Mickelsen.
1977. Effectsof group, individual and isolated
rearing ofcalves on weightgain and behaviour.
J. Dairy Sci., 60:947-953.
Webster, A. B., andJ. F. Hurnik. 1990. Open-
fieldassessment ofbehavioral phenocypewithin
genetic stocks of the White Leghorn chicken.
Appl. Anim. Behav. Sci., 27:115-126.
Weiss, J. M. 1972. Psychological factorsin stress
and disease. Sci. Am., 226:104-113.
Wiener, S. G., and S. Levine. 1983. Influence of
perinatal malnutrition and early handling on
the pituitary-adrenalresponse to noxious stim-
uli in adult rats. Physiol.& Behav., 31:285-291.
Zuckerman, M. 1991. Basic dimensions ofperson-
ality. In M. Zuckerman (ed.), Psychobiology of
Personality,pp. 1-43. Cambridge University
Press, Cambridge.