Walsh, RN.,and Rk Cummim The open-field test A critical review. P s v c h o l o e i c a l Bulletin ' .83:482-504, 1976.

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1976. ~ y 1 o 8 KO.3 . 482-IM ,

d B&lb

The Open-Field Test: A Critical Review

Robert A. Cummins Roger N. Walsh Department of Psych+ and ~ e b a o k r a ~ Department of Physiology, Llnioersify .c$ S&nces, Stanford Unioersity Queensland, Brisbane. Australia Over the w t 4 0 years Lhc open field bar ~ o l v e da a commonly used tool for the rnmumcnt of animal behavior. Thh m i e w taka a dtical look at & instrument, u&y with regard to the development of a the we of I standard form for iu w. The variou procedura and .their sbortcomingr are 'dkmued, - w i t h partimlar rcfupacc to the seemingly incooseguential detdk which have b.& showb to ioduhte open-field prformancc per w. Depndent paramrerr are considered both vith regard to their reliability and their validity for the measurement of such undul,ing mnstrucb as emotionality. Since its introduction some 4 0 years ago. the open-field test bas attained the status of one of the most widely used instruments in animal psychology. Its popularity probably stems in large part' from the simplicity of the apparatus, tbe-easy &d rapid meaurement o f dearly defined behaviors, and a generally accepted interpretation of these behaviors. I n . addition, certain ol tbe measured behaviors are sensitive to a a i d e range of genetic! experiential, physiological, and pharmacological manipulations and are sufficiently reliable under standardized conditions t'o give repeatable measures on an enormous range of independent variables. Simplicity, ease of quan: tification, and a i d e applicability are therefore probably the prime determinants of its popularily. However, in spite of its'sbtus as one of the most widely used tests of animal behavior, the open-field test bas survived for 40 years uilh only one major review (Archer, 1973), and this was limited to a consideration of its usefulness for slimatinn emotionalitr in rodents. Apparatus, techniques, subjects, parameters, analyses, and interpretations .have diversified enormously, yet in the literature, sweeping generalimtions and conflicting interpretations continue to he made on the basis of univariate studies. This paper aims at detailing the many variables involved in testing and their influences on dependent parameters, as well as methods of analysis and interpretation of results. We thereby hope to gain an overview o i this area of study! to point out shortcomings of some present work, and LO derive implications for future research. The originator of the open field was Calvin Hall (Hall 1 9 3 4 ; Hall & Ballechey 1932), who used d e f a t i o n in the open field as an index of timidity. However, time bas seen a proliieration of other dependent variables. Some 30 have been used at one stage or another:. and the number of underlying constructs they supposedly measure bas multiplied accordingly. I n niany cases, however. proof of construct validity has been a d l y lacking. IV'hat then is the open field and what, in general terms: does it really measure? I n essence, the test consists of the measurement p i behaviors elicited by placing the subject In a novel open space from which escape i s prevented by a surrounding wall. We would like to exDrps our ~ratitudcto Otto T h e elicitation of these behaviors is deBudlz-Olsen, Bun ~icdelman,TO& Horvalh, and pendent upon the interaction of the animal Alice LH for their encouragement, advice, and with a variety of test factors such (a)criticism. Our uperimeotal work and prepration of -stimulation z a result of removal from a be manulc,jpt were supporkd from Australian Rwarch Grants Committee and t h e familnr home environment; ( b ) stimulation Foundatton Fund for Rcvarch in Psychiatry. involved in transferring the animal to the Rcqursu for reprints should be x n t to Robert A. Open field; !c) m ~ o s u r e the test environto cumrnins, D~~~~~~~~~ Psycholow,Univerrlt,. of of \Vutero .4ustralia, Nedlands, Perth 6039, ~ust~alia.ment, consisting of both the open field itself

OPEN-FIELD TEST

4S3

and its surroundings; and ( d ) aU prior eiperience of the t e t situation. In ee & ,c t' tbis last factor means that one is measuring,. among other things, habituationand learning in response to the test environment. Where several test s q i o n i are employed, further factors to be' considered indude previous stimulalion involved in removing the animal from. the. testing situation, transfer and reexposure !o the home environment a t the completion of prior sesions, and modification of h o m e a g e pehavior .and interaction- with other home environment animals. The magnitude of any particular behavior elicited will therefore be a function of the multiway interaction oi these factors. .4s yet their relative importance is almost completely unknown,.but thereis evidence to suggest that each factor exerts a differential elfect on animals oi varying genetic and experiential backgrounds, and this is examined later. Effectively 3nv behavioral experimentmeasures responses to the above fattors. However, in many-studies, such as maze learning;. one hope3 that the subject will habituateto, and hence be minimally influenced by, aspects . of thetes: siruation other than the specific stimulus c~lmponentbeing u s e d % the independent variable. In -the open-field test, on the other hand, the whole test situation (rather than any one specific stimulus component) is the independent variable, and.by its very nature this independent variable must be multifactorial. These factors are now considered under the headings of Techniques and Apparatcs Characteristics, Testing Environment, and Procedural Details:

~ o o k i & a t the range of techniques employed. one finds'tbat for the apparatus, its size, shape, color,. subdivision, wall height, Boor texture, odor, nature and locauon.of the starting arm, and presence or absence and nature o i additional inherent stimuli have all been varied; while for the surroundings the nature, intensity and position of light, sound andodor sources, and the visibility and position of the observer have- suffered similarly. In fact it is hard to think of any facet which has not been modified. This .diMculty of standardization b compounded by the ex1rerre:rarity of reports which cite details of more than a smdl proportion .of relevant procedural variables. Ph?sical .Characteristics o j the Apparatus

The most common shape of the open field has been circular, but square and rectangular designs are also prevalent. The wide range of shapes leads eventually to the quejtion. \i:hen is an open field not an open field? The extreme of the rectangular design is usually termed a straightaway or a rur&a.v, yet the behaviors measured may be akin to those employed in the open. fidd (e.g., Poley & Royce, 1970; Zimhardo & Ilontgomer)., 1 9 5 7 ) . Perhaps in view of the paucity of eiidence on the comparability of behavior observed in these devices and in the open field, they are best regarded separately. As ,yet there would seem to be no data available on the effect o i open-field shape on behavior, hut in view oi the evidence on strain difierences in thigmota<s (or "wall hugging," Valle, 19i0) and the tendency of some animals to remain in corners, standardization would seem a sensible precaution. Difierent s ~ e c i e jhave naturdlv been allocated appropriately sized open fields, such The difficulty of finding comparable techa whole room for human infants (fieinniques in the use o f the open field has been gold, 1969) and a .5-m square field f o r mice mentioned previously. Almost every physical (hlanosevitz. 1970). More importantly, howcharacteristic of the apparatus; i t i surround- ever, open-field size has -commonly been in&, a n d every s!ep have been varied for intraspedes studies, and the efiects widely varied, so that although standardin- of such dimensional changes have been shown Lion may have been established aithin in- to exert a significant &ect on some aspects dividual laboratories, there is a disturbing oi behavior. .4s a ~ e n e r a lrule. ambulation lack oi conformity in procedure and resulu urould seem to be more susceptible to change in apparatus a n d environment than would within theliterature as a whole.

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ROGER K . WALSH ASD ROBERT A. COMbfINS

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defecation: Thus, while defecation is largely unaflected by arena size in rats (Broadhurst, 1957, 1958a, 1958b), gerbils (Oldham & Morlock; 1970), but not male WH mice (Nagy & For&, 1970), ambulation increases with increasing field size in rats (Broadhurst. 1957; Montgomery, 1951), mice (Blizard; 1971 ; Krsiak & J d u , 1971 ; Nagy & Forest, 1970); and gerbils (Oldham .& Morlock; 1970). Large field size has been reported to produce a , disproportionately large increae in ambulation under conditions of low illumination (Blizard, 1971): An .example of the daculties .of comparison where different apparatuses are used is afIorded by ~ l a r i , Gorman, and Vernadakk (1970), wbo tested ambulation of the offspribg of mothers injected with impbetamine or chlorpromazine. Treatment effects were found on Days 13-21 but not on Days 46, and 60, and the results were interpreted ar being due to differential maturation rat& (an Age x Treatment' interaction hypothesis). However, since two different field k w e r e used for the infant and adolescent animals, a n interaction between treatment and field size was also possible. Color bas ranged through white (Oldham &'3Torlock, 1970) to black (Delbarre, Durn=, & duionniere, 1970), and the material composing the field, particularly the Boor, has included wood, metal, cqncrete, rubber, and even glass (Satinder, 1968). There is almost no evidence as yet on the eEect of these variables on behavior, but in view of the evidence for the effects of similarity of test envimnment lo rearing environment on exploratory behavior (Nielson, 1970; Wells, Lowe, Sheldon, & .Williams, 1969), some of these variables may be of particular relevance when testing animals with differential rearing histories. Klost commonly, the open field has been bare but occasionally experimenters have added objects, usually with the aim of obtaining a measure of interaction with these additional stimuli. The number of these objects has ranped from 2 (Ehrlich & Burns, 1958) to 15 (Furchtgott, Wechkin, & Dees. 1961) a n d t h e y have usually been small solid ob-'' jec&, such as nuts and balk, door stops, and

mirrors. However, the more exotic have included caged rats, f l d i n g ' l i g h t s and loudspeakers (Ehrlich & Bums, 1958; Fox & Spencer, 1969), food pellets (Jarrard 9. Brunnel, 1968), designs painted on the floor and walls (Wimer & Sterns, 1964); and Rheingold's (1969) study of human infants induded toys and the .subject's mother or another person(basicaUy a social facilitation study). The relevant dependant paramiters are most commonly the number of approaches and time spent invejtigating the objects, and sometimes preference scores for particular objects.

THETESTINGX ~ O N M E N T E Characteristics not o n l y of the open field itself but also of its surroundings infringe upon the subjects and modify behavior. The level of illumination has been the variable most closely examined; but in spite of repeatedly demonstrated eElects, . f&er than one third of the articles mention the test lighting used. With the exception of Candland and Nag?r (1969), who reported Lhe reverse, i t bas consistently been found tbat high levels of illumination are associated a i t h diminished locomotor. behavior. Valle (1970) found that ambulation, rearing, and thigmotaxis were all less under higher illumination. A number of interactions of illumination level a i t h other independent variables bare been reported. Thus, L i v w y and Egger (1970) found tbat ambulation was less under an illuminance of 9.3 lx than 0.005 lx in rats a t 47 or 115 days of age but not at 18 or 24 days. Testing C57 BL/6J mice, Nagy and Glaser (1970) found no main effect for illumination (9.3 k versus 0.09 k ) but found si~nificant interactions between level of illumination, age of subjects, and day of testing. Under high illumination, there were no reliable activity differences due lo age, while under low levels, IO&day-old subjects were more active than 5&day+lds. T h e subjects were less active under high than under low illumination on Days 1 and 2 of testing but not thereafter, suggesting that for the C57 BL/6J strain, illumination effects are largely transitory. Interactions with strain have been reported by McClearn (1960) and by Dixon

OPES-FIELD TEST

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and Defries (1968b), who also found albinos to he more photosensitive than pigmented rats. Interaction witb. prior visual rearing environment (dark, alternating light-dark, or light in black, white, or patterned cages) was noted by Sachett (1967). Another commonly studied dependent pa; rameter of. illumination has been defecation, and Rith. some exceptions (Blizard, 1971); no significant main.e8ect has been reported (Kagy & Forest, 1970; Nagy & Glaser, 1970; Nag) 8: Holm, 1970). The result seems unexpected in terms of much current thinking which considers high illumination as "stressful" and defecation as the prime index of emotionality. A dijadvantage of the available studies of illumination is that they include only two, or a t the-most three levels, so that the precise relationship with the magnitude01 the observed behavior is quite unlmoivn. Less study has been made of ambient noise and few papers refer to it. Presumably. Lherefore, in most cases it comprises merely the' background noise oi the test room, but white noise, most commonly of about S dB (e.g., O Eysenck & Broadhurst, 1964; Ivinskis, 196S), has sometimes been superimposed. Its addition h s usually reduced locomotion (e.g., Bindra & Spinner, :l9jS), but L i v e ) , i n d Egger (1970)' reported that white noise of 90 dB increased both ambulation and defecation. Certainly any abrupt loud noise can markedly inhibit locomotion a n d even induce prolonged immobility in a variety of species (Hofer, 1970; Cummins, Walsh: & BudtzOlsen, Kote 1). Environmental odors have largely been ignored. although several experimenters have washed their apparatus. with a vaiiety of agents in order to obviate possible biasing efiects of odor trials left by previous subjects. \\%ittier and McReynolds (1965) found this to be asigni&ant effect for the test behavior of mice. However, Satinder (1969) found that the time spent by a rat on the side of the open field which had been occupied by its predecessor was significant only for males preceded hy females. Interestingly; urination or defecation by the,predeceswr was without effect.

McCall (1969) has demonstrated tbe importance of odor for what he termed the "caretaker efiect." I t was found that rats tended to spend more time on the side of the field nearest to the caretaker, who had reared them, than on the side opposite where there waj another experimenter, who had no previous experience with them. This effect was. shown to b e dependent on olfactory rather than %%ual cues, The visibility and behavior 01 the experimenter during testing have rarely been mentioned. Presumably, therefore, in most test situations he is visible to the subject except where obsenration is frombehind a screen (e.g., Nielson, 1970) or a one-way mirror (e.g., Fox 8: Spencer, 1969). This hiding would seem a wise precaution, since although no precise studies of the effects n i experimenter visibility are available, it i i quite obvious that any visible abrupt movement may cause inhibition of ongoin.=;..ac: ~ i v i t y in some u s e s prolonged immobtl~ty and (Cummins et a]., Note I ) . PkioCEDurw~ DETAILS As is obvious from the foregoing discussion, careful measurement can detect changesin behabior due to very small changes in the apparatus. I t is therefore regrettable that there has beenalmost no study of the efiects of variation in testing procedure. Testing normally consists of removing the animal from its home environment, carrying it to the test area, and placing it in the open field. The carrying can be done either by hand or via a start box. Testing itself may vary on a num.ber of temporal factors, such as the duration of exposure. to the open field and t h e intertrial interval. I t would be surprising if changes in these procedures did not measurably aRect open-field behavior. Details o i the animal's removal from the home cage and transfer to the open field are seldom reported, so that presumably they are usually transported by hand. However, some workers aiming to reduce handling stress have employed transport compartments, such as a box (Nielson: 1971: Tighe, 1965), tube ( D i ~ o n Defries, 1968a), or transparent cup & (Hofer. 1970): In some a e s , the subjects have been habituated to a transport compart'

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ROGER

x. \VALSH

AKD ROBERT A: C U ~ ~ ~ I I X S

I.'B&>~o;

k Whole m mnjor body mmcmorl 1. Type of movement a. Distance covered per unit time b. Time spent in ambulntioo c. Wesring frequency d: Escape attempts e. Laleocy (uwdlytime taken lo l a v e start area) i. Time spentaithout movement
2. Loc1tions a. Field area viGtnl (inner or peripheral a r m . mmm, elr.) ' 4. .AMliation (distance from p n n e r subject) c. Stimulusintetxtion (e.g., dirtan& irom stimulus

abject)

B. Par1 body nromnmr a. \lanipulatius of objects

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b. S S m g c. Smtchinc d: Digging e. Teeth chattering I. Grooming g. vocalimtion h. Visual erplomtion

11.

Autonomic nervnus %stem

'a. Defecation

b. Digestive transit time c. Urination. d. Hurt tale a d rhythm -e. X s p i r s t ~ r ? rstc

1U. Adrend activity a, Adrenal ascokbic s d d ' .

b. Serum

corticosteroidr

W. E 3 m ~ 0 p b y s i o l o ~
3.

have been employed by Block and Essman (1965). Many workers measure only total behavior lor e3cb trial (intratrial time unit equals trial length), thus relinquishing any possibility of studying intratrial temporal patterns of behavior. Some go a staee further, mesuring only total behavior over all trials. These practices sacrifice a considerable amount of available information, and their disadvanta,nes are detailed i n the d i s m ' o n on temporal analysis of behavior.. Many aperimenters employ only one trial: a procedure of doubtful value in view of the difficulties of interpretation indicated by Wlinibey and Denenberg (1967), who found a chanye in factor loading of ambulation from Day 1 to Day Z..3.fultiple trials avoid this criticism and afford greater reliability and the opportunity of temporal analysis. Those who give several trials seldom use more than 4, but up to 6 0 h a v e been used (Bronstein, 1972). \\'here multiple trials. are given, the question of the optimal intertrial internal arises; but most commonly, 24 hours has been chosen, partly from convenience hut a h since this obviates complications of diurnal rhythm. Almost no study seems to have been perlornied on .theefiects of variing these temporal factors. However, Battig (1969) found that patterns of activity were undected by exposure to the apparatus 2 hours previous to the experiment, but that intertrial intervals o i 3 and 12 minules produced a mild inhibition of ambulation on subsequent testing.

Hippocampal theta utivity

b. Elccvomyogmm activie

DEPENDEXTA R A ~ ~ R S 'P
The number of dependent variables used to aswy open-field behavior has grown substantially since the early work of Hall (1934). until now over 50 are listed. This list (see Table ' 1 ) is mostly compiised of behavioral measures, although recently some physiolog'ical parameters, such as heart and respiration rates! electrom~ogramrecordings, and plasma steroid levels,. have also been included. . can be seen from Table 1 most paramk eters have been varieties of motor behavior, and of these, measures of ambulation have been most favored. This is presumably because of the ease of quantification and the evident face validity for interpretive con-

ment and carrying procedure prior to testing (e.g., Nielson, 1970). Such familiarization may increase the levels of ambulation a t the start o f an open.-field trial (Abel, 1971). Once ' traEported, the animals may be placed either in the center of the open field (e.g., Clark et al., 1970) or against the retaining wall (6ing, 1970). I n this context i t is interesting 1o'note.Satinder's (1969) find'ing that rats tehd to remain on that side of the field on which they are originalls placed. Jndividual trial durations are usually short (Krsiak & Janku,-19il), but trials of 1 hour

0PES.FIELD TEST strucb of exploration and arousal. Amount of ambulation has usually been scored spatially by the number of subdivisions entered, but has also been estimated temporally by the proportion of time spent inambulation. I t has also been quantified according to cbaracteristics 01 its apparent aim, locality, and latency. Thus, ambulatiob directed toward escape has been measured by Ehrlich and Burns (195S), who scored an escape attempt if the subject got its head and forefeet over the wall 01 the field. Ambulation has also been scored according to its locality, the most frequently .used regional divisions being either inner or peripheral areas of the apparatus (Ebrlich & Burns, 1953; Ivinskis, 196s). Occupancy of the peripheral a r m , either in corners ( h l o r r k n 8. Thatcher, 1969) or near walls (Valle, 1970);has been used as ai index of timidity. Locality of ambulation has also been used as a measure of interaction with either inanimate objects or other subjects. Fox and Spencer (1969) measured object interaction by the frequency and duration of activity occurring within the same square as the object. In addition to these measures, McCall, Lester, and Dolan, (1969) noted any qualitative difierences in the animals' responses to the objects. The-w included the approach behavior t o the object and the exploration oi the object itieli. Where conspecifics have been used instead of inanimate objech, measures of "affiliation" (Latank, Cappell, & Joy, 1970) hare been obtained by scoring the average distance between the animals and the time spent in direct contact with one another. Activity can also be scored by it; absence. Here the two major parameters are idenrified by.the terms latency and freezing. Laten? is measured by the time taken from the start of a trial to the occurrence of a certain tvoe of <. behavior. Theoretially, h e latency of an arbitrary amount of any dependent parameter might be used, but open-field studies have mercifull!, confined themselves to a relatively m a l l number, usually involving ambulation. Most commonly, latency to leave the start area has been used (I~insb-is,1363; Poley & Royce, 1970). However, laten? to reach the center from a peripheral starting

487

position (King, 1970) and laten? to reach the periphery from the center (Tobach, 1966) have also been measured. The other open-field parameter measuring the absence of activity is freezing, defined as the absence.of movement. T i is a widely hs used parameter usually taken as indicative of a high-stres state. Certainly it is a behavioral response which occurs across the phylogenetic scale in the iace of perceived danger; elements such as abrupt change,. environmental dislocation, physical restraint, and presence of predators are patticularly potent eliciting factors. In the open field? freezing in response to stimuli such as the above shows a marked species specificity and has been recorded as sometimes lasting for over 1 hour. I t has also been found to be associated with marked tachpnoea, bradycardia, and vagotonic cardiac arrhytbrnis (Hofer, 1970). Another cause of prolonged immobility is of course sleep, and the not infrequent occurrence of apparent sleep has been noted b y Fox and Spencer (1969) and Cummins et al. (Note I ) . Fox and Spencer observed that dogs liable to apparent sleep were extremely inactive and that they would often defecate. urinate,. and shiver when placed in the start box. Once apparently asleep they were easily roused by a sudden-noise but rrould then appear to promptly fall as!eep again, and the authors suggested that this might possibly represent displacement sleep as a result of intense arousal. Similar apparent sleep has been noted i n r a t s by Cummins et al. (No:e I ) , sometimes associated withapparent shivering, which might actually be a result of the marked tacbypnoea.observed in subjects during immobility (Hoier, 1970). Against the suggestion of this apparent sleep being the direct result of h>perarousal is the fact that i t s frequency increases with increasing time elapsed within and between trials. This time course is more in accordance with that o f habituation, and in point of fact, it has frequently been observed that habituation of an arousal reaction may be accompanied by the rapid onset of drowsinw and sleep (see Lynn, 1966, for a review). Paradoxically, a generalized orientation reaction may be easily elicited during this drowsy phase. Subjectively? it seems possible to differentiate the

immobility followingsudden threat from that as the abruptness of onset, wide-open eyes, and muscular rigidity in the former case, as opposed .to the gradual development, closed eyes, and relaxed posture accompanying a p pareni sleep. Perhaps the two behaviors representexamples of the startle reaction and habituation of the arousal reaction, respectively. One test of this hypothesis might be the use of electroencephalograph (EEG) recordiog? since the orientation reaction is accompanied by bippocampal theta rhythms,. whereas hippocampal desynchronization accompanies the startle reaction-an interesting example of electroph~siological data differentiating two behaCiorally similar responses. I n summary then, immobility i n . the open field has been regarded as indicative of high stress hut may actually confound two distinct behaviors. Another widely used measure of activity has been rearing and bas proved a reliable (Itinskis, 1968) and valuable measure. Combined with ambulation it has proved to reflect a stab!e individual trait, "nonspecific excitability level," which has been significantly correlated with hippocampal slow. wave activity. a well as with a wriety of other behaviors. This.measure.aljo displays systematic variations with individual differences in;somatic functions such .as growth rate, body temperature, caloric intake per surface area, qualitative food preference, and endocrine functions ( L i t - & Gollov6-Hemon. 1969; Martinek & Lit, 1969). However, attempts other than. the above to. systematically link rearing a i t h other variables have been rare, and it is most frequently taken at face value as an index of activity. .4s -rriight be predicted, sitling has been found to be more frequent during conditions associated with low levels of activity and to be negatively correlated with ambulation, rearing, and sniffing (Prescott, 1970). A surnmary of the influences exerted by different esperimental-procedures on whole body movement and defecation a n be seen in Table 2. :With the exception of defecation, parameters other than whole body movement have been less closely studied and i n many cases have been cited in very few reports. These
of apparent sleep by such features

include scratching, digging, teeth ,chattering, respiration, electromyograph (E3,lG); digestive tra&t time, cardiac rhythm, and EEG measures. Of these part body movement measures, snihing has been relatively common and bas generally been taken as an index of exploration. It has akw proved a . useful coindex for nonspecific excitability, although a less adequate one than either ambulation or rearing. The terms scratching and digging probably refer' to wentially the same behavior evinced under conditions 01 hard a n d loose flwring material, respectively. Prescott (1970) found that greater amounts of digging in the sawdust floor of the open field were associaled a i t h other evidence of highactivity. states. Teeth grinding was used by Hughes (1969) as a possible indicator of anxiety on the rationale that i t mayrepresent a' '"tooth sharpening defenske behavior." Respiration and E M C were used by Hofer (1970) in her studies of prolonged immobility and have been mentioned previously. Grooming and wushing are terms describing tbe.same be5avior and have been found to be of relatively low reliability (.Ivin!kis? ,1968) and to be negatively related to indexes of high-activity states (Prescott, 1970). Vocalizo!ion bas been taken as another indicttion of distress, and the vocalization emitted on placing an animal in the open field has sometimes been termed distress calling (e.g., Candland & Kagy. 1969). Canaland and Kagy have suggested distress calling a s the major index of emotionality in species for whom the normal indexes of defecation and ambulation are not reliable, such as he cat and domestic fowl, although alartinek and L i t (1965) found hat it was not a reliable measure in dogs. F'osihle p2ramete:s o f autononic nenrous svstem function aie legion, but in practice they have been limited to the more easily measurable ones oi excretory and cardiac iunction. Defecation, the parameter for which the oppn field was designed, remains as one. if not the most widely used, measure and remains as the prime index of emotionality, a role whose validity has been confirmed by factor-analytic studies (\\limbe? & Denenberg, 1967). A related, but uncommon, measure is digestive transit time, defined as the

OPEN-FIELD 'TEST

489

timeinterval between consumption and first appearance of a fecal staining ageni such as chromic acid. hrot surprisingly, digestive transit time and amount of defecation would appear to be negatively correlated. These two parameters have been used by Tobach (1966) to demonstrate that open-field testing elicits a significantly greater effect than the manipu'lative procedures involved prior to actual testing. The third excretory measure, urinition, has been scored by frequency, presence or absence, or amount and has occasionally been combined with defecation to yield a composite elimination -score (Tobach, 1966), but in any form has failed to yield reliable resullr in a variety of species (Ivinskis. 1968; hlanosevitz, 1970; Martinek 8: Lat, 1969). Cardiac measures have been used litge eycept by Hofer (1970), whose study has previously been mentioned, and by Candland and N a p (1969) in an atttempt to validate the use of the two most commonly used indexes of emotionality, irAbulationand defe-' cation. The C F E strain of rats were exposed to the open field for 21 minutes for 30 days and compared with home caged animals. Cardiac rare and defecation were greater in the open field, but whereas defecation declined over trials, there was no similar adaptation of cardiac rate, although the rate did fall within irials. Furthermore, there was no significant correlation between heart rate and defecation, s that although both changed in o stable fashions and were both considered as indexes of emotionality, they changed' in largely independent ways. Recent years have b e y n to see the application of physiological techniques to the open field, a'movement which would seem to have immense potential for expanding the =ope of studies of reactions to novel environments, for behavioral-physiological correlation! and for validity testing of parameters and behav; ioral constructs. The examples of respiration and cardiac rate have prevjously been discussed, which leaves biochemical and electrophysiological parameters. of The number of biochemi~al.~arameters potential interest is boundless, but studies' have a s yet been largely restricted to assays of adrenal function. This interest stems from the long-held view of theinterrelatedness of

adrenal gland function and emotional behavior. However, studies have shown little relationship between open-field behavior and adrenal weight or stemid output, and a yet s adrenalectomy bas yielded inconsistent or negative effects in t h e r a t , mouse, and hamster (Fuller, Chambers, & Fuller, 1956; . Moyer, 1958; Paul 8: Ravlena, 1962). Pare and Cullen (1965) were unable to detect consistent relationships between adrenal ascorbic acid levels and open-held behavior, and similar negative finding5 were reported by Ader (1969) for plasma and adrenal corticosterone in hooded and albino rats. Furthermore, although there was a significant effect. across trials for mbulation, defecation, and latency, there was no such change in plasma corticosterone levels smplpd 1 5 ininutes alter each test. Ader concluded that Lhe d a t a p r o ~ i d e d evidence lor a relationship between no open-field behavior and adrenal function. In contradistinctinn to this is the report by Levine, Haltmeyer, liaras, and Denenberg (1067) of greater plasma corticosteroid levels in nonhandled than-in handled.subjec& I5 minutes after testing. There was no change. however, in these corticosteroid levels across the 4 days of testing, and the immediate postt e t steroid' levels did not differentiate Lhe two treatment p u p s . This difierence in ability of the steroid levels to.differentiate the handled and nonhandled subjects at 0 and 15 minutes after testing can probably be explained in terms of the differences which Levine has consistently noted in the time course of adrenal response in these two poups. However, plasma corticosteroid levels also failed to differentiate between enriched and isolated C57BL/6J mice or to correlate w i t h defecation or adrenal weight changes in a study by Denenberg, Wehmer, Werhoff, and f i r r o w (1969). I t would therefore seem that plasmasteroid estimates represent a potentially useful tool but that their relationship to other open-field measures is as yet unsettled. Future studies will probably require = temporal analysis of the adrenal' response after testing, rather than the simpler but less informative method of sampling only immediate or maximum (appmldmately 15 minutes after testing) levels.

lndclendrnl rarlsblc

Study

Increased npenficld size

Increared illumination

Broadburst (1957, 195Sa, 1958b) Oldham 8; hlorlock (1970) hlontgomcry (1951) Elmadhunt (3957) h'ao 8; F o r a t (19i0) Ulizord (1971) R ~ i a k Janku (1971) 8Oldham 8; hlcrlork (19i0) Naby & Forest (19i0) Nagy & G l m r (1970) h'ngy & Holm (19i0) Rlimrd (1971) Vnlle (1970) Livrsey 8: Eggcr (1YiO) hlcClearn (IYW) Diran 8; Eldries (1968b) Cnndland 8: Nagy (1969) NOW 8: Clarer (1970) Ilindm (I. Spinner (10%) Livesev 8: Emcr (1970) . . Hofcr 119i0)Cumrnins, \Val&, & Budtr4lsen (Sote I) \\Inittier & >lcReynoldr (1965) !%tinder ( 1 x 0 )
'

Rnt Gerbil Rat >louse Gerbil hlouse

tlelecation Defeatinn hmbulation hmbulation :tmbulitinn Defecation

'

0 0

1 i i
7
f

0 0 0

Rot

Ambulation An~bulatian

1 1 1 only alter 24 days 01 age

1 only on
I

>louSe

1 albinos more Lban pignlcnted

I albiios more than pigmented

Dnys 1 and 2 in 1W- but not jOdny+lds

Environment noise \\'bite noirc hl,rupt noiw

Rnt Rnt 3louse (freezing) h s t i o n of ambulstion

u 1

Odor

Rot

f ambulatiun in n r w in which prior subjects had b m ~ u lnlrd : s b v e i u t ~ignificant only lor m a l n preceded by k femnles "Caretaker ellec1"-time spcnl on side of o l r n field nearest to P familiar caretaker

Subjc~t

P~r~melcr
'

Ellecf

Invatrial tmparil nnalgsis

'

Broadhunt B; Eywnck (1964) C u m i n s , \:& \a, & Budk-Olsen (Sate 2) \Vwds, Ruck&haur, & Bowliog (19fLI) Oldhnm gi hlorlock (19iO) Cmdland B; Nagy (1969) Collins (1966) Nogy b- C l w r (1970) Branstein (1972) Broadburst (1969) Cummi-, Wnlsh, & Budk-Olsen (Note I) Furchtgou, \Vcchkin, & Dees (1961) Ader (1969) Ehrlicb & Burns (i953) hlanoscuitz (1YiO) h R a r t a & \Y&e (1971) Diron 8; Defries (1%) Nngy & Holm (1970) h'agy & Clarer (19i0) Adcr (19C9) Brmdhunt & Eysendt (1964) Cumnlinr. \Val&. & Budtr-Olwn &ole I)

Rat Gerbil Cst nlouse Rat

r\mbulntion

Def-lion

I - q u a d n l i c !rend I~uadrntic trend I-liner trend !-linear Vend 0 change--nmbulnlion described a nancxplaratory s padng f a c m sir trials, in\.ertd U over 10 days

I I 1 from nu). I to Dny 2

Pcrret hjourc
I

but then f

Ambulnlion

1 across triall I ~ C T O I S trials

I linmr trend I q u a h t i c trend 1 quadratic trend

0 Cat Domestic fowl 0

!across trials 1 a c r e s trials' 1 across trids

! Lath studies shot\. reliable ! individually specific mler

af d c c r u r e across trials

.
.

492
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ROGER X. \ V U H LVD ROBERT A. C U l n f N S

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'

odd-even correlation. Scores were summed across Days 1 and 3 and across Days 2 and 4 and correlated for both strains separately. Coefficients lor ambulation with both deiecation and rearing scores were .68 or above for both strains, wbile frequency and duration of wahing .were reliable for albino but not for hooded subjects. All other variables failed to display acceptable reliability. Somewhat similar findings bave been reR E r r m n l r v OP OPEN-FIELD VARIABLES ported by Martin& and Ut (1969) in their As yet there have been veq'few study of the long-term stability of individual of the reliability of the many variables in differences in evloratory and other behabior use. This represen& a very disturbing state d Lhe rate of habituation in dogs. ne , sub. of affairs, since unless a parameter can be j & were given , of ,,,inUte.' durashorn to possess a satisfactory degree of reli- tiqn each spread over days and then ability and hence to be a stable characteristic retested in a smiliar manner approldmately of individual subjects or situations, its use- . 300 days later, ~ ~ b ~ satisfacl ~ fubess is almost nil. Fortunately, the most torily smb]e, a i t h the of ambuwidely u . 4 variables, ambulation m d deleca- lation, raing, and snifhng gi\ing the tion, have been found to poacceptable reliability even though snifing alone proved reliability in several species. However, ambureliable, Vdimtion, del&lation yields a complex pattern of test-retest tion, urination, and body (smding, correlations because it is a factorially complex slthng, lying) all proved inadequate. Further. . parameter, loading on both exploration and more, the rate of habituation of the combina. emotionalit?, yet changing the direction of tion of ambulation, reuing, and miffing,gi\.en its loading on-emotionality from positive on Gther by the regresion coefident by Day 1 to. negative thereafter (.\\'himbey 6: relative between and last Denenberg, 1967). \Vhile correlationsof Day 1 on a day, was also found to be hi^ ambulation 6 t h scores of subsequent days - studyof the of habituation has been -are satisfactoq' (about . j ) , they are lower further expanded by it and Gollo\+-Hemon than the intercorrelations between other days. ( 1969), who reported that habituation cumes Ivinskij (1968) studied a, variety of vari- Show dear intrinsic oscillations whose size able5 m w u r e d in several ways. Albino n d a stable individual characteristic.. hooded rats were tested ove'r four daily tnals, The sum of these oscillations has been and albinos were reteste'd in the same way a lobilily rcorc and a correla"on coeficient 63 and 217 days thereafter. I n mamining , 7 7 (!\, = 20) was found when retesting test-retest reliability of variables for the performed after months in a dinlerent albino group, scores were averaged over 4 situation, days, and it was found that ambulation and for ~h,,~, there would seem to be the frequency of both defecation and washing the not only oi the total magnilude yield& product-moment correlations greater but in son,e also for the rate and inIhan .4 ($ < .O1) Over the 217 days. trinsic o ~ i l l a "of habituation of certain ~ ~ ~ frequent). of rearing, latenc?l to leave the . beha\iors. ~ ~ b ~ lrearing, iand deieca~ t ~ ~ , center d r d e when initially placed there, and tion would seem to adequak duration of washing all yielded coefficients while urination, snihg, body position, and of .34 (p < .Oj) or above. This left all three . measures of urination (frequency, presence or ~ n n e r circle ambulation would seem to be absence, and amount in ,,,illigrams),,duration definitely inadequate; and a number of 01 rearing, and inner circle ambu~a~ioo t . others, such as washing and latency to leave n h i very low and quiie nonsignjti-t correla- the central circle where initially placed, must tions. A further test dFas provided by an be viewed as only marginally reliable. H o a Possibly el~troencephalographic measures represent some of the most uselul and fascinating parameters of the future. .As yet they a r e a novelty, but the succes of the CzechoslovaL5an workers L i t and Gollovi-Hemon (1969) in relating bippocampal theta activity to behavioral open-Aeld measures augurs well for this and other electroencephalography.

were

,,,

OPES-FIECLD TEST

493

ever, these few variables represent less than a Lhird of those reviewed in this paper, so that i t is obvious that most of the remainder must ar y e t also be viewed with suspicion. I t is interesting to note the apparent strain differences in the reliability of the washing measures. (I\inskis, 1968) ;which suggest that due care must he exercised in extrapolating the reported reliabilities to subjects of other genelic and experimental backgrounds. Also interesting is Itinskis' finding that different m w u r e s of the same bebavior.gave comparable coefficients. I t is disturbing to note the unacceptably low reliabilities of many of the parameters which have been tested and to reflect on the probable unacceptability of the reports employing them. These low reliabilities may partially account for the plethora 01 inconsistent findings which fill the literature.

-. ,.
1

TE~OIUL ANALYSIS OPEN-FIELD OF B~mt~on

I t was mentioned in the discusion on techniques that testing may consist of more than one trial and that these trials may be subdibjded into intervals, thus alloving temparal analysis and effectively adding another dimension to the behavioral study. Many workers measure only total behavior per trial or even total behavior over all testing. This failure to perfom1 temporal analyses within and between trials efiectiuely coll3pses results across two dimeasionsand hence the worker tends to view behavior as static rather than as constantly changing, as an event rather than as a process, and partially ignores tbe efiect of prior exposure to the apparatus. 1n so doing, the analyses must result in a diminished sensitivity, since the subjeclrc may difier in their behavior only at certain phases of testing. The failure to periorm temporal analyses also results in the dijcarding of an immense amount oi information includine the possibility of studying the na:ure, rate, and lability of habituation-characteristics aha% individual stability and imporlance hare been clearly demonstrated ( L i t 8. Gollovi-Hemon: 1969; 3Iartineli gi f i t , 1969j. Occasionally where an experiment calls for the manipulation of multiple independent 1.ariables: the diiwrding of temporal analy~esmay wnier

some advantage in obviating the difiiculties of interpreting higher order interactions, but against this must be weighed the disadvaot a g s listed above. Intratrial temporal analyses have b e e n l w frequent h n those across trials and have largely been..limited to ambulation. The general pattern for a variety of species seems to be a decreasing frequency of ambulation across i n t e n d s mithin trials. This decreased rate may either remain approximately steady (linear trend) or diminish exponentially from an initially relatively high value (quadratic. trend). The latter trend has been reported in both male and female r a h of the hIaudsley Reactive and Nonreactive strains by Broadh u n t and Eysenck (1964) and in young \\'bite Legborn (GoUus domeslicrr~). The former linear trend has been noted by Oldham and Xforlock (1970) in Mongolian eerbils and in Sprague-Dawley rats (Woods, Ruckelshaus, 8. Bowling, 19.60). Studying \ c u l i u t i o n in the cat, Candland and Nagy (1969) found differences in intra-, trial trends to be a function of age. Kittens showed a marked intraswional decline over 10 minutes'but did not reach the considerably lower levels of the adult cats,. whose vocalization diminished only slightly. In v i e t ~ of the absence of defecation and the apparently none.~loraton. nature of ambulation (subjects paced backwards and forwards near .the unit door without any apparent exploratory intent), the authors suaested that vocalization might yield a better index of emotionality in this species than the traditional measures. Studie~ across trials hatre been more extensive than those witbin trials. The varieties of satistical analysis are of course limited by the number o i triali. The simplest and most common analysis has been determination of the sienificance level of intertrial diiferences. .9 more inlormative metbod is trend analysis, and'where several trials are used, i t is possible to examine not only the general trend but also the nature. magnitude, and periodicity of trend Euctuations. Once again ambulation has most often been studied and a variety oi patterns has been noted. Consistency has been greatest in the

>

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49.1

ROGER

N.

WALSH A m ROBERT X

A.

CUMMISS

mouse where the majority of workers have reported decreasing ambulation across trials. This has. been reported as a significant, efiect for subjects reared under enriched and standard colony conditions (Manosevitz: 1970), in small or large litters .(LaBarba &! iV%ite, 1 9 i l ) , and for B.ALB/c.J and CS7BL/6.J inbred mice and their reciprocal F 1 hyhrids a t sevcral aTes (Dixon & Deiries, 1968a). Ambulation decreased across 4 days in handled and unhandled C3H .mice tested under high or low illumination a t 50, 70, or 100 days of age ( N a p & Holm, 1970). This report furnishes an example o i the added sensitivity and information afforded by intertrial analysis, since although the main effect for handling was not significant,. a number of its interactions with trials were. Thus, 50day-handled subjects were more active than controls.on the first day, but their ambulation decreased more rapidly such that i t was less than Lhe controlj on Daxs 3 and 4, and this pattern was different a t the three ages. Similar examples are available in the study of Nag? and Claser. ( 1 9 i 0 ) , who demonstrated a significant (apparently asymptotic) decline across 10 days in C57BL/6.J mice. Less consistent results have been obtained with the rat, although a decrease across days . has been most often reported. This has sometimes been linear (Ader, 1969) or apparently quadratic (Broadhurst 8: Eysenck, 1964) where a decrease was reported f r o m D a y I to 2 which was partially recouped on Days 3 and 4. Broadhurst $nd Eysenck 'hypothesized that inhibition may account for the initial intertrial reduction as well as the intra. trial decline already discussed, while reduction of fear m a i account for the i n c r m e in ambulation across Days 3 and 4. The rate of decrexse washeightened by prior rearing in a complex environment, a finding attrihuted to a more rapid habituation of the arousal response to novel stimuli (\\'alsh 6Cummins, in press; Cummins et a]., Note 1). Barrett and Ray (1970) and VaUe (1971) found that young r a t s become more active across trials, but other workers have found no significant intertrial chanze (e.g., Furchtgott e t al., 1961 ). Thus, every possi-

ble change--increase, decrease, or none-has been reported. Other s p m e s have been l e s closely studied. I n the dog! Nartinek and Lit's (1969) find-ins of individually reliable d e c r e a in ambulation across trials has already. been discussed, but Fox and Spencer (1969) found that exposure to the field some weeks previously resulted in modest increases. Xeither kittens nor adult cats displayed any significant change across 10 days, while. the domestic iowl showed a dramatic i n c r w e in spiie of consistent decre& within trials (Candland &! N a p , 1969). Latency to leave the starting .unit wass found to increase across 3 days in rats of various ages (Furchtgott e t al., 1961). A more complex picture aas noted by Ader (1969) when latency fell markedly from Day I t o 2 but then increased slightly over the' next ? days. Latency declined-across 5 test days in ferrets (Ehrlich k Burns: 1958) and there was a similar trend for both rearing and scratching, while vocalization declined over 6 days in i d u l t cats but not in kittens (Candland 9 Kagy? 1969). On the . other band, snifing by rats increased across 3 days, Lhough this was dependent on the age of the subject (Furchtgott e t al., 1961). Cross-trial studies of defecation have been almost entirely limited to the mouse and the rat, and once again only three or four trials has been the norm. However, within these limitations there would seem to be consistent evidence of species difference3 in trend, i o r n,hile the rat shows a l e w n i n g in deiecation across days (a pattern that has beenaccepted as the norm and the basis for hyptheses building both within and betueen species), the mouse displays the opposite trend. This decrease in the rat has been widely reported,. thought not without exceptions (Ader, 1969), and has been confirmed over as many as 60 trials (Bronslein? 1972). Furthermore, this decrease has been s h o r n by Broadhurst (1969) to have a d e a r genetic-component with a high average level of dominance, with the s u ~ e s t i o n that natural selection will tend to favor low-scoring strains resistant to change across trials.

OPEX-FIELD TEST
.

495

For the mouse on the other hand (practically. the only other species for which evidence is available: indicating the reliability of the defecation measure), there has been a high degee of consistency btween reports on intertrial trends. Thus, defecation has been found to increase across as many as six trials (e.g., Collins, 1966). These studies afford an interesting example oi the oversimplification which may result from taking a relatively small number of levels of any factor under investigation, for when the number of trials KU increased to. 10 (Kagy S. Glaser, 1970), i t was found that the trend could now be identified as an inverted U with the number of boluses increasing through to Day 6 followtd by a decrease over the remaining 4 days. The marked consistency existing between studies of intertrial changes in defecation has recently become explicable in light of a quantitative genetic analysis of openfield behavior in mice by Deiries, HeLpan, Ross, and Howard (1969). I t was found that change in defecation displayed as high a degree of heritability as did the daily and total scores:In spite of a similarly hish consistency between reports on change in mouse ambulation, genetic influence on change in this measure was found to be considerably less than for eith-r daily or t o h l scores or ior any of the defecation scores. Interpretations of temporal changes in openfield behavior have varied with the paiameter under study and the meaning attached to it by the experimenter.. Thus, for example, the cro%-trial' decrease in ambulation and deiea t i o n in the rat has been taken as indicating a diminution in emotionality, anxiety, fear, w p e attempts, and territorial marking, or at !he more general level: of the development of inhibition or habitualion. However, in conjunction with an!, interpretation must b : an awareness that the placement of a subiect in an originally novel environment must elicit an orientation reaction which subsequently hnl~ituates.One might conceive of this reaction as a high+rder factor in a psychophysiological construct hierarchy, modulating multidetermined lower order constructs such as fear, anxiety. territoriality, and the like. a,hicl~would in turn modulate the even more

overdelemined spedric behaviors observed in the open field. The precise nature and maggitude of the changes in these bzhaviors will of course be determined by the geneticexperiential background of the individual, but any attempt to esplain temporal behavioral changes must certainly incorporate the concepts of orienhtion reaction and habituation.

I t has long been known that many dependent variables in the open field correlate significantly with one another. This is all the more to be noted since some positively correlated behaviors are mutually e~clusi\.e (ambulation and rearing) and hence their .degree of relatedness is presumably underestimated by simple correlation. A basic deduction from these correlation studiff has been that many parameters tend to measure t h e same psychophysiological -state and as such have provided several useful implications. First, such correlations allow for validity testing, since the patterns oi behatior serving as a s u y s for altered psychological states should be predictable under diverse conditions. Second, they may afiord an increased sensitivity and reliability of measurement. At the same time, they may also allow an economy of measurement because where parzmeters are highly correlated, one may well dispense with some of them. Thus, L i t and Cmllovi-Hemon (1969) were able to dispense with measures of snifing and deaning in the knowledge thzt a weighted sum of 3mbulxion and rearing would still yield an adequate correlation a i t h hippocampal them activity. Not surprisingly the correlation between ambulation and defecation scores has most often been studied. Since Hall's (1936) report there has been a high degree of consistency in the literature affirming a negative relationship between these measures in the rat. In the mouse a similar trend has most often been noted! and this in spite of the previously mentioned increase in defecation across davs. More detailed s t u d i s in this. species, however, have begun to reveal some of the complexity of the relationship, and

496

ROGER N.WALSH .Ah73 ROBERT A. CUMhfISS

in a diallel study, Bruell (1967) found a positive significant correlation (r = ,124) in males, a i t h a negative and equally significant correlation ( r = -.I 59) in femal6.s. The relationship has been less frequently studied in other species ,and .has almost always yielded nonsignificant correlations, espedally for $ecies in which defecation bas been found to be an unreliable measure (e.g., Candland & S a g y , 1969). I n the vast majority of cases, correlation has been performed between scores totaled over aU trials. However, considerably more light h a been afforded by recent studies which have examined the relationships between scores obtained on individual trials. Nagy and Glaser !1970) divided C576L/6.J mice into high and low ambulators and studied the cross-trial patterns o i defecation under a variety of ages and illuminations. High and lorn ambulators did not differ in defecation on Day 1, but thereafter the low subjects defecated significantly more; and their defecation continued to rise until declining from Day 6, whereas high ambulators defecated man'mally on n a y 2. Meanwhile, ambulation decreased steadily in both groups, suggesting that the correlation is not asimple one and afiordina another example of the 1 0 s of information contingent on failure to perform temporal analyses. As might be anticipated, the various measures of motor activity tend to be positively correlated, even in cases in which the behaviors tend to be mutually exclusive, ris with amhulation and rearing. These two parameters have been found to be highly (up to 3 1 ) correlated in a variety of rat strains (e.g., lvinskis, 1968; Ray Fc Hxkhauser, 1969), although Delbarre et al..(1970) have noted a dose;dependent, pharmacologically induced dissociation between ambulation and rearing. Since the definition oi latency usually involves the ahsence of ambulation, i t is not surprising that these two measures have been found to be negatively correlated. This has been widely reported for both the rat andmouse, and both parameten have been found to load on common factors hut in opposite directions--namely, exploratory behavior in

the rat (Denenberg & Wlimbey, 1968) and on a factor which was unnamed and uninterpreted by the authors in the mouse, but by analogy with studies on the rat would seem to represent a factor of emotionality (Poley 8. Royce, 1970). Correlational studies of ambulation with oLher variables have been less frequent. Ader's (1969) use of corticosteroids has already been mentioned. A negative correlation with urination, just significant a t t h e .O5 level, was reported b y Satinder (196S), a doubtful finding in view of the demonstrated l o r reliability of urination measures; Similarly, ambulation displayed a sipificant positive correlation with inner circle actitity in spite of the latter's demonstrated unreliability (Ivinskis, 196s). Finally, ambulation and vocalization showed a positive nonsignificant trend in dogs (Fox & Spencer, 1969) and the reverse in human infants (Rheingold, 1969). . s the most widely studied parameter, A defecation has frequently been used as a co;relate. The negative correlation a i l h ambulation has already been detailed. I n view of the ncative correlation of ambulation and latency, i t might be anticipated that defecation and latency would he positively related, but in the main 'only nonsi~nificant trend< have been found (e.g.. Ader. 1969: Porter Fc Wehmer, 1969). The lack of correlation uith changes in heart rate (Candland & N ~ F , 1968) has already. been mentioned: while Satinder (1968) reported a n q a h v e correlation Kith grooniin~ over four trials. .A logical extension of intercorrelating openfield variables is the study of their relationship to measures obtained on other behavioral tests. Such correlations may afford the advantages previously mentioned of increased sensitivity. reliability, and economy a well ? as providing valuable information on the apparatus specificity of aqv apparent relationships. Perhaps the best example o i this specificity is afforded by ambulation. Thus, although some workers report good correlations between ambulation scores obtained in different apparatuses (e.g., ambulation in the open field, endosed maze: and an exploratory box [Stretch, 1960, cited by Broadhurst & Eysendt, 1964]), most have not been so en-

OPES-FLELD TEST

497

thusiastic. Particularly common have been studiff of ambulation a s measured by activity wheel and open field. These studies have yielded consistent reports of significant but not particularly high correlations (Manosexitz, 1970; Weasner, Finger, PI. Read, 1960; correbtion coefficient of .41). Considerahly lower correlations have been found where motor activity is measured by cage tilting or stabilimetn.. Here i t is obvious that the highly coordinated motor wheel activity may be only slightly similar to the multitude of part and whole body movements registered on the stabilimeter. I t should be noted that even simultaneous measurement of motor activity may yield relatively low correlations. Thus, simultaneous mex?urement of total open-field activity over 30 minutes gave coefficients of .65, .65, and .49 for cage tilting- beam interruption, cage tilting- flwr contact, and heam interruption- floor contact, respectively (Sparks 8: Lodiard, 1966). Openfield ncliuiry is sometimes used synonynously with ambuhtion, but in \iew of the term's varying usage by different workers and the relatively low correlations above, it is best avoided in this contest. Ambulation h3s also been found to be correlated .+th m w u r e s whose ambulatory nature is less obvious. \Voods, Ruckelshaus, and Bowling (1960) found significant correlations of the Hebb-\Villiams' maze error ambulation in rats reared under scores ~ 4 t h free or restricted eovironments. They therefore suggested that the often reported finding of lower error scores on maze and discrimination tasks in animals reared under conditions of increased environmental complexity might be due to a reduction in conflicting exploratory tendencies rather than to an increase in learning ability per se. This sugests an a yet apparently untried u u g e of the open field, that is, the use of one or more of its parameters as covariate adjusters in cases in which related behaviors are believed to be confounding variables. Thus, in the above study the u s e o f ambulation as a covariate oi error scores might yield a clearer pictuk of the origin of the error score difference. Satinder (196S), using measures of ambulation, defecation, urination! grooming, and

rearing, found little relation to conditioned escape avoidance behavior in the rat except for positive correlations of avoidances and intertrial crossings m'th ambuktion and a negative relationship between intertrial crolsings and defecation. L i t and Collola-Hemon- (1969) have described the relationship of their previously described open-fieldderived m w u r e s (nonspecific excitability level, inhibition, and lability) to both behavioral and physiological measures. Thus, a n analysis of individualdifierences in learning a double-T maze revealed h t these three factors accounted for a major portion, of variance on measures of learning, running time between starting box and first r u n m y , and decision time on choice points. Furthermore, nonspecific excitability level was found to van. systematically with indiridual diiferences in such diverse physiological m a ures as growth rate, body temperature, caloric intake, qualitative food preference, and endocrine functions; a a i d e range to be sure and an interesting example of what will hopefully be one of many demonstrations of physiological substrates of open-field behavior. In view o i its multiple intercorrelated raria b l s , mosi of &em oi doubtful meaning and their correlations with variables obtained in other tests, the open held would seem to lend itself ideally t o factor-analytic studies. Indeed, such an approach mould seem to aflord an optimal method of interpretation and de-' termination o f the factorial structure of openfield behavior, yet such itudies remain a rarity. Since it furnishes an excellent example of the potential of this method? the study by \\?himbey and Denenberg (1467) is described in some detail. IVistar rats were assigned to one of 1G treatment combinations that resulted irom completely crossing four independent e.xperiential conditions, each at two levels, yielding a 2 :< 2 X 2 :< 2 iactorid design: The four variables a c r e handling oi the subject's mother during the latter's infancy, handling of the subject during infancy, housing o i molher and young betureen birth and weaning, and, finally, housing ior the first 21 days after weaning. Commencing a t 220 days of age, scores were obtained on a numhzr of widely

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ROGER S . \ V . U , S H ASD:ROBERT ,A. CL;M>iISS

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used :measures of exploration, emotionality, avoidance learning, consummatory behavior, and- the. Like, yielding a tntal of 3.7 scores including open-field ambulation and defecation on Dags I-4-and a f i e i a n intervening period of testing on several other apparatuses, on Day 14. Outstanding feature of theanalysis were the relatively l o x correlations of the first day's ambulation score with those o i .other da-s and the positive coirdation di Day I ambulation w i t h a l l defecation scores -in-cnmpsrison to the negative currelations of ambulation on other days. The two orthogonal factorsacco'unting for most' o f . t b e variance of Lhese variables were interpreted as cmotional reaclivily and cxpforation. Defecation loaded only on emoliond reacliaily. whereas ambulation proved factorially complex, :loading positively on . czplorution but changing i t s loading on emotional reactkit? from.positive on Day 1 to negatirre for other days. I n addition, defecation was found L o load on a Lhird factor wGch was named consummation+limination (Denenberg, 1969b). T h e factorial complexity-of the ambulation score Frovidcs, for the firs: time, an explana. tion f o r w m e of the lar'gedumber of contrad i c t o ~ f i n d i n g sand interpretations of .this -parameter. Ambulation: has f o r . many y a r s been the traditional memr-e of rat exploration, while others h u e used il (sometimes in conjunction with defecationbut sometimes not) as an index of emotionality, fear, or escape behavior. It can. now be seen that it may-well he indicative of esploration as well as .either high or low emotionality but that intekpretation i s next to impossible where only one trial is e'ven and the information from deiecation scores is not taken into account. I n view of the similarity of the withinto the between-trizls decline in z m h u l a t i ~ n in the rat, i t i s interesting,to speculate as to whether there might be a similar reversal of loading on emotionality within trials, especially for Trial' 1 . T h e advantage conferred by the finding.that the two major parameters of the open field' load well o n these two important dimensions of animal behavior is immense, but i t -must be noted that the generality of this finding for other species and strains, for different experiential backgrounds,
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and for different .test conditions remains unproved. One has only to remember the inc r k n g defecation across. trials iound in the mouse, as compared w i t h t h e decrease o f . the 'rat, to realize the relevance of these. qualifications.

\\%at then are the iactors determining t h e qualitative and quantitative nature of be: llavior erjnced by a subject in the "pen field? Basically, & is true: of any behavioral test, this behavior represents the interaction of the suhject with the experimental situation. This concept of operationalism, that is, t h e interaction between that which is measuring and that which is being measured &d the inseparability of the properlies and efiectj of one irom the other, might well be extended from physics to the behavioral science. Furthermore, each o i these factors influencing bebavior may be divided into interacting subcomponents which of course may he iurther subdivided ad infiniturn. Division will mainly be carried only to the first stage in this study: since it is a t this level o i behavioral de:ermination which most open-field studies are concerned with and because of the incresing complexity a n d diminishing returm trhich iurther subdi\ision brings. Sutject,variables are perhaps best clavified under genetic, developmental, and experien.tial headings. Genetic c o m p n e n b of species, 'strain, and sex are most often discussed. Developmental features usually refer t o the physiological maturation procwes, but o n e might subsume biological rhythms under this beading. .E.xperiential variables have been c l s i f i e d by a variety o i criteria,. most commonly by the nature of the stimulus and the development phase a t xrhich it was given. For the purpose of the present discussion, the most u x i u l classification is into experience p i n e d prior to testing, manipulation of the subject involved in bringing it to the expe~imental situation, and e.rperience of the experimental situation up to the instant a t which hehavior is beine measured. -. Some idea o i the interactional tornplexity of behavioral determination may be gained

:*.L

;.,

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from looking at studies which have simul- mental situation, stimulation afforded by the taneously examined the effects of several vari- experimental apparatus, stimulation afforded ables from just one of the above divisions. by the test environment, e . ~ r i e n c eof the Denenberg and his co-workers (Denenberg, test situation up to the inrtant of measureKaras, Rosenberg, 8i Schell, 196s; Denenberg ment, and method o f measurement. The imSr Rosenberg, 1963; Denenberg.& Whimbey, plications of this. for open-field studies are 1969) manipulated the handling of the-sub- discussed below but may also be generalized jects, their pretieaning.and postweanins en- to other areas of behavioral research. This interactional n a t u r e o i the behavior vironments, using both male a n d female Wistar rats and found. a significant four-way places severe limitations on the extent to interaction among all variables o n open-field which generalizations czin be made from the results of any individual esperiment. I t also . ambulation. Coming now to the test situation side of increases the potential importance of changes the equation, Lhis may be divided i n t o the in any one factor 01 the interaction equatest environment and measurement procedure. tion, so that apparently Lribial alterations of T h e test environment. has previously bcen any one stage of the chain reaction may reconsidered in some detail under the headings sult in totally unexprcled changes in hebavTechniques and Apparatus Characteristics, ior. The importance of this for coniparisons T h e Testing Environment, and Procedural between treatment groups rests on the differDetails. The nonequality of results,obtained ential efiects of any 'changes. hleier (1963): by difierent methods of measurement of sup- in discussing the conditions which modify posedly the same behavior has a h previously behavioral development, has stated: been mentioned? and interactions between Thc rondilions that have been drrcribed (c.8.. treatmqnt and measurement techniques are handling, Litler sire, malcroal w a i n and prepartal well known in the literature. Such an inter- cxperirncc, cage sire and complexity. lo name a action was remrtrd bv IVeasner et al. (19601. f r w ] . wcrr ~ r e v i o u s l y releqatrd to the groccles demonstrated that' photoelectrically reg. limbo a: m i n t e n a n t e routines .which s e r e inire2nd codihed, and even then ior istered home-cage ambulation and revolving- quentty recordedlocal conrumplion. Now we rcaliur only limited or wheel counts yielded different results for that variablrs are in their poteoo. equivalent treatments. In comparing such t o cffrrt behavior change that is drmonlrable for measures of behaxior obtained by-difierent prrio& often a t e n d i n g far into adulthood. \Ye tffhniques, there are several factors to be canno: help hut wonder how many of the nowc k i c controrersie in the behavior sciences could considered. First, there is the question of .,,be rewired were detiled information availtibether the behaviors being measured by able on the maintenance routines employed by L ~ each method a r e in fact thesame. Presum- protaaonisls in thore controversies. (P. :7) ably they can never be identical; the study 4 note of despair. has been c a t by of S p a r k and Lockard (1966) using cage Henderson (1970), who stated "for the time tilt, beam interruption, and floor contact m w u r e s of activity afiords a gross e m p l r being investigators must be aware of the posof this. Second, there is the queslion of dif- sibilities that early environmental interactions ferential sensitivities of techniques,. as regards nith cenotype may limit the validity of their bolh ~hresholdand sensitivity to increments Findings to their OUT unique laboratory situaof behavior. And third, turning full circle: ' t i o d ' (p. 509). This statement stems from there is the matter of interaction b e t ~ e e n the author's work on effects of genetic and early environmental interactions on a number the subject and the measurement apparatus. of subsequent behaviors (Henderson, 1963, The concept of operationalism fits well here. 1969); including open-field defecation, in In summary then, any behavior represents which it was obvious that there tias no single the determinant o i the interaction of genetic relationship between prior treatment and badground, maturation, biological rhythms, subsequent defecation across difierent mouse experience prior to testing, stimulation in- strains. >foreover, this is only one of the volved in bringing the subject into the experi- posible 72 one-way, let alone multiaay,.inter'

widespread ignorance of the ethologid significance of much behavior studied in laboratory situations (Henderson, 1968). . The construct of emotionality bas been the major one for open-field work. Although rarely defined except in circular operational t e r n (Denenberg, 1969b), i t can be thought of as an entity underlying the nonspecific affective components of behavior. We say nonspecific components because. an. adequate stimulus and appropriate goal-oriented behavior cannot be identified, although anthmpomorphic. analysisor experimental manipulation suggests the presence of a n aiiective state (Ader. 1969). ii'hile initially b a e d on anthropomorphic interpretation, the construct has been factoridly validated (Zi'himbey 8: Denenberg. 1467). .%lLhough Ridely ajsumed to underlie a large number of behaviors, factorial loadings have as yet been demonstrated only for defecation and.ambulation. Ilinskis (1970) attempted to test the validity of deiecation, an~bulation,latency, rearing, aashing, inner drcle activity, and urination as indexes ol emotionality in rats..His criteria of validity were, first, intertrial decrease of scores acrosr, 4 days; second, efiects 01. prior openfield testing to reduce scores; and third, eifects of alterations in anibient auditory and tisual stimulation. The adequan. of these criteria would seem to be debatable, and in iact Ivinskis concluded that ol the three, only stimulus variation was satisfactory. Using this criterion, of the seven parameters tested, be only t w d e i e c a t i o n .and latency-ould considered valid indexes of emotionality. The necesit).. for interpretive caution when using the o~en-fieldtest is even more aDDarent in . light of this study, especially when i t is reINTERPRETATION OF OPEN-FIELDMEASZTRES membered that of these two m w r e s only Ihat t h e n does t h e open field measure? defecation has been found to be .acceptably Interpretation may be in terms of under- reliable (Ivin~lris,1968). lying constructs or on the basis of the behav: Another widely referred to aflective conior's presumed purposi\-e or adaptive nature. struct, which would seem to be ven. d o s e t o Underlying constructs may be suggested by the emotionality, is that of fear. It does not face validity or anthropomorphic interpretation of a particular behavior, by resemblance seem certain to u h a t exent the behavioral to a natural behavior pattern or to other andphysiulogical components of fear can be constructs, or by factor analysis. I n t ~ i t i \ ~ edifierentiated from those of emotionality, and or face validity interpretations have been the the two t e r n often seem to be used synony'norm until verv recentlv:, the diificulties and mously. Since measures of emotionality have , dangers of which are compounded by the most often been obtained in situations wbicb actions derivable from the nine major independent variables listed earlier! As early as 1958, King listed variables likely to be of importance in determining subsequent behavior and pointed to the lack of concern by investigators for control oi variables other than t h e o n e in which they themselves were interested. Today, little has changed except for the enormous r o w t h of the list .of variables known to be important. I t is small wonder then that contradictions and failures of replication abound in open-field and much other behavioral research. -What then cyl be done short of abandoning a nomothetic for an ideographic approach. First, experimenters must bccome a m r e of the nonsdditive nature of behabioral determination. With this in mind: one can see that studies which examine only one factor in imlation are of considerably lesj value than those which permit consideration of a variable in light of the effects oi others. To this end Henderwn (1969) recommended the use of considerably more elaborate multifactorisl multivariate desi.ps than have previously been customary and felt that drawbacks o i size and multiway interactions are a necessary price to be paid if this area is to advance beyond its present limitations. . further need \ . . which will enlarge such designs even more i s the .need for large numbers of factorial levels in view of the nonlinearity of response to s many variables. Furthengore, those releu vant variables not included in the design must be ~ r u p u l o u s l y controlled, and' the leveln a t wbich t h e were controlled must be reported.

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anthropomorphically would seem likely to induce fear, one wonders if there is a n advantage to be gained at this stage by trying to difierentiate them except denotatively in terms of the specific experimental stimulus situation. Specific.affective behaviors and constructs have naturally been rare in view of the absence of adequate stimuli in most open-field testing. However, with two subjects in the field 'simultaneously; the construct of gregariousness has been used to explain differences in average distance between and time spent in contact by the subjects (Latan6 et al., 1970). Exploration has been a much used construct whose prime measure has been ambulation. While this assumption has been validated by factor analysis, its limitations have been pointed out by hIcCall et al. '(1969). Once again, many other parameters are thought to be indicative of exploration (sniffing, rearing, etc.), but factor-analytic validation is still awaited. At the psychophysiological level, arousal-habituation has proved extremely useful, especially in the work of U t and Gollova-Hemon with their derived constructs o f nonspwihc excitability level, inhibition, and lability. One of the' most pressing needs in the formulation of open-field constructs is an increased reporting of validity studies.

have been enumerated already. but their inclusion in a concluding section seems more than warranted in view of the danger of "the growing body of literature in this area suffocating under its own weight" and in the hope of helping to "convert the current paper explosion in this area into a knowledge explosion" ( H e n d e w n , 1969, p. 867). First, with regard to procedural matters, there is a need for a more precise specificstion.of subjects including their genetic background, prior treatment, apparatus, testing conditions, measurement techniques, and temporal factors. Where replication or compari-' son is the aim, all possible factors other than the one under manipulation must be suupulously controlled. ' h regards experimental design, tbere is a need for the recognition of the essentially nonadditive nature of behabioral determination. \Vith this in mind experiments which manipulate only one independent variable would be better replacd by multiway iactorial designs, which because of their economy andnonassumption of additivity yield vastly more information and whose limitations regarding generality of conclusions can be a r s e w d in light of interaction terms. Similarly, there is a need for increased numbers of levels i n factors under investigation. Testing subjects under. light and.-dark tells The erlablishiog of validity u always tenuous, for nothing about the precise relationship bein the long rua validit!: b determined by whether tween behavior and level of illumination the %ajority oi inrrsti~alars,or at least t h c most unless demonstrably untenable mumptions of outspoken, believes the external criterion to hare linearity are made. Similarly, comparing two been adequak. (Candland k Nagy. 1969, p. 841) species or strains tells nothing of the genetic Such has largely been tlie case in the open basis of behavioral differences: whereas an field, but this consensual validity must now approach such as the diallel cross, which afrest on the b g i s of further criterion and fords a large number of precisely quantifiable construct validity testing, for which, in addi- genetic levels, allows very detailed psychotion to the correlational studies which form genetic analysis. Failure to perform temporal the basis of most convergent validity testing analyses of behavior discards large amounts (h'unnally, 1967), factor analysis would seem of information and may result in diminished sensitivity. particularly suited. For dependent parameters, there is a great need for reliability and validity testing for a I t is obvious in reviewing this area that wide range of conditions and subjects. >.Ian? many of the all-too-numerous discrepancies, papers base far-reachinr assumptions and failures of replications, and contradictions conclusions on parameters whose reliability stem from preventable methodological and and validity remain unproven. The wider use experimental design causes. Many o i these of physiological variables, particularly bio-

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ROGER X. WALSH k J ROBERT A. C U J 1 M ~ ' S \ K Broadhunt, P. L. Determinants of emotionality in the rat: I. Situational factors. Bn'tirk Journal of Pryckology. 1957, 4S. 1-12, Bmadhurst, P. L. Detcrminanls of emationalitg in the rat: 11. Antecrdent iactors. British l o u m l of Psychology, 1958, 49, 12-20, (a) Broadburst, P. L. DctcrminanU of emotidnatity in the rat: 111. Strain diflcrcnres. Journol of C m parafiuc snd Ph?siological Prycholo~.~, 1958, 51, 55-59. !b) Broadhunt. P. L. Psychogenetits of emolionalily in the rat. .4nnnlr 01 Ihc Scw York Acodcmy o] Sdmcc, 1969, 159, 806824. Broadhunt, P. L., k Eysenck, H. J. lnterprctationr of erploralory behavior in the rat. I n F I . J. Eyrenck (Ed.), Ezpcn'mcntr inmotivation. Elmsford. X . Y . : Pergamoa Prru, 1964. Bronstein. P. hf. Open fic!d behavior 01 the rat as a iunctian of ape: Cross sectional and l o n ~ t u d i n a l invertigaliozs. J o m l 01 Comparative ond Phyriologicnl Psychology. 19i2, 80. 335-341. Bruell. J . H. Brhasioral hetcrasb. In J . Hirwh ( E d . ) , Brhozior-Gcr.t!ic rlnal?sis. S e w York: n1cCra~-HiJI.1967. Candland. D. K..'9: S ~ F , Z. h1. Thr Open-Field: Some comparative data. Annolr 01 ihc rVew Yolk rlrodnny o! Science, 1469, 159. 831-Sjt. Clark, C.. Gorman, D., Vrrnadlkir, A. EBects o! & p r e ~ a t a ladministration of prychorropic drugs on behavior of d.,,e!oping rats. D~~~~~~~~~~~~ chobioiogy iO, , 2:5-2j5, Collins. R . L. What clw does thc defecation score measure? Proccrdingr of the Aznval Conoentioc of the Am~n'can P~ycholoj-icol .4srodotion, 1966. I , 147-1;s. Dcfries. J. C. H e w n , J. @., Ross, D., b- Howard h1. A gumtirative genetic analysis of change in o ~ field behavior of mice. Ps>,chonom'c Science, n 1969, 17. 152-154. Delb=rrc. B.. Dumas, G., 8. Guionniere. 1 . .an a u t o s a t e d open-fieid method. P~ychophormacologin. 1970, 18, 227-230. DcnenScrg. V. H. Opcn-field behavior in the :a!: What docs it mean? Annals. a the iYcut Yorh ! .4codrmy of Scirnrc, 1969, 159, SS2-859. ( b ) Denncnberg. Y. H.. liaras, C. G., Xmenberg, I . 6 ;, . Scbell, 5. Programming liie histories: An crpcrimenlal d e s i q and initial results. Dcudopmrn!al Pryckobiilogy, 1963, 1 , 3-9. Denenberg. \'. H . , & Rorenberg. I . M. Proqram; minq liic historits: EKrcts of maternal and enrironmcntal variables upon open-field behavior. Dcvelopmeald P r y d o b i o l o ~ y ,1965, 1, 93-96. Denenberg, . H.. \Vrhmer, F., Wcrhofl, J.. B Za:ron,, hl. S . Effects of portweaning enrichment and isolation upon emotionality and brain weight in the mouse. Physiology and Bchmior, 1969. 4.

chemical and electropbysiologicaI, .and the determination of their relationship to behavioral would seem to hold consider; able prom&. ,As regards interpretation of behaviors, there is a need for mnstruct validation' for which factor analpis and ethologiul data would seem to be particularly relevant. The former tendency to regard variable and construct as almost equivalent and constant across subjkts and treatments must be abandoned except where construct validation indicates that it is permissible. Individual dependent parameters shouldnot be considered in isolation but in light of changes in other parameters. This has been demonstrated particularly ior arnbulation. Finally, the dangers' oi unqualified generalization acmss genetic, experimental, and testing backgrounds must be appreciated.
REFEKESCE S O T E 1. Cumminr. R. A,, Vialsh, R. N.. & B u d u - O k n , 0.E. EnvironmenuUy induced cbango in opcnfield beha\,ior. Paw< prc-tcd a t Lhe 44th annual meeting oi Lhc Australian and K e n Z e a l a n d ASOciation ior the .Aduancement of Science, Sydncy, August 19i2. REFERESCES AbeI. E. L. Habituation as a factor in carly handling. J o u r n d of Comporoli;~ and Phyriological Prycholoqy, l F i l , 7 4 , ?IF-222. Ader, R. Adrenocortical function and the measuremen1 of emotiooality. .4snolr of !he n'cw Ymk Acodrm? 01 S d m c t , 1969. 159. 791-S95. Archer, J . Tests for emotionalit? in rots azd mice: A revira. Animal Bthocior, lFi3, 2 1 , 20'135. Barrett, R. J., 8 Ray, 0. S. Behavior in Lhe openfield. Lashley I l l m ; r e , l u t t l e box, and Sidman avoidance as a function of m a i n , sex and age. Dcorlopmcnfal Psychology, 19i0, 3, i3-ii. Battig. K. Drug r6erts on caploration of a combincd maze and open-&Id system by rats. Aznalr o ! the X t w l'ork .4rodtmy o! Sdcnce, 1969, 159, 892-S97. Bindra, D., & Spinner, N. Raponse to dinerent degrcer of novelty: T h t incidence o l various activities. Jourw! of thc Erpcrimcnfol A n a l y k ol Behatior; lqj8, 1 . 341-353. Blirard. D. A. Situational determinants of open-field lehavio; in m u murcullis. Bn'fish Jrmrnol of Prycho!ogy. 1971. 62. 243-252. B&k, I. B.. & Errman, \V. B. C:ou-fh hormone 'administration during prrpnanc?.: A behrviornl diflerencc in oflrprinq rats: Solure, 196j, 205. 11361137.

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&on, L. K., Deiries, J. C. Development of o p n & field behavior in mice: Effects of age and e r p r i en-. D m e l o p m m t d Ps?chobiology, 1965, 1. 100107. ( a ) . D h n , L. K.,& Defrier, 1. C. Effects of illumination on o p n held h h a r i o r in mice. Journal of ComparDlive rmd Phjriological Psychology, 1968, 66, 605-805. (h) Ehrlich. A,, & R u m , S . ErploratoryhebaCior of - the black fooled ferret. Canodion Journal of PI?chology, 1958, 12, 235-241.Eyxnck, H. J., & Broadhurst, P. L. Introduction. In H. J. Eysenck (Ed.), E r p e n m n l r i n molioolion.~Elmslord,N.Y.: .Pergamon Press. 1964. . Fox, hf. W , & Spencer; J. W. Exploratory behavior in the dog: Erperimcntal or age d e p n d c n t ? Dcvrlopmcnlal Psychobiology. 1969, 2, 68-74. Fuller, J. L., Chamben, R . . . & Fuller. R. P. M, EBects of cortisonr and of adreoalcctamy on aclivlty and emotional behavior of mire. P s ~ c h o ~ o m o l i cUcdicine, 1956, 18, 234-242. Furcbtgott, E.. Wechkin, S.'. & Dces. J, \\'. Opeoheld exploration as a iunction of a g . Journal of Comparo!ive.and Phpsiologicol Psychology, 1961, 54, 386-3-355. Hall, C. S. Emotional behavior in the rat: DcfecaLion and urination k measurcs of individual diiferences in emotionality. J o u m a l o Comparath:c ! Ps~ch~logy, 1934, 18, 385403. Hall, C. S. Emotional behavior in the rat: n l . The relationshio between emotiomlitv and ambulator). aclivity. l o u d of Comparntiue Plychology, 1936, 22. 345-352. Hall, C. S., B'Rdlechey? E. L. A s!udy of the rat's behavior in a 6e!d: A contribu:ion to method in comparative psychology. Uniumrity o,! California o Publications i n P v c h o l. ~ ~ . . . 1932. 6. 1-12. Henderson. S. D. The ranlaundinz rficcu of mnetic variables in early experience research: Can we ignore them? Dcseloptentol P~ychobiology. 1965, 1. 14+152. Henderson, N. D. Prior treatment effects on open- field emotion?lity: The "red for representative design. Annals of the Ncm Yorb Acodemy of Sdcnce, 1969. 159, 8E-868. Henderson, X. D. Genetic influences oo the behavior of mice can he obscured by laboratov rearing. ! Journal o Cornparalive ond Ph.vriologicd Prpchology. 1970. 72, 505-511. Hoicr, M. A . Cardiac and respiratory function during sudden prolonged immohililv in wild rodenla. P~ychoromeric h f e d i d ~ e , 1970, 32, 633647. Hughes, R. N. Social facilitation of locomotion aod erploratio? in rats. BritLh J o u t d of P5pchofog.v. 1969, bO? 365-358. Ivinskir, .4. The reliabilily of behavioral measurer oblsined in t h e open-field. Aur!mlim Journal of Ivinskis, A. A study of validity of opca-held measures. AuslroL'on J w m d of Psychology, 1970, 22, 175-15.3. - - ~-.. Jerrard, L. E., 8; Brunnel? 8. X. Open-6cld bchavior of hipporampal icu'onrd rats and hamsten.

Journal of Cornparalivc and Phydological Psychology, 1965, 66, 50W502. King, D. L. Comparisoo bctwceo two metbods of demonstrating whtcdners of emotionality rariahlu in me. J o d 01 Comporarivc and Phyriologkal Psychology. 1970, 72, 238-243. King, 1. Parameters relevant to d c t e r m i k n ~the effech of carly experienv upon the adult behavior of animals. Psycholofical BJlclin. 1958, 53. 46-55. Xrsiak, ? ,. I & Janku. I. hlruurement of pharmacoof erploratorv activity in mice: logical dcp-on A contribution la the problem of time economy and wnsitirity. Psychophormocologia, 1971, 21, 118-130. Labarba,R. C., & White, J. L. Litter sizevarialiom and cmationalreacti\ity in BALBJc mice. J o m a l 01 Compomlicr and Ph?riulogicol Prychology, 1971, 75, 254-257. L i t , J., & GoUo\=-Remon, E. Permanent efircts of nutritional 2nd cndocrinolopical iotrrvention in early ontagcny on the level of n a n - r w & c u c i t ahililp and on lability (cmatioaslity). Ann& of Ihc 'YLW York Acadcmy of Science, 1969,129, 710720. Latan&, B., Cappll. H., & Joy, 1'. Social deprivation, housing density. a n d gregariousncrs in rats. Journal o Comparative and Phyriologicol Pry! chology, 1970. 70. 221-227. Le\ine, S., Haltmeyer. G., Karas, G., & Denenberg, V . Physiological and behavioral eRecU of infantile stimulation. Physiology and.Bchocim, 1967, 2, 5s59. Livewy, P. J., & Egger, G. J. A;e as a factor in opn-field rpspohiivmtrs in the white rat. Jou+nd of Comgnroliur and Phyriologicnl Psychology, 19iO. 73, 93-99. Lynn. R. ' Arlnlion, orourd, onr! the on'enlation rcaclion. E l m f o r d , N.P.: Pergamon Prerr, 1966. 3fanoresitr. 31. Early enriranrnenml enrichment and mouse behavior. Journnl. of Comparoliae ond Phyriologicol Psychology, 1970. 71, 459466. Martinek, Z., & L i t , J . Long term stability o: individual differences io exploratory behavior and rate of habituation in dogs. Phyriologio Bohemoslounico, 1969, 18. 217-225. 3IcCall. R . Caretaker rffert in rats. Dcr!dnprrm!d P$?cholog?. 1969. I. 771. 3lcCall. R.. Lester, >I., & Dolan. C. Differential rearing and the crploration stimuli in the openfield. Uct~clopmcnlalPryrholog?. 1969, I. ;jO-:t?. >llrClearn. G. E. Strain diffcrenvs in adirit)' in mice: ln6ucnre of i!lumination. J o m a l of Comporntioa ond Pkpriological Psycholog?, 1960, 53, 142-14:. hleier, G. W. The half to:d tale and th: half replication. Dsr~r1oprnm:al Psychubioiog~, 1968, 1, 77i8. hlontgomery, K. C. The relation between crploratory behavior and spontaneous alternation in the white rat. J o u r n d 01 Comporoliva end Phjsiological Pspchology, 1'351, 44, 581-559.

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