Behavioural Processes 41 (1997) 213 – 226

Intrinsic exploration in animals: motives and measurement

Robert N. Hughes
Department of Psychology, Uni6ersity of Canterbury, PB 4800, Christchurch, New Zealand

Received 2 December 1996; accepted 22 May 1997

Abstract

Intrinsic exploration involves exploratory acts that are not instrumental in achieving any particular goal other than
performance of the acts themselves. Of the theories proposed to account for the motivation of intrinsic exploration
in animals, concepts of exploratory drive, optimal arousal and fear have featured prominently. But since no single
approach has adequate explanatory or predictive power, it is probably sufficient to go no further than accept that
organisms may have some type of ‘need’ for sensory change which can be satisfied mainly by intrinsic exploration.
Attempts to measure the phenomenon in the laboratory can be divided into forced tests in which locomotion and
other motor responses are recorded in animals placed into a totally novel environments, and free tests involving
measurements of active choices of differing degrees of novelty. Because of the difficulty of distinguishing between
extrinsic and intrinsic exploration with activity indices, tests of free exploration are always preferable. These include
novelty-related location preferences (including spontaneous alternation and responses to brightness change), object
exploration and learning for exploratory rewards all of which can be viewed as reasonably valid measures of intrinsic
exploration to a greater or lesser extent. © 1997 Elsevier Science B.V.

Keywords: Intrinsic exploration; Animals; Motives; Forced exploration; Free exploration; Novelty

1. Introduction 1899; Slonaker, 1912), most research into explo-

ration has occurred during the last 50 years. And
The tendency to explore unfamiliar environ- yet there are still answers to important questions
mental stimuli has been described in many free- that allude us and misunderstandings with respect
moving animal species ranging from invertebrates, to motives for and the measurement of ex-
such as bees (Lindauer, 1952) and cockroaches ploratory acts that do not appear to be instru-
(Darchen, 1952, 1955, 1957), to the highest pri- mental in achieving any particular goal other than
mates. While there were a few isolated studies of performance of the acts themselves.
inquisitive or investigatory behavior in laboratory The first complete analysis and categorisation
rats near the beginning of this century (Small, of the various forms of exploratory behavior,

0376-6357/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved.

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214 R.N. Hughes / Beha6ioural Processes 41 (1997) 213–226

their environmental determinants and their possi- atory responses (comprising changes in stimulus
ble functions was D.E. Berlyne’s highly influential objects effected by the exploring subject, e.g. ma-
book, ‘Conflict, Arousal and Curiosity’, published nipulation). Typically all three categories would
in 1960. By bringing together the results of the be involved, to a greater or lesser extent, in a
many diverse experimental studies carried out particular exploratory sequence and occur, at
mainly, but not exclusively, in the USA during the least initially, in the order 1–3. Berlyne (1960)
1950s, Berlyne was able to establish useful guideli- made another distinction that embraced all of the
nes for future research into the functions of and above three categories, namely that between spe-
reasons for exploratory behavior in animals (in- cific and diversive exploration. Specific explo-
cluding human beings). Berlyne’s book was fol- ration was said to be directed towards a particular
lowed 5 years later by another important source of stimulation such as when ‘taking a
contribution that was more directly focused on closer look at’ something (Berlyne, 1963), whereas
nonhuman (chiefly rat) exploration, namely H. diversive exploration consisted of responses di-
Fowler’s (1965) ‘Curiosity and Exploratory Be- rected towards a wide range of stimuli in order to
havior’. During the ensuing three decades, these satisfy a need for further interactions with envi-
two publications were to have a major influence ronmental stimuli. Within this framework, diver-
on the development of research into animal ex- sive can never precede specific exploration since it
ploratory behavior. However, in spite of some usually arises once exploration of a specific stimu-
excellent reminders (Archer and Birke, 1983; Voss lus object has reached a natural conclusion—in
and Keller, 1983; Renner, 1990), awareness of the other words, the answer to ‘what is it?’ is followed
resulting body of knowledge along with a number
by the questions ‘what can I do with it?’ (Hutt,
of the lessons learnt earlier seems less obvious in
1970) or ‘what other new stimuli are available?’
more recent investigations of animal behavior in
An important distinction Berlyne made was
which measurements of exploration have been
that between extrinsic and intrinsic exploration.
included. To some extent this might be due to the
Extrinsic exploration was seen as behavior pri-
study of exploratory behavior per se having be-
marily directed towards an external goal in re-
come of minor interest since the mid 1960s (Rus-
sponse to some specific requirement. It involved
sell, 1983). And yet measurements of exploration
continue to feature in studies of the behavioral active seeking of a particular outcome such as
effects of a variety of pharmacological and neuro- finding food when hungry or encountering a
physiological manipulations. The aim of the means of escape from a dangerous environment.
present paper is to therefore briefly present some On the other hand, Berlyne (1960) viewed intrinsic
of the ideas and research findings responsible for exploration as behavior that facilitated investiga-
what we know about responses that serve intrinsic tion of stimuli mainly in response to an interest in
exploratory functions and draw attention to some these stimuli for their own sake. Intrinsic explo-
of the issues that bear on how laboratory studies ration encompassed much of what later authors
of such responses are conducted and the results referred to as ‘novelty seeking’ (McReynolds,
interpreted. 1962), ‘reactive curiosity’ (Penney and McCann,
1964), ‘sensation seeking’ (Zuckerman, 1971) or
‘stimulus seeking’ (Hoyenga and Hoyenga, 1984)
2. General classes of exploratory behavior in response to what came to be known as the
‘curiosity-investigative motives’ (Butler, 1960).
According to Berlyne (1960), three general cate- But while Berlyne’s distinction between the two
gories of exploratory response can be ident- types of exploration has considerable appeal from
ified: (1) orienting responses (comprising changes a motivational perspective, in experimental prac-
in the orientation or state of sense organs); tice it can be less obvious since both can occur
(2) locomotor exploration (comprising changes in together. Even when seeking an extrinsic goal an
location of the whole animal) and (3) investig- animal’s attention can be captivated by a stimulus
 R.N. Hughes / Beha6ioural Processes 41 (1997) 213–226 215

that is unrelated to the task in hand but provides squares would have been defined as more visually
the opportunity for more intrinsically-based ex- complex than an 8× 8 cm pattern comprising 2
ploration. For example, Cohen and Stettner black and 2 white 4-cm squares. Likewise, visual
(1968) observed that, after having learnt to run a patterns containing ‘surprising’ elements that were
straight runway for a sucrose solution, on subse- at odds with most of the other elements that made
quent trials water-deprived rats explored a newly up the patterns, such as a triangle amongst circles
introduced blind alley before they finally ap- (heterogeneity) or a drawing of a four-legged bird
proached and drank the reinforcer. As will later amongst normal birds (incongruity), would be
become obvious, it is often difficult if not impossi- seen as more complex than regular patterns.
ble to experimentally distinguish between extrinsic A simpler way of classifying collative variables
and intrinsic exploration because, although their had been provided earlier by Dember and Earl
motives or consequences might differ, the re- (1957) who viewed them in terms of the types of
sponses emitted can be identical. stimulus change involved. Changes made to a
stimulus during exposure or from one exposure to
another were defined as temporal changes,
3. Stimuli that elicit exploratory behavior whereas changes experienced as a result of the
discontinuities in stimulation encountered while
Another of Berlyne’s significant contributions scanning the components of a stimulus pattern
was his identification of those qualities of stimula- were called spatial changes. Accordingly, tempo-
tion that initiate and sustain exploratory behav- ral changes would include novelty and surprising-
ior. He referred to these qualities as ‘collative
ness, and spatial change would involve stimulus
variables’ (Berlyne, 1960) since they depended on
complexity in its various forms. While the two
collation (or comparison) of information from
types of change can be important for both extrin-
different sources. The most important of these for
sic and intrinsic exploration, their role in the
animal behaviour were novelty, change and sur-
latter form has characterised most laboratory-
prisingness (involving comparisons of present
based studies of exploratory behavior in animals.
with previously experienced stimuli) and complex-
Consequently, the remainder of the present paper
ity —involving comparisons of present stimuli
with others accompanying it, (Berlyne, 1963). will be largely confined to a discussion of intrinsic
Novelty and change were largely synonymous exploration. Nevertheless, one should not ignore
terms since, although change may occur during the adaptive importance of more extrinsic forms
exposure to a stimulus, novelty implied that a which is perhaps most evident in the foraging
change in stimulation had occurred between one behavior of mainly feral species that has intrigued
exposure to a stimulus or situation and another. behavioral ecologists for nearly 30 years. System-
Surprisingness also comprised a change in stimu- atic investigation of a location which has potential
lation between two or more experiences, but one for providing the necessity being sought by an
that involved an expectation with which the en- exploring animal will clearly maximise the chance
countered stimulus disagreed. of success. Irrespective of whether the exploration
Complexity effectively referred to the amount is extrinsically or intrinsically determined it is
of variety or diversity within a stimulus pattern generally accepted that familiarisation with the
and could be said to increase ‘with the number of environment being explored incidentally provides
distinguishable elements’ and ‘with dissimilarity information about resources for future reference
between elements’ (Berlyne, 1960). A more com- (Barnett, 1963) possibly by enabling the establish-
plex stimulus was thought of as one that the ment of ‘cognitive maps’ to assist in later search-
perceiver could ‘do more with’ by providing ‘more ing behavior (Bell, 1991). Further details about
potential opportunities for responding’ (Dember, relationships between exploration, foraging and
1960). For example, an 8×8 cm chequerboard searching can be found in Bell (1991), Kamil and
pattern comprising 8 black and 8 white 2 cm Sargent (1981) and Kamil et al. (1987).
216 R.N. Hughes / Beha6ioural Processes 41 (1997) 213–226

4. Motives for intrinsic exploration and spatial changes in stimulation. Another no-
table difference between exploratory drive and
Amongst the attempts to account for the mo- the other drives was evident in the consequences
tivation of intrinsic exploration have been the of drive-related behavior — whereas hunger and
postulation of exploratory – investigatory drives, thirst, for example, resulted in a decrease in
appeals to concepts of optimal arousal, and ex- stimulation through reduction of the drive state,
planations based on the energising effects of exploration inevitably resulted in an increase
fear. With varying degrees of success, others (Fowler, 1965).
have involved reducing conflict, discrepancy or A further refinement of the concept of ex-
uncertainty with respect to information inherent ploratory drive involved drawing clearer distinc-
in the external environment (Berlyne, 1960,
tions between the nature of eliciting and
1963; Russell, 1983), but the three mentioned
reinforcing stimuli. The initial ‘titillation’
above have been the most widely applied to in-
(O’Connell, 1965) or ‘curiosity’ approach
trinsic exploration in nonhuman animals.
(Fowler, 1965) characterised by Montgomery
4.1. Exploratory dri6es (1953), Harlow (1953) and Berlyne (1950), main-
tained that curiosity was instigated by novel
Some of the earliest demonstrations of an ex- stimuli which were accordingly explored, thereby
ploratory activity that occurred merely for its reducing the strength of the exploratory drive.
own sake were reports of how rhesus monkeys This idea required the same novel stimuli to
learned to solve mechanical puzzles and contin- both elicit and reinforce exploratory behavior
ued performing for up to 10 h without any con- which was totally inconsistent with the tradi-
ventional reinforcers (Harlow, 1950; Harlow et tional drive framework’s insistence on different
al., 1950). Such results led to the idea that cer- eliciting and reinforcing stimuli. An alternative
tain types of exploratory response may arise approach first suggested by Myers and Miller
from a separate exploratory motive that was in- (1954) was to postulate that familiar stimuli
dependent of other motives relevant to the satis- elicit exploratory behavior which was then rein-
faction of specific bodily needs (Myers and forced by the novelty subsequently experienced.
Miller, 1954). Today, in the face of overwhelm- Or as Fowler (1965) put it, ‘animals became ‘sa-
ing evidence, there can be little doubt that such tiated’ or ‘bored’ with stimuli to which they had
behavior has some intrinsically-derived basis, but been or were being exposed, and thus responded
not necessarily of the sort suggested by propo- to other stimuli that were novel or unfamiliar’.
nents of a drive-based motive to explore. Glanzer (1953) developed a concept of ‘stimulus
When it became clear, that the motivation of satiation’ which was similar except that contin-
intrinsic exploration could not be easily ac- ued exposure to a stimulus did not have an
counted for by learned secondary drives and re-
avoidance-related energising function but merely
inforcers which had developed from associations
caused a decrement in an animal’s tendency to
with primary drive arousal and satisfaction, a
respond to that stimulus. Contrary to curiosity
new type of ‘nonhomeostatic drive’ was pro-
theories, the boredom approach was more con-
posed (Berlyne, 1950; Harlow, 1953; Mont-
gomery, 1953). This ‘exploratory drive’ differed sistent with the traditional drive framework be-
in a number of respects from ‘homeostatic’ drive cause different energising and reinforcing stimuli
states such as hunger and thirst. For example, were said to operate, namely familiar and novel
contrary to homeostatic drives, exploratory drive stimuli respectively. With its emphasis on ener-
was said to be ‘exteroceptively aroused’ which gising functions of the attractiveness of novelty,
meant that the eliciting stimuli for intrinsic ex- the curiosity approach was more closely aligned
ploration resided in the animal’s external envi- with incentive (or ‘pull’) rather than with drive
ronment (Fowler, 1965) in the form of temporal (or ‘push’) theories of motivation in general.
 R.N. Hughes / Beha6ioural Processes 41 (1997) 213–226 217

4.1.1. Sensory reinforcement changed to black or white from two of the same
Studies of learning in which rats and monkeys brightness), they would have been equally satiated
in particular were shown to solve a variety of for black and white and should therefore show no
tasks for opportunities to explore or experience preference for either arm when able to choose.
novel stimuli, were regarded as evidence for the However, if they were attracted to (or curious
drive status of both types of exploratory motive. about) novelty, the rats should choose the arm
In addition to the puzzle-solving behavior of Har- that had changed from what it had been during
low’s monkeys described above, there have been exposure, even though both were of the same
many reports of rats, mice and monkeys learning brightness. Since the rats conformed to the re-
bar-pressing responses for changes in light or sponse-to-change (or novelty) prediction, Dem-
sound stimuli (Kish, 1955; Marx et al., 1955; ber’s results appeared to favor the operation of a
Moon and Lodahl, 1956; Barnes and Kish, 1961; curiosity-related motive in intrinsic exploration
Robinson, 1961), rats learning position and (Dember and Earl, 1957) at least as it is reflected
brightness discrimination problems in a Y-maze in spontaneous alternation. The results of Dember
for the opportunity to explore a checkerboard (1956) were later confirmed in several investiga-
maze (Montgomery, 1954; Montgomery and tions with rats (Walk, 1960; O’Connell, 1964;
Segall, 1955) and rhesus monkeys learning to Leaton and Buck, 1968; Stewart, 1975) and ferrets
discriminate between colors for the opportunity to (Hughes, 1965a, 1967) and are generally regarded
open a door and look outside the experimental as strong evidence for spontaneous alternation
chamber at groups of people (Butler, 1953), at a comprising an active choice of the more novel
moving toy train (Butler, 1954) or at monkey arm—even though its curiosity basis still remains
colony (Butler and Alexander, 1955). But while to be empirically substantiated (Dember, 1989).
apparently supporting a drive-type motive, such In the course of trying to determine which of
evidence also provided somewhat of a paradox the two types of exploratory drive was the most
for curiosity theorists. As Brown (1961) pointed likely explanation for intrinsic motivation, it be-
out, the curiosity position virtually forced one to came increasingly obvious that a more plausible
conclude that if novel stimuli elicited an ex- approach should incorporate both points of view.
ploratory drive, this drive was not aroused until As well as demonstrations of responding to novel
after an animal had emitted the behavior the drive objects provided in both novel and familiar envi-
was supposed to be motivating. ronments (McCall et al., 1969; Glickman et al.,
1970; Cowan, 1976), studies in which experimen-
4.1.2. Responses to change tal subjects were relatively deprived of environ-
In an attempt to account for why nondeprived mental stimulation showed how such conditions
rats and other animals spontaneously alternate would provoke active seeking of various temporal
successive choices of T- or Y-maze arms, Dember and spatial changes in stimulation (Kish and An-
(1956) carried out what also became a classical tonitis, 1956; Darchen, 1957; Premack et al.,
test of the stimulus satiation and curiosity theories 1957). Clearly, an organism would explore in
of exploratory drive. Rats were confined to the order to either further investigate a novel stimulus
stem of a T-maze and prevented from entering the that had attracted its attention, or to avoid con-
arms by clear glass barriers. On a subsequent trial tinued contact with a familiar stimulus. In other
they were allowed access to both arms, one of words, it would respond to or for novelty (i.e.
which had been changed in brightness. During inspective and inquisitive exploration respectively,
exposure, one arm was black and the other white, (Berlyne, 1960) depending on the nature of its
whereas for the choice trial both arms were either current situation. This compromise was incorpo-
black or white. The author reasoned that if the rated into theories of arousal which in the case of
rats had become satiated for the stimuli experi- exploratory behavior were largely attempts to ac-
enced during exposure (as was concluded by Kivy count for intrinsic exploratory phenomena
et al., 1956 who observed rats select the arm through a reformulation of the drive concept.
218 R.N. Hughes / Beha6ioural Processes 41 (1997) 213–226

4.2. Concepts of optimal arousal as a U-shaped function of what he called ‘stimu-

lus impact’—that is, a combination of collative
Inspired by research into the possible role of variables and intensity of stimulation. Conse-
the reticular activating system in attention, sen- quently, arousal would be high when an animal
sory processing and other behavioral phenomena, was exposed to either highly novel or highly fa-
a number of disenchanted drive theorists were miliar stimuli. But as Fowler (1965) pointed out,
attracted to the concept of arousal. In spite of this position committed Berlyne to assuming that
inconsistent relationships between CNS and be- an individual would also be highly aroused by a
havioral arousal (Thompson, 1967), the reticular low intensity stimulus that was neither especially
system appeared to provide a physiological basis novel nor familiar. By only considering decreases
for drive theory and promised to solve some of in stimulation, Berlyne’s position was the closest
the problems encountered by that approach to the classical drive framework.
(Beck, 1983). Accordingly, early advocates of Not surprisingly, problems soon began to
arousal theories proposed that organisms continu- emerge with this initially appealing but oversim-
ally strive to maintain an optimal level of sensory plistic, unitary formulation. For example, it was
input and hence CNS arousal (Hebb, 1955; predicted that events which increased arousal,
Leuba, 1955; Malmo, 1959; Fiske and Maddi, such as the action of stimulant drugs, should
1961). Activities that resulted in movement away lower tendencies to respond to or for novel stim-
from this level would be avoided, and activities uli. While this has occurred for stimulants such as
that maintained the level (either through increases methamphetamine (Berlyne et al., 1966), am-
when it was low or decreases when it was high) phetamine (Robbins and Iversen, 1973) and
would be reinforced. In other words, by insisting methylphenidate (Dyne and Hughes, 1969), the
that behavior could be directed towards increases same outcomes have been reported for depressant
in stimulation if the level was low and decreases if drugs that have the opposite effects on arousal,
it was high, optimal arousal theories marked a such as chlordiazepoxide (Hughes, 1972) or
radical departure from classical drive theory that sodium pentobarbital (Berlyne, 1969). Because of
only considered decreases (Hoyenga and the many inconsistencies in research findings
Hoyenga, 1984). Intrinsic exploration was there- along with the lack of acceptable correlations
fore seen as a means for increasing input from between different behavioral and CNS arousal as
environmental stimulation and thus facilitating well as between different indices of arousal level,
maintenance of the optimal level. Conversely, arousal as a unitary explanatory construct has
avoidance (by not exploring) of excessively high outlived any usefulness it might once have ap-
degrees of arousing stimulus change or of milder peared to have had (Neiss, 1988, 1990). Even as
degrees when overaroused by some other state long ago as 1965, Fowler had raised the possibil-
such as fear, was seen as an attempt to reduce ity that the concept of optimal arousal applied to
high arousal or at least prevent it from increasing exploration explained everything and predicted
further. As the proposed relationship between ef- nothing.
fective behavior and arousal was in the form of an
inverted U, the whole idea of an optimal level of 4.3. Fear
stimulation and arousal was essentially a more
elaborate version of the Yerkes-Dodson Law It is well known that, while many animals will
(Yerkes and Dodson, 1908). approach and investigate temporal and spatial
Berlyne (1960, 1963) attempted to encompass changes in stimulation, avoidance can also occur
the principles of curiosity and boredom drives if the degree of change is too great. Even changes
into one arousal theory by suggesting that the that would be relatively mild and attractive for an
optimal level of arousal was always the lowest adult or domesticated animal can be excessive and
possible so that organisms behaved only in order frightening for a young or feral member of the
to reduce arousal. This meant that he saw arousal same species, and thus avoided. These observa-
 R.N. Hughes / Beha6ioural Processes 41 (1997) 213–226 219

tions led to the postulation of two-factor moti- approach behavior (Halliday, 1966; Lester, 1967,
vational theories of exploration (Russell, 1973) 1968) in an inverted U-shaped fashion (Lester,
whereby novelty (and other related variables) 1967). However, unitary fear theories of intrinsic
was seen to invoke competing states of both fear exploration are no longer taken seriously since
and curiosity (Montgomery, 1955). Conse- evidence in support of them is sparse, and what
quently, the extent to which exploration would little exists is largely inconclusive and open to
occur would depend on how much it was inhib- alternative interpretations (Russell, 1973, 1983).
ited by fear. In terms of this formulation, initial Although exploration might reduce fear, it is un-
contact with a novel stimulus can be assumed to likely that fear alone motivates the behavior
provoke an approach-avoidance conflict with the (Russell, 1973).
relative incidence of each component depending
on the degree of novelty characterizing the stim-
4.4. Conclusion
ulus. Consequently, the extent of approach
would be an inverted U-shaped function of de-
Given the lack of progress over many years in
clining novelty. In essence two-factor theories
arriving at a universally acceptable theory to ac-
were drive-type explanations whereby fear ener-
count for the motivation of intrinsic exploration
gised behavior in the presence of intense novelty
in animals, one is still faced with Fowler’s
and then curiosity became the drive when nov-
elty was milder. With both very high and very (1965) question of whether or not the postula-
low degrees of novelty (determined by amount tion of motives to explore does little else than
of previous exposure to or number of prior con- restate the facts that remain to be explained.
tacts with the stimulus) the tendency to ap- These facts include the knowledge that fed and
proach would be low because of fear and watered animals will approach and investigate
disinterest respectively. The inhibition of explo- mild temporal and spatial changes in stimula-
ration by fear has been exploited in some assess- tion, that their investigation will decline to the
ments of the effects of anxiolytic drugs point of disinterest with continued or repeated
(Crawley, 1985; File, 1985; Kelley, 1993). The exposure to such changes, and that they will
assumption is that fear of novelty will be allevi- seek and work for changes in stimulation at a
ated by the drugs thereby resulting in an in- rate that is proportional to the amount of stimu-
crease in exploratory behavior. While this might lus familiarity or monotony in their environ-
appear to be so from their effects on activity in ment. Attempting to account for the responses
a totally novel environment, such as an open emitted by animals in relation to novel and fa-
field or a Y-box (Marriott and Spencer, 1965; miliar stimuli by some form of ‘exploratory mo-
Christmas and Maxwell, 1970), anxiolytic drugs tive’ has clearly limited explanatory and
can have the reverse effect on a usual preference predictive value. If a motivational force has to
for novelty when rats are allowed to freely be proposed, it is probably sufficient to go no
choose between a novel and a familiar environ- further than accept that, as indicated by studies
ment (Hughes, 1972, 1981; Hughes and Syme, of stimulus deprivation (Kish and Antonitis,
1972; Hughes and Greig, 1975).
1956; Darchen, 1957; Premack et al., 1957), or-
Although two-factor theories seemed to de-
ganisms appear to have some type of behavioral
scribe most responses to temporal and spatial
‘need’ for sensory change which can be satisfied
changes in stimulation, an alternative view was
by intrinsic exploratory responses. However,
favored by some people namely, that all phases
of an exploratory response could be accounted even though intrinsic exploration is more obvi-
for by fear alone. Proponents of such unitary ously focused on this need, any extrinsically-mo-
fear theories maintained that uncertainty about tivated behavior that incidentally facilitates
novelty instigated fear which, at high levels pro- sensory contact with environmental stimuli can
duced avoidance but at lower levels produced also provide some degree of satisfaction.
220 R.N. Hughes / Beha6ioural Processes 41 (1997) 213–226

5. Measurement of intrinsic exploration variables being investigated. As well as the

difficulty of identifying valid intrinsic exploratory
Accurate measurement of intrinsic exploration responses, forced tests represent an ecologically
in animals has been an ongoing problem ever improbable situation since animals in the wild are
since psychologists became interested in the phe- rarely thrust into totally novel environments with-
nomenon. Many procedures have been developed out the opportunity to retreat to more familiar
of which a large number are of suspect validity. It surroundings (Russell, 1983).
is possible to divide all of these procedures into The dangers of assuming that a motor response
two groups based on the classification of Welker (such as gross open-field locomotion) reflects an
(1957) of ‘forced’ and ‘free’ tests of exploration. exploratory tendency alone should by now be
Forced exploration refers to situations where an glaringly obvious. And yet, in spite of repeated
animal has no option but to remain in a totally reminders (Robbins, 1977; Corey, 1978; Renner,
novel environment (such as an open field) into 1990; Kelley, 1993), examples of locomotor and
which it has been placed, whereas free exploration other activities emitted in forced situations
is that which occurs when it can freely choose defined as ‘exploratory behavior’ still appear in
between exploring two or more environments or the literature (Fahey et al., 1995; Sherif and Ore-
stimuli differing in degrees of temporal and/or land, 1995; Erickson et al., 1996; Handa et al.,
spatial change. The following discussion is not 1996). Nevertheless, it is not intended to dwell on
intended to be a detailed review of specific tests as the problems of validity which characterise the
this has been done to a greater or lesser extent by use of locomotor and other activity measures in
several previous authors mainly in relation to forced tests of exploration apart from reinforcing
drug testing (Robbins, 1977; File, 1982; Kelley, the view that they should be abandoned (Renner,
1993). Instead, it is hoped to provide an overview 1990) by serious students of intrinsic exploration
of general groupings of tests in order to reawaken in animals. In addition to the difficulty (if not
awareness of some of the problems of interpreting impossibility) of distinguishing between the two
experimental outcomes that could arise. types of exploratory behavior in forced tests, fol-
lowing some severely disruptive manipulations
5.1. Forced tests of exploration (such as stimulant drug administration) it is even
difficult to reliably distinguish between either type
Most forced tests have involved placing animals and other nonexploratory activities such as non-
into novel open fields, Y-boxes and the like where specific general activity and stereotyped or perse-
there is no opportunity for them to retreat to a verative responding.
home or more familiar environment. Frequencies
of certain emitted behaviors, notably locomotion, 5.1.1. The ele6ated plus-maze
rearing, sniffing and even nonspecific activity have The elevated plus-maze devised by Handley and
then been interpreted as exploratory in nature. Mithani (1984) was based on apparatus that fea-
While there has usually been no attempt to distin- tured in an earlier study of the role of fear in
guish between extrinsic and intrinsic exploration, exploration (Montgomery, 1955). Although the
it has often been assumed that such responses version in current use was primarily developed
reflect responses to or for novelty rather than and validated as a test of fear (or ‘anxiety’) for the
some other more extrinsically derived behaviour evaluation of anxiolytic and anxiogenic drugs
such as attempts to escape from a fear-inducing (Pellow et al., 1985), it is often used to assess
situation (Welker, 1957). Whether or not behavior exploratory behavior in animals (Sherif and Ore-
in totally novel environments is interpreted as land, 1995; Menard and Treit, 1996; Mendonca et
intrinsic exploration depends largely on the focus al., 1996; Thongsaard et al., 1996). The maze is
of attention of the investigator (Bindra, 1959) elevated to about 50 cm and comprises two open
who might also take account of the deprivational arms opposite each other and two enclosed arms.
state of the animal and the specific independent Generally, rats and mice prefer to occupy the
 R.N. Hughes / Beha6ioural Processes 41 (1997) 213–226 221

enclosed rather than the more fear-inducing open preference (Fehrer, 1956; Richards and Leslie,
arms. Because of the opportunity to retreat to the 1962; Hughes, 1965b, 1968; Russell, 1975; Misslin
enclosed arms, the plus-maze procedure could be and Ropartz, 1981). While measurements of this
mistaken for a free exploration test. But since preference are more indicative of the responsive-
there is no prior habituation to any arm(s), none ness to novelty that would characterise intrinsic
will be familiar. Consequently, the main reason exploration than activity indices alone, there is
for occupying the enclosed arms is not to respond still the possibility that venturing out into the
to their novelty, but to avoid venturing out onto novel environment may sometimes comprise seek-
the equally novel open arms. While subjects in the ing something that the home or familiar area had
maze may exhibit certain activities with an appar- lacked e.g. a means of escape from the apparatus.
ent exploratory function (e.g. rearing and sniffing, However, this seems unlikely in the face of evi-
especially in the enclosed arms), as with behavior dence that anxiogenic experiences (such as treat-
recorded in other forced tests, there is no reliable ment with methylscopolamine, methamphetamine
way of distinguishing between their extrinsic and or adrenalin) reduce rather than increase the ten-
intrinsic bases. Besides, compelling evidence dency to visit the novel half of an exploration box
against the elevated plus-maze being a test of (Horsburgh and Hughes, 1981; Misslin and
intrinsic exploration is found in the lack of any Ropartz, 1981; Hughes, 1987). A test of the possi-
correlation between behavior in the apparatus and bility that a novel environment might be seen as a
exploratory head-dipping in the free exploration potential escape route could involve providing
hole-board test discussed later (Pellow et al., two novel areas that differed in amount of stimu-
1985). lus change. For example, there would seem little
reason why a novel area that was a different
5.2. Free tests of exploration brightness from the familiar environment should
encourage more extrinsic exploration than one
Concern with the highly suspect validity of that was the same brightness. But, a change to a
forced tests led to a number of other procedures different brightness might be expected to produce
designed to more accurately measure incidences of more intrinsic exploration. In spite of difficulties
intrinsic exploration. Most of these involved more in confidently distinguishing between extrinsic and
direct observations of reactions to temporal and intrinsic exploration, tests of preferences for novel
spatial changes in stimulation in animals given the locations have found particular favor amongst
opportunity to freely choose between such behavioral pharmacologists in the belief that their
changes. The most widely adopted paradigms relatively weak reliance on locomotion enables
have involved preferences for novel versus less drug effects on reactivity to novel stimuli to be
novel locations, object exploration and learning teased out from effects on motor activity (Rob-
for exploratory rewards. bins, 1977; Kelley, 1993).
Since spontaneous alternation involves a choice
5.2.1. No6elty-related location preferences between the most recently visited (or ‘familiar’)
In most real-life situations, animals eventually and an unvisited (or ‘novel’) T-maze arm, the
move into and explore new territory from the procedure effectively embodies the principles of
relative security of a familiar ‘home’ environment. novelty-related location preferences discussed
Awareness of this principle has given rise to a above. Although it is generally believed that spon-
number of more ecologically valid experimental taneous alternation in nondeprived rats and mice
procedures that involve providing access to a involves a preference for the more novel (or least
mildly novel area adjacent to a more familiar one. familiar) arm (Dember, 1989), as with other pref-
In general, animals are confined to a living or erence tests, this does not automatically define it
familiar area before being allowed to move freely as an example of intrinsic exploration since other
to and from a new, previously inaccessible novel extrinsic goals could be involved. For example,
area for which at least rats and mice show a the maze arm chosen on trial 2 could merely be
222 R.N. Hughes / Beha6ioural Processes 41 (1997) 213–226

regarded by the animal as a potential means of can be meaningfully studied is found in the recent
escape that was absent in the trial 1 arm (Hughes, research of Renner and colleagues (Renner, 1987;
1989b). Alternatively, while a tendency to repeat Renner et al., 1992; Renner and Seltzer, 1991;
rather than alternate could be interpreted as nov- 1994).
elty avoidance (Hughes, 1982), it might equally be A procedure related to object exploration is the
due to unintentional reinforcement of an animal’s hole-board test first introduced by Boissier and
trial 1 choice, such as temporary removal from an Simon (1962). In the floor of the apparatus are a
aversive environment between trials (Hughes, series of holes underneath which can be found
1989c). For a comprehensive account of sponta- various objects. These can be investigated by the
neous alternation, see Dember and Richman animal when it dips its head into the holes. Such
(1989). head-dipping is believed to reflect intrinsic explo-
Although it has been adopted by some authors ration of the objects which is independent of
(Aitken, 1972, 1974), another example of a nov- locomotor activity. While this seems no less rea-
elty-related location preference that has received sonable than for other forms of object investiga-
less attention than it deserves is the response to tion, some animals (especially extremely active
brightness change phenomenon developed by ones) can accidentally break with their feet or tail
Kivy et al. (1956) and Dember (1956), described the photocell light beams used for recording the
in Section 4.1.2. As suggested above, it would behavior (Boissier and Simon, 1967). To some
seem unlikely that any preference for a brightness extent, this can be rectified by reducing the num-
change were only extrinsically determined since, ber of holes (File and Wardill, 1975). There is also
without any prior opportunity for exploring either the possibility that head-dipping may comprise a
alternative before the critical choice trial, there is search for ways of escape rather than intrinsic
no convincing reason why the changed arm exploration (Renner, 1990). However, rats and
should have any more potential for an extrinsic mice have been shown to dip their heads less often
reward than the unchanged arm. In addition, as into empty holes than into those with objects
with spontaneous alternation (Hughes, 1989a), underneath and to head-dip more frequently in
this procedure enables assessment of an animal’s the presence of novel objects (File and Wardill,
initial attention to novelty as well as its preference 1975). Provided that the number of holes is small
by recording the arm first approached or oriented and that due account is taken of the novelty of
to, and then the arm finally entered. By also the objects underneath, the hole-board test would
recording visits to and from the changed arm and seem to be an acceptable measure of intrinsic
time spent in each over an extended period of exploration.
time, response-to-change could become a quite
powerful test of intrinsic exploration. 5.2.3. Learning for exploratory rewards
The various ways in which opportunities to
5.2.2. Object exploration experience and explore temporal and spatial
Observations of their investigation of novel ob- changes in stimulation have been used as rein-
jects (usually within a less novel or familiar home forcers in certain learning experiments were
environment) comprises one of the better ways of briefly described in Section 4.1.1. Provided it can
studying animals’ intrinsic exploration. By care- be established that the changes are not merely
fully recording the nature of their interactions conditioned forms of more conventional rein-
with the objects, a wealth of information can be forcers (such as food and water), responding for
obtained about the precise details and sequencing exploratory rewards seems a valid measure of
of exploratory responses in animals which may intrinsic exploration. But when assessing the ef-
have some value in the development of models of fects of any experimental manipulation on re-
learning and memory and a better understanding sponding for change, adequate account must be
of the biology of these processes (Renner, 1990). taken of the possible effects of the treatment on
An excellent example of how these interactions processes other than intrinsic exploration such as
 R.N. Hughes / Beha6ioural Processes 41 (1997) 213–226 223

learning ability or sensory-motor capacities. To involving learned responses because they are
avoid any serious confounding between changes quicker and cheaper.
in performance and sensory reinforcement or
learning following some experimental treatments
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