THE WHEREIS IT? AUTOSHAPING THEORIENTING RESPONSE … · (classical) and response-dependent...

JOURNAL OF THE EXPERIMENTAL ANALYSIS OF BEHAVIOR

THE "WHERE IS IT?" REFLEX:AUTOSHAPING THE ORIENTING RESPONSE

GYORGY BUZSAKI

UNIVERSITY MEDICAL SCHOOL, PiCS, HUNGARY

The goal of this review is to compare two divergent lines of research on signal-centeredbehavior: the orienting reflex (OR) and autoshaping. A review of conditioning experimentsin animals and humans suggests that the novelty hypothesis of the OR is no longer tenable.Only stimuli that represent biological "relevance" elicit ORs. A stimulus may be relevanta priori (i.e., unconditioned) or as a result of conditioning. Exposure to a conditioned stim-ulus (CS) that predicts a positive reinforcer causes the animal to orient to it throughoutconditioning. Within the CS-US interval, the initial CS-directed orienting response is fol-lowed by US-directed tendencies. Experimental evidence is shown that the development andmaintenance of the conditioned OR occur in a similar fashion both in response-independent(classical) and response-dependent (instrumental) paradigms. It is proposed that the condi-tioned OR and the signal-directed autoshaped response are identical. Signals predictingaversive events repel the subject from the source of the CS. It is suggested that the functionof the CS is not only to signal the probability of US occurrence, but also to serve as a spatialcue to guide the animal in the environment.Key words: orienting reflex, autoshaping, conditioning, learning theory

CONTENTSIntroductionTraditional view of the ORStimulus significance and the ORClassical conditioning and the ORMeasurement of the conditioned responseConditioned ORAutoshapingStimuli signaling aversive reinforcersStimulus-reinforcer versus response-reinforcer

contingenciesThe "where is it?" reflexFinal Comment

The general theme of this review is the sug-gestion that the underlying mechanisms of thesignal-directed autoshaped response (sign-track-ing) and the orienting reflex are identical.

I wish to thank Abram Amsel, Robert A. Boakes,Vilmos Csinyi, William Dailey, Eduardo Eidelberg,Endre Grastyan, Chris Lewis, John A. Nevin, MichaelE. Rashotte, and Mark Stanton for their helpful com-ments on an earlier draft of this manuscript. I am espe-cially indebted to John A. Nevin and End,re Grastyinfor their continuous encouragement. I thank the Divi-sion of Neurosurgery, University of Texas Health Sci-ence Center, San Antonio, Texas, for facilities duringthe preparation of this article. Send reprint requeststo Dr. G. BuzsAki, Department of Psychology, Univer-sity of Western Ontario, London, Ontario, Canada N6A5C2.

Although this may sound a trivial sugges-tion, to date theoretical accounts of autoshap-ing have not raised this possibility. To illus-trate, neither the influential monograph ofHearst and Jenkins (1974), nor a recent bookon autoshaping and conditioning theory (Lo-curto, Terrace, & Gibbon, 1981) contains asingle paragraph on the orienting reflex. Theconverse seems also to be true. In two recentlypublished books on the orienting reflex andgoal-directed behavior (Kimmel, van 01st, &Orlebeke, 1979; Thompson, Hicks, & Shvyr-kov, 1980), there is not a single reference tothe autoshaping literature. I hope that thepresent review reflects part of the powerfultrend in experimental psychology that prom-ises to provide a unitary framework for analy-sis for a variety of psychological phenomena.

TRADITIONAL VIEW OF THEORIENTING RESPONSE

The importance of the orienting reflex (OR)lies in its involvement in processes such as at-tention, perception, learning, and memory.However, the mechanism of how the ORcontributes to these psychological processes hasremained conjectural until now. The OR isusually defined in terms of a conjunction of

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stimulus and response properties. Pavlov(1927) viewed it as follows:

It is this reflex which brings about theimmediate responses in man and animalto the slightest changes in the worldaround them, so that they immediatelyorientate their appropriate receptor organin accordance with the perceptible equal-ity in the agent bringing about the change,making full investigation of it. (p. 12, ital-ics added)

According to Sokolov (1963), the OR possessestwo important characteristics: it is evoked bynovel, salient stimuli above the sensory thresh-old, and it decreases as a function of stimulusrepetition (habituation). Sokolov's neuronalmodel theory described the OR as an inborn(unconditioned), automatic by-product of anencounter with unfamiliar stimuli. Mismatchbetween model and current stimulus inputproduces "impulses of discrepancy" (Sokolov,1963, p. 289), which trigger an OR. Thus,what might be termed the traditional view ofthe OR is that it is a reflexive reaction to stim-ulus change, triggered by mismatch to a hypo-thetical neuronal model. However, it is diffi-cult to define stimulus novelty in operationalterms. Neutrality, salience, slightest change,novelty, and related terms are notoriously dif-ficult to define. They are not controllablephysical or physicochemical properties of thestimulus but always reflect a momentary re-lationship between the perceiving organismand the physical features of the test stimulus.Given a particular state of the organism, astimulus change may evoke an OR. In a differ-ent state that same stimulus change would not,or would do so to a lesser degree (Maltzman,1979; Ray & Brown, 1976). Consequently, the"threshold for novelty" (Sokolov, 1966, p. 352)will depend on stimulus antecedents and con-text within which the OR occurs. Since stimu-lus novelty is defined post hoc, as inferredfrom the reactivity of the organism, it cannotbe determined whether the absence of the ORreflects familiarity with the stimulus or a stateof reduced responsiveness with an increased"orienting threshold" (Sokolov, 1966, p. 352).Even if we accept that the OR is "a sign thatthe nervous system has detected a change inthe stimulus" (Sokolov, 1963, p. 283), its ab-sence does not guarantee that the stimulus

features have already been encoded in theneural model.Another problem with the traditional defini-

tion is that the OR does not habituate to allstimuli. A trivial but revealing example is theOR that we give upon hearing our own name.The subject's own name is considered to beparticularly effective in evoking an OR (Lynn,1966; Siddle, O'Gorman, & Wood, 1979). Spe-cies-specific "calls" are also very resistant tohabituation (Ploog, 1970). Thus, it appearsthat stimulus novelty is neither necessary norsufficient for elicitation of the OR. It seemspossible that there is a basic misunderstandingof the phenomenon under investigation. It isnot clear whether the function of the OR isbest characterized as enhancing the efficiencyof the nervous system for processing of thenovel stimulus or as preparing the organismfor efficient processing of future environmentalevents. In addition, as Siddle and Spinks (1979)pointed out, the novelty hypothesis involves alogical problem in that the novelty of a stimu-lus can be determined only once the stimulushas been analyzed. When this has occurred,there is no requirement for enhanced proces-sing because the stimulus has already beenidentified. Moreover, if stimulus novelty aloneis sufficient to evoke an OR, the reflex may bemaladaptive, in that the organism's ongoingbehavior will frequently be disrupted by en-counters with novel but nonimportant stimuli.From the foregoing analysis it appears that

the only acceptable definition of the OR re-mains its objective description in terms ofskeletal movements toward the stimulus sourceand correlative changes in the autonomicnervous system. The "nature" of the evokingstimulus remains to be defined, however.

STIMULUS SIGNIFICANCEAND THE OR

Several investigators have concluded thatthe data did not require a model that includeda matching process (Bernstein 1969; Germana,1968; Grastyan, 1961; Kahneman, 1973; Maltz-man, 1971). As early as 1968, Maltzman andMandell (1968) argued: "Stimulus change perse is not the critical factor nor sufficient to in-duce an OR" (p. 99). Bernstein (1969) ad-vanced the view that became known as thesignificance hypothesis of the orienting reflex

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(Bernstein, 1973, 1979; Bernstein, Taylor, &Weinstein, 1975). This view amplified earlySoviet opinions based on psychological inves-tigations of the handicapped. Zemtsova (1969)observed that blind subjects showed an aug-mented OR to auditory stimuli that was highlyresistant to habituation. She interpreted theseresults to mean that auditory stimuli havegreater significance for the blind than for thesighted subject. A similar conclusion wasreached by Tikh (1949) on a comparativepsychological basis. She found that sound stim-uli did not evoke an OR in the developingyoung of the ape. Children, on the contrary,were readily diverted by the sound. Tikh hy-pothesized that this difference could be tracedback to the different kinds of communicationsused by the two species.

In Bernstein's original experiment the gal-vanic skin response (GSR; Voronin & Sokolov,1960) was habituated to a visual stimulus. Thestimulus was then altered on a test trial. Allsubjects were able to report on experimentalinquiry that they had detected a change inthe stimulus, but only 47% responded to thechange with a GSR. Bernstein did not discarduncertainty or the mismatch process but sug-gested that an interaction between them andstimulus evaluation triggers the OR. O'Gor-man (1979) criticized the significance detectorhypothesis on several grounds. Most impor-tantly, he pointed to the inadequacy in arguingfor a revision of OR theory from a single setof data, in which only one component of theOR (GSR) was monitored (see also Barry,1977). Second, he drew attention to the dif-ficulties in coupling cognitive processes andphysiological response classes. Third, Bern-stein's conclusion was at variance with Vino-gradova's findings (1965). She reported that adefensive reflex was successfully conditioned toa metronome paired with an electric shock ina subject who showed no OR during condi-tioning trials. "Postexperimental inquiry re-vealed that the subject did not see any connec-tion between the stimulus; only with the helpof leading questions could she remember thatthe metronome was used in the experiment;she said she 'did not pay attention' to it" (p.52). Fourth, since there was no independentmeasure of significance, and judgments of "sig-nificant" were inferred solely on the basis oftest trial responding, the hypothesis has re-

mained tautological (O'Gorman, 1979; Siddle& Spinks, 1979).

However, there is a clear advantage of thesignificance hypothesis as opposed to the nov-elty notion: the significance of a stimulus canbe explicitly introduced and varied experi-mentally. Although we can never be sure thata stimulus is truly nonsignificant (neutral),we can at least vary its significance by alteringits correlation with an unconditioned stimu-lus (US).

CLASSICAL CONDITIONINGAND THE OR

The term classical conditioning implies theexperimental operations of CS-US pairingwhere the occurrence of CS and US is notcontingent upon behavior of the organism.The orthodox view of conditioning impliesthat subjects automatically associate appro-priately paired events. The general similarityof the form of the conditioned response (CR)and the unconditioned response (UR) observedin the salivation experiments led Pavlov toformulate his principle of stimulus substitu-tion (1927). Stimulus substitution predicts thatas a consequence of CS-US pairings, responsesevoked by the CS will be determined by USqualities (Jenkins & Moore, 1973; Konorski,1948, 1967; Pavlov, 1927). Several authors havesuggested alternative characterizations of thefunction of the CS; for example, "a learnedreleaser" (Woodruff & Williams, 1976), "objectsubstitute" (Hearst & Jenkins, 1974), or an"incentive stimulus" (Bindra, 1978).An often cited anecdote from Pavlov's labo-

ratory described a dog, which when let freeafter an experiment, ran to the metronome(CS) and began licking it (1934). If the estab-lished CS is within reach "the animal eventries to come in touch with it, namely; bymeans of its mouth. Thus, if the conditionedstimulus is the switching on of a lamp, thedog licks the lamp. . . In this way the condi-tioned stimulus actually stands for the animalin place of food" (p. 187). It is less known,however, that this incidental observation waslater painstakingly elaborated by Pavlov's suc-cessor, P. S. Kupalov. I will describe his ob-servations later. In the present context, it isenough to mention that this behavior wascertainly not a consummatory response re-

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leased by the US-surrogate (CS). On the firstpresentation of the signal (i.e., prior to CS-USpairing) "most often the dog turns his headtoward the stimulus and looks at it; less fre-quently he approaches it ... Some of the ani-mals sniff at it, touch it with a paw, or lick it"(Kupalov, 1969, p. 741).The discovery that the OR plays an impor-

tant role in conditioning originates from Pav-lov (1927). A previously habituated or a novelstimulus transformed into a CS evokes a largeOR (Grastyin, 1961; Luria, 1973; Luria &Vinogradova, 1959; Maltzman & Raskin, 1965;Razran, 1961, 1971). Since the OR lawfullyemerges during conditioning, it is regarded asa reliable predictor of learning (Grastyan &Vereczkei, 1974; Maltzman & Mandell, 1968;Sokolov, 1963). Once the learned connection is"firmly established, consolidated and automa-tized" (Sokolov, 1963, p. 292), the OR isclaimed to disappear (Bykov, 1958; Grastyan,1961; Lebedinskaya, 1965). The "orienting re-flex has the property to become extinguishedin the course of continuation of pairings"(Sokolov 1965, p. 150). During the formationof a CR, "an orienting response develops firstand later undergoes into the specific reactioncorresponding to the nature of the reinforce-ment employed" (Vinogradova, 1969, p. 714;italics in original). Does this imply that theOR is being gradually transformed into aUR-like consummatory response? There is alogical problem here: if the OR is directed tostimulus qualities of the CS (Holland, 1977;Prokasy & Ebel, 1967; Sokolov, 1963), how doesit facilitate the formation of the CR, which isinterpreted as being determined by US quali-ties through the process of stimulus substitu-tion?

MEASUREMENT OF THECONDITIONED RESPONSE

The question "what is a CR?" can be askedand answered in two general ways dependingon expectations and the depth of the dataanalysis. First, in terms of operational defini-tion: any change that differs significantly fromappropriate controls (Rescorla, 1967) is essen-tially regarded as the CR. The second ap-proach concentrates on its adaptive functionand meaning for the organism. What is its sur-vival value? How is it caused and controlled?How does it develop in the individual? And

how did it evolve in the species? (Simpson,1962; Tinbergen, 1968). The first approachconcentrates on the second of these questions.The problem with that approach stems fromthe difficulty in defining the "control" (Garcia,1981). The subject may associate a variety ofevents in a conditioning experiment, and thechange in behavior recorded by the experi-menter is simply a convenient index of theformation of these associations. If stimulussubstitution is the underlying mechanism ofclassical conditioning, then it is reasonable tolook for the "true" CR late in the CS-US in-terval (Gormezano, 1966; Martin & Levey,1978; Thompson, 1976). But what is the sig-nificance of other reactions that occur earlierin the CS-US interval? Furthermore, if thestimulus substitution principle proves to be aninsufficient account of conditioning, severalquestions arise. By way of illustration, con-sider the following example:1. Assume that the magnitude (or probability)of a response to a CS is a function of the on-going behavioral state: when the CS is pre-sented during Behavior A the response is twiceas large as the response obtained during Be-havior B.2. The structure of inter-CS behavior changesacross sessions in the following manner: InSession 1, presentation of CS coincides withBehavior A on half of the trials and with Be-havior B on the other half; by Session 10 theintersignal activities change so that presenta-tion of CS coincides with Behavior A on 90%of the trials and with Behavior B on 10%, ofthe trials.

It follows from postulates (1) and (2) that inthis hypothetical experiment there is an aver-age of 27% increase of responsivity from Ses-sion 1 (50 - 2X + 5OX = 15OX) to Session 10(90 - 2X + lOX = 190X) due to the change ofintersignal activities. Is the increase due toCS-US pairing? What is conditioned? Experi-mental data are available to support bothpostulates. In a Pavlovian procedure with ratsas subjects, the highest OR scores were ob-tained when sniffing was in progress at the mo-ment of CS occurrence and lowest when theanimals were engaged in grooming (BuzsAkiet al., 1979a, Experiment 4). Similar observa-tions were reported by Ray and Brown (1976).Changes in the intersignal structure of behav-ior are also well documented (Buzsaki et al.,

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1979a, 1979b, 1981; Ray, 1977; Ray & Brown,1976; Staddon, 1977). These intersignal effectsmight, at least partially, explain the trial-spac-ing effect of autoshaped key pecking (Gibbon,1977, 1981; Jenkins, Barnes & Barrera, 1981).Changes of the inter-CS interval may con-siderably affect the inter-CS structure of be-havior (Staddon, 1977), and consequently themagnitude of the CS-evoked response.The issue is not whether any behavioral or

autonomic changes occurring during the CS-US interval are the consequences of CS-USpairing, but whether any or all of them mightbe regarded as the "true" CR. In classical con-ditioning it is not only local reflexes, such assalivation, jaw and beak movements, licking,blinking, leg flexion, or nictitating membraneclosure, that are modified by the conditioningprocedure. These classes of behavior are rep-resentative of but one category of CRs, usuallyreferred to as consummatory responses (Craig,1918; Konorski, 1967), as opposed to a secondcategory of responses, preparatory CRs, whichare conditionable to CSs of longer duration(such as contextual and apparatus cues) anddo not necessarily produce discrete reflex re-sponses (Rescorla & Solomon, 1967). Sincenumerous components make up the CR, it isespecially important to study the order inwhich the various reflex components of theOR appear in conditioning. Dykman, Mack,and Ackerman (1965) reported that in dogsthe earliest reliable evidence of conditioningwas reflected by somato-motor reactions suchas eye-opening movements, perking of the ears,and head elevation. Autonomic measures(heart rate and blood pressure) showed altera-tions several sessions later. Further, somaticresponses outlasted vegetative responses in ex-tinction. Another problem with the exclusiveuse of autonomic measures, such as GSR, isthat the CS- and US-related responses cannotbe easily separated. It is essential for a CS thatit must not initially elicit the same responseas the US (Kling & Riggs, 1971). However,there is virtually no stimulus that will notelicit a GSR (Gormezano, 1966). Also, it is ofutmost importance to ascertain what controlsthe different responses during the CS-US inter-val.To overcome these difficulties a multiple

behavior-oriented methodology is requiredwhich is capable of describing behavioral flowand relating the various succession of responses

to eliciting events. Only in this way can onedecide whether the orienting components ofthe CR represent an essential part of the con-ditioned response.

CONDITIONED ORBiryukov (1965) exposed fox cubs to squeaks

of mice. OR was either not observed or habi-tuated rapidly upon repetition. However,when the cubs were allowed to chase and eatthe mice, such experience conditioned the ORto the squeaks that proved almost unextin-guishable. A similar way to produce prolongedORs is to require the subject to respond tothe stimulus. In this case the previously habit-uated OR is found to recover fully and tohabituate very slowly (Gruzelier & Venables,1973; Sokolov, 1963). The OR is unusuallypersistent in discrimination training, and is"as a rule, the stronger, the more difficult isthe discrimination" (Sokolov, 1965). If noveltyis the crucial dimension for eliciting an OR,it is hard to tell why the OR persists in a con-ditioning situation where the same physicalsignal recurs repeatedly. It is possible that theOR may reflect a more complex interactionthan was considered in Sokolov's conception ofan unconditioned "reflex receptor mechanism"(1960). A prerequisite for observing the signal-directed investigatory-orienting response is theuse of freely moving subjects. Among the firstinvestigators to use freely moving animals ina conditioning paradigm was Kupalov (1969,1978; Kupalov & Yaroslavtseva, 1949). Kupa-lov's situation reflex paradigm requires a sub-ject (always a dog) to go to a specific locationin the experimental environment. The targetlocation is marked by a carpet, usually a fewmeters from the food magazine. When the dogis situated correctly on the carpet, the condi-tioned signal, signifying the availability offood reward, is switched on by the experi-menter. The goal is to teach the animal to sitor stand on the carpet correctly until the de-livery of the CS, at which time the dog runs toreceive food at the appropriate location. Thelocation of the carpet and the CS (buzzer, met-ronome, or light) can be changed when re-quired.Kupalov and his associates repeatedly ob-

served that during the course of training, anincreasing tendency to orient toward the CSsource developed. This consisted of head turn-

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ing toward the CS and sporadically approach-ing it and licking it. Although similar re-sponses were observed in some dogs prior toconditioning (see above), the incidence of suchtransactions was considerably higher duringthe course of conditioning. Yakovleva (citedin Kupalov, 1978, p. 91) described that somedogs were unable to move from the soundingmetronome (CS), reached for it, and jumpedon the barrier behind which the metronomewas placed. Sometimes the dog stopped on itsway to the food bowl, returned to the metro-nome and intently watched it for several sec-onds, and only then, with some effort, turnedto the food bowl. Kupalov called this CS-directed response the "primary alimentarymotor reaction" differentiating it from the"secondary food reaction," which was directedtoward the food source (US). Kupalov's inter-pretation of these findings was that the startplace and the CS acquired the features of thefood stimulus and that the behavior of theanimal could be best described as like that ofa dog hunting or catching his prey.

Similar observations of the targeting reflexwere frequently made in Konorski's laboratoryusing a modified version of the place reflex,but these were interpreted as pathologic mag-net reactions (Stepien 1974; Stepien, Stepien, &Konorski, 1960) or a result of "parasitic" in-strumental contingencies hidden in classicalcontingencies (Konorski, 1967; Konorski &Lawicka, 1959; Lawicka, 1979).Dramatic signal-directed tendencies were re-

ported by Grastyan and Vereczkei (1974) withcats as subjects. They used Kupalov's situationparadigm with the auditory CS placed be-hind the starting platform. It was found thatapproach to and contact with the CS-source(a loudspeaker) developed in the course of con-ditioning. In some animals this orienting ten-dency transiently suppressed the goal response,and the cats even refused food that was offeredby the experimenter. The authors attributedthis behavior to the conflict between CS-di-rected tendencies and the goal-directed in-strumental response. Based on these observa-tions Grastyan and Vereckei (1974) offered acomplete reinterpretation of the role of theOR in conditioning. In essence, they proposedthat under the effect of reinforcement the CSbecomes a new goal, and that is why the ani-mal approaches it instead of the old goal (thefood magazine). Further, they suggested that

the occurrence and persistence of the "instru-mentally conditioned orienting response" (p.128), claimed to be a sufficient condition forlearning, may also be the only necessary con-dition. Most important, they pointed to theadaptive function of the signal-directed OR:in nature, where signal and signaled usuallycoincide, approach to the signal results in foodreward.

Since the Kupalov's place reflex is basicallyan instrumental paradigm in which the signaloccurs as a result of subject-experimenter in-teraction (Ray, 1977), it was not possible totell whether the signal-related activities weredue to a Pavlovian CS-US relationship or alearned operant response-reinforcer relation-ship. This problem will be elaborated uponlater.

Since the skeletal components of the OR aredefined in terms of signal-centered behavior(e.g., directing the eyes and head toward thesource of the stimulus), we asked whether sim-ilar responses emerge and persist during thecourse of classical conditioning.Our experiments were conducted in a large

experimental cage with cats as subjects. Thesource of the auditory CS (the loudspeaker)was placed on the wall opposite the foodmagazine. The purpose of the spatial separa-tion between CS and US was to permit a clearseparation between approach to the signalsource and approach to the site of the rein-forcer. The CS (2 sec long, 500-Hz tone) wasautomatically followed by the US (raw meat).A daily session consisted of 20 trials. Intertrialintervals ranged from 20 to 80 sec. In a sub-group of animals CS-US pairing was followedby extinction and discriminative recondition-ing. In the discriminative phase, CS + andCS - (both tone signals) were delivered fromthe same loudspeaker. The CS-directed be-havior of the cat was rated on a 4-point scalein the following manner: '1' was given forpricking of the ears or turning of the headless than 300 towards the source of the CS, '2'for turning 30 to 900, '3' for greater than 900of head turning and/or stepping towards theloudspeaker. Zero was given for a responseother than towards the source of CS regardlessof its magnitude (e.g., scratching, ambulation,grooming, jumping to feeder). OR scores weresummed for a day resulting in a maximumdaily score of 60 for an individual animal.This subjective description was complemented

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by objective indexes, such as eye-movementrecording, neck-muscle electromyogram, andhead-movement recording (for further detailssee Buzsiki, Grasty.an, MolnAr, Tveritskaya, &Haubenreiser, 1979a; Buzsaiki, Haubenreiser,GrastyAn, Czopf, & Kellenyi, 1981).

Figure 1 illustrates the development of theOR during CS-US pairings, extinction, andtwo-tone discrimination. In the course of 300to 700 trials, the OR to the reinforced stimulus(CS+) did not decrease, whereas the OR tothe nonreinforced stimulus (CS-) did decrease.Responses during the CS-US interval fell re-liably into two classes: (INI) initial behaviorearly in the CS-US interval corresponding toOR toward the source of the CS; (TER) ter-minal behavior that consistently occurred justbefore food delivery and was directed towardthe food magazine (Staddon & Simmelhag,1971). TER included activities like turningof the head back to the food magazine, sniffing,pawing, and occasionally jumping to thefeeder.This "two-phase" responding was already

evident in the first conditioning session. Thetime-course of INI and TER behavior withina single trial varied with training, showing ageneral decrease of the INI/TER ratio. It wasa consistent observation that if the head ofthe animal was already directed toward theloudspeaker, presentation of CS evoked aquick head jerk toward the food magazine.The data of this experiment indicate that in aPavlovian situation OR toward the CS persists

Cond

60-

50-

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c' 30-c

20-

10-

Ext Discr

cs+

--- cs-

l 5 10 15 20 25 30 35Sessions

Fig. 1. A representative orienting response curve in asingle cat during classical conditioning (Cond), extinc-tion (Ext), and two-tone discrimination (Discr). Ordi-nate: total orienting score per session. Solid line: re-sponses to CS+; dashed line: responses to CS-.

throughout conditioning. This occurs eventhough it is always the TER, not the INI, thatis contiguous in space and time with food rein-forcement.However, in the Pavlovian arrangement

there is no independent measure of learning.Thus, we could not demonstrate how the de-velopment of OR correlated with learning perse. Also, in the classical conditioning situationthe occurrence of US might not only reinforceCS-related behavior but interfere as well withthe OR in progress. If, however, the occurrenceof US is paced by the subject, this latter prob-lem can be eliminated. The discriminated in-strumental procedure fits this requirement.

In a second experiment we compared thedevelopment of the OR with the decrease ofintertrial (CS-off period) responding. The lat-ter was regarded as an index of learning. Theapparatus was the same as that used in the clas-sical conditioning experiment. The upper partof the protruding food magazine was convertedinto a pedal by placing a microswitch belowthe panel. In addition, a pneumatic pressuretransducer was connected to the pedal. Eachcat was put into the apparatus for half anhour daily for 5 to 7 consecutive days (adapta-tion). On the last day of the adaptation phase,the tone signal was presented 20 times with anintertrial interval of one minute (habituation).Next, the animals were handshaped to pressthe pedal in order to obtain a food reward.In the go, no-go discrimination phase onlythose presses that occurred in the presence ofthe tone CS were rewarded. The CS wasswitched on by the experimenter and termi-nated by the cat's lever press. Those pressesthat occurred in the absence of the CS weretermed intertrial pedal presses (ITP). BesidesCS-directed responses prestimulus behavior(PRE, during the 1.0 sec preceding CS), likeambulation, standing, sitting, lying, grooming,abortive pressing, etc., and the position of thehead (relative to the source of CS) were alsorecorded. The principal findings are shown inFigures 2 and 3.The most striking finding was the low level

of responding to the tone signal during habit-uation and in the first conditioning sessions.In fact, some of the animals did not respond tothe tone at all. This observation is contrary tothe general belief that novel stimuli will in-variably elicit an OR. Some earlier observa-tions, however, corroborate this finding. Kar-

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(a 130W; 120co 110W 100

X 900.o-j 70.

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during the interval" (p. 391). Since in our ex-periment the occurrence of US was response-dependent, the explanation that these oscilla-tions represented induced interim activity, dueto the delay of US, can be excluded.To summarize, the spatio-temporal separa-

tion of the CS and US allowed us to analyzeINI and TER behavior separately. The inversecorrelation between the number of errors andORs left little doubt that the OR occurred asa result of conditioning. The identical topog-raphy of the CS-directed behavior and theORs to the same physical signal prior to con-ditioning (habituation) suggested that the un-derlying mechanism might be the same. Sincesignal-directed activity built up as a conse-quence of conditioning, then by definition, itwas a conditioned OR.The persistent nature of the OR has also

been reported in several experiments usinghuman subjects. Although the OR is com-monly described as a generalized, holistic re-sponse with both skeletal and autonomic com-

ponents, measurement in humans is usuallyrestricted to its autonomic components. Thegalvanic skin response (GSR) appears to be theindex most frequently used (Badia & DeFran,1970; Barry, 1977). The multiple GSR re-sponses occurring in the CS-US interval areclaimed to represent different processes (Pro-kasy & Ebel, 1967). Stewart, Stern, Winokur,and Fredman (1961) recommended a responselatency criterion to separate the GSR com-ponent. The CS-response (the OR or firstresponse) is claimed to be determined by stim-ulus qualities (Prokasy & Ebel, 1967). The pre-US response (late or "second" response) is re-lated to expectancy and anticipation of theUS (Grings, 1977; Lockhart, 1966; Ohman,1971, Stewart et al., 1961). Prokasy and Ebel(1967) showed the CS and pre-US responsesto be independent both in terms of condi-tional probabilities and in terms of suscepti-bility to changes of CS and US variables. Ifthe above analysis is correct, then accordingto the classical notion of the OR, parallel with

S O s s I on

4

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-XE, WoJt,.4

- w ~~u ILFig. 4. Competition between signal-directed and goal-directed tendencies in an early and a late session. 1, electro-

oculogram; upward deflections: saccadic eye-movements to the right (towards the source of the signal); downwarddeflections: eye-movements to the left (towards the food magazine). 2, force of lever pressing; arrows indicate pressesand release of the lever. 3, heavy line: discriminative signal; downward deflection: switch closure. Note frequentgaze shifts between signal and food magazine, and the gradual increase of force of lever pressing on each trial. Cali-brations: 1 sec, 1 mV; .5 N.

2

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GYoRGY BUZSAKI

the development of the pre-US response, theCS-onset response should adapt. Gale and as-sociates (Gale & Ax, 1968; Gale & Stern, 1967,1968) and Ohman (1971, 1972) did not findthis to be the case. Rather they found that theCS-onset component did not diminish afterseveral hundreds of CS-US pairings. Both ORand pre-US anticipatory components reachedmaximum within the first few trials and re-mained throughout the conditioning series.Other response systems show similar charac-teristics to the GSR. This is particularly trueof evoked brain potentials. The late compo-nent of the contingent negative variation(CNV) is commonly associated with anticipa-tion, preparation, and- expectancy of the US(TER). More recently, the early component ofthe CNV (INI) has been associated with ori-enting behavior and shown to be resistant toCS-US repetition (Callaway, 1975; Hillyard &Galambos, 1967).These findings are difficult to reconcile with

Sokolov's view that an OR is produced as aconsequence of mismatch alone, independentlyof any other stimulus attributes (1960, 1963;Pribram & McGuinness, 1975). It seems clearfrom the above discussion that since Pavlov's(1927) original description of the "what is it?"reflex, the range of OR-eliciting conditions hassteadily expanded. It has been demonstratedthat an OR is never a consequence of stimuluschange alone. On the other hand, pairing astimulus with a positive reinforcer will invari-ably induce CS-directed responding. The sup-port for the notion of the CS response (INI) asrepresenting conditioned orienting behavior isvery strong.

AUTOSHAPINGIn their influential paper Brown and Jen-

kins (1968) reported that hungry pigeons be-gan to approach and finally peck a lighted key(CS) if illumination of the key signaled thatfood (US) was forthcoming. In this classicalconditioning paradigm, key pecking had noconsequences, yet virtually each CS presenta-tion reliably evoked it. Since this behaviorrequired no hand shaping, the term autoshap-ing was adopted. A more descriptive term, signtracking, was suggested later by Hearst andJenkins (1974). Although pigeons have been byfar the most popular subjects for this kind ofresearch, a number of studies have demon-

strated its existence in a variety of species(Hearst & Jenkins, 1974). The consistent find-ing that pigeons do not peck the source of anauditory CS has led some investigators to sup-pose that for the pigeon "auditory cues by theirnature are not readily localizable" (Bilbrey &Winokur, 1973; Burt & Westbrook, 1980, p.305; Schwartz, 1973). This conclusion is prob-ably inadequate in the light of the neuro-physiological evidence that the "spatial map-ping" system does not reside in specific sensorysystems (Buzsaki, GrastyAn, M6d, & Winiczai,1980; O'Keefe & Nadel, 1978; Whittington,Hepp-Reymond, & Flood, 1981). A possibleexplanation for the lack of pecking to audi-tory targets is offered by experiments showingthat visual cues in birds play a primary rolein food selection (Wilcoxon, Dragon, & Kral,1971).

Several excellent reviews of the autoshapingliterature appeared recently (Davis & Hurwitz,1977; Dickinson & Boakes, 1979; Honig &Staddon, 1977; Locurto et al., 1981).The conclusion of the vast amount of auto-

shaping research can be summarized briefly:if you allow an animal to move freely, it willapproach and contact localizable stimuli pre-dicting positive reinforcement. The main goalof this review is to argue that this signal-directed behavior is a conditioned orientingresponse. If, in a response-independent para-digm, a tendency to approach a positive CSdefines the autoshaped response, then the con-ditioned OR meets this criterion. From thisviewpoint, autoshaping is not a new phenom-enon, but rather, a new way of looking atan old paradigm (Buzsaki, Grastyain, Molnar,Tveritskaya, & Haubenreiser, 1979a).

Theoretical accounts of autoshaping (Hearst,& Jenkins, 1974; Jenkins, 1973, 1977; Mackin-tosh, 1974; Moore, 1973) do not share thisview. First and most important, the learnedOR is seen as a newly acquired preparatorybehavior suppressing the consummatory act ofeating, whereas the autoshaping response isgenerally interpreted as being a signal-triggeredconsummatory activity (Jenkins&Moore, 1973;Locurto, 1981; Moore, 1973; Peterson, Ackil,Frommer, & Hearst, 1972). Second, the auto-shaped response is commonly explained bysubstitution, surrogation, and generalizationprinciples (cf. Hearst & Jenkins, 1974) and assuch determined mainly by the qualities ofthe US, whereas the topography of the condi-

470


tioned OR is determined primarily by thequality and spatial location of the CS (Hol-land, 1977; Prokasy & Ebel, 1967; Shettleworth,1978; Wyrwicka, 1972). For example, Jenkins& Moore (1973) reported that exposure to CS-US pairings caused the pigeon to peck the CSlight spot in a way that resembled the consum-matory reaction evoked by the reinforcer (eithergrain or water). Also, rats showed differentresponses to the lever CS depending uponwhether it signaled food or brain-stimulationUS (Peterson et al., 1972). After a number ofpairings of CS and food US, the rats ap-proached and contacted the lever with theforepaws (touching and pressing) or with themouth (gnawing and licking). Approach andcontact of the lever also occurred with brainstimulation US, although less oral respondingand more sniffing was observed. A note of cau-tion is in order here: the descriptions of CS-directed tendencies with the two types of USsin the Peterson et al. study may reflect a dif-ference more of the degree than of the kind.This might simply be attributed to the differ-ent magnitude of the reinforcing effects of foodand brain stimulation USs.Other autoshaping experiments question the

stimulus substitution explanation (Boakes,1977; Gamzu gc Williams, 1971; Hogan SeRoper, 1978; Shettleworth, 1978; Woodruff &Starr, 1978). For example, Wasserman (1973)reported using heat reinforcement to sustainkey pecking in chicks. The appropriate URto heat is wing-flapping, not pecking. Wood-ruff and Williams (1976) used a lighted keyas CS and water-US injected directly into themandibles of unrestrained pigeons, and ob-served that the CS-related response (approach,bowing, rooting) was dissimilar to the US-elicited response (swallowing). They, togetherwith Timberlake and Grant (1975), concludethat a biologically preorganized behavior sys-tem is conditioned to the CS, and those re-sponses in the behavior system that are "re-leased" or "elicited and supported" by the CSconstitute the autoshaped response. Further,in higher order autoshaping experiments (BurtSc Westbrook, 1980; Holland, 1977; Leyland,1977; Nairne & Rescorla, 1981; Rashotte, 1981;Rashotte, Griffin, & Sisk, 1977; Rescorla, 1980)the topography of the second-order CR doesnot depend on the response evoked by thefirst-order reinforcing CS.Although this latter group of experiments

lends support to the view that "preparatory" isan apt description of the autoshaped response,it is not clear why in other experiments theCS-directed response resembles the US-relatedresponse. I suggest that the degree of spatialdiscontiguity between CS and US might beresponsible for the divergent results. In ourexperiments spatial separation of CS and USsites allowed a clear distinction between INIand TER behavior. TER (US-directed) activi-ties definitely showed some resemblance to theUR (biting screws on the wall, nosing, paw-ing, and scratching the magazine wall). It ispossible that the autoshaped responses thatshowed resemblance to the UR were actuallyTER responses. In the experiments of Wasser-man (1973), Timberlake and Grant (1975), andWoodruff and Williams (1976) separation ofINI and TER responses was relatively easysince the locations of CS and US were far apart.In a more typical autoshaping arrangement CSand US sites are closer and are usually placedon the same response panel (e.g., Jenkins &Moore, 1973). Consequently, distinction be-tween INI and TER behavior may be moredifficult. The spatial proximity of CS and USand the relative dominance of TER late inconditioning might explain why the topog-raphy of the autoshaped response is judged asresembling the UR. The topography of TERbehavior depends on the type and strength ofthe reinforcer also in situations where time isthe only variable that signals the imminenceof reinforcement (Anderson & Shettleworth,1977; Hurshman Sc Moore, 1976; Reberg,Mann, & Innis, 1977; Staddon, 1977). In sec-ond-order conditioning when both first-orderand second-order stimuli were presented onthe same key, the second-order CS showed sen-sitivity to the current value of the first-orderCS. However, autoshaped responding to asecond-order CS paired with an auditory first-order CS, delivered from another location, wasrelatively insensitive to changes in that first-order stimulus (Nairne & Rescorla, 1981). Thatsome part of pecking behavior may correspondto TER activity is supported by Moore (1973).He noted that autoshaped pigeons occasionallyabandon the CS key to peck down the wall tothe US site.Boakes (1977, 1979) distinguishes goal-track-

ing (TER) from sign-tracking (INI) behavior.When compared with goal tracking, sign track-ing develops faster, is more strongly sustained

471

GYoRGY BUZSAKI

by partial reinforcement, and extinguishesmore slowly. He argues that goal tracking maybe regarded as a form of consummatory re-sponding and sign tracking as a form of prepa-ratory behavior (1979). "Two-phase" responseswere also observed in monkeys when presentedwith discrimination problems in which the dis-crimination stimulus was spatially discontigu-ous with the site of the instrumental response(Polidora & Fletcher, 1964; Polidora & Thomp-son, 1965). The monkeys invariably looked atthe site of the stimulus and touched it beforeexecuting the required instrumental response.The distinction between INI and TER re-

sponses is further supported by experiments inwhich the magnitude of reinforcer was manip-ulated. A CS paired with a higher magnitudeUS evoked strong key pecking in the earlyportion but weak pecking in the later portionof the CS-US interval (Gibbon, Farrell, Lo-curto, Duncan, &c Terrace, 1980; O'Connell &Rashotte, 1982). In agreement with the presentanalysis, these authors concluded that the rela-tively weak key pecking late in the CS periodis due to the strong tendency to approach theUS site (TER) when the US magnitude orprobability are high.The foregoing analysis lends support for the

claim that the conditioned OR (INI) and thesign-tracking component of the autoshapedresponse are identical. The conditioned ORapproach shares several features of the sign-tracking formulation but is couched in a dif-ferent conceptual language.A widely discussed problem of associative

learning is the occasional lack of conditioningdespite CS-US temporal contiguity. These re-lated phenomena are termed "overshadowing"(Mackintosh, 1974; Pavlov, 1927) and "block-ing" (Kamin, 1961). The compound signalsused in these experiments are almost exclu-sively stimuli of different modalities (e.g., lightand tone). None of the experiments in thisresearch area has addressed the question ofhow the degree of spatial discontiguity (rela-tive to US) and localizability of the stimuliaffect "overshadowing" or "blocking." The ob-servation of Schwartz (1973) is relevant here.During an initial phase of an autoshaping ex-periment, food was delivered in the presenceof a tone CS. No pecking occurred in thisphase. In a subsequent phase the occurrenceof food was signaled by a compound CS con-sisting of the tone and a lighted response key.

This latter, easily localizable portion of thecompound CS did sustain key pecking; thatis, no blocking occurred (see also Gibbon,1981; Tomie, 1976).

STIMULI SIGNALINGAVERSIVE REINFORCERS

Protopovov (1909, cited in Skipin, Ivanova,Kozlovslaya, & Vinnik, 1969), working in Bech-terev's laboratory, was probably the first inves-tigator of conditioned defensive reflexes. Theprocedure is identical with the salivation ex-periment: the CS and the aversive US are pre-sented independently of the subject's behav-ior. In this procedure, therefore, the behaviorof the animal does not attain its chief pur-pose-avoidance of a noxious stimulus (Bolles,1970; Skipin et al., 1969). In a modified ver-sion, the CS signals that the aversive event isimminent but the subject can avoid it byactive responding (Bechterev, 1933). Several in-vestigators argue that there is a critical differ-ence between procedures with avoidable andunavoidable aversive stimuli (Bolles, 1970;Seligman, 1970). The unique feature of avoid-ance procedures is the fast rate of learning.Signals correlated with dangerous events maybe avoided after a single pairing (Bolles, 1970;Garcia & Ervin, 1968; Seligman, 1970). Bur-stein (1977) argues that "any population whichrequired 5, 10 or 20 trials or experiences toacquire a fear response to the sight or soundof a dinosaur would be destined for rapid ex-tinction" (p. 122). By contrast, when an aver-sive stimulus is unavoidable, subjects may fleeor engage in aggressive behavior and finally re-sponse tendencies become suppressed and thesubject may fall asleep (Bolles, 1970; Pavlov,1927).As in appetitive situations, the importance

of the CS location and CS-related activities re-ceived little attention in aversive conditioningprocedures. The marked facilitation of avoid-ance learning by separation of stimulus andresponse, described by Biederman, D'Amato,and Keller (1964), remained unnoticed, per-haps because it arrived in a theoretical vac-uum. The use of houselight flashes and plac-ing the source of an auditory CS outside theexperimental chamber have remained com-mon practices.

Recently, we investigated the effect of anunavoidable aversive event on the OR (Buz-

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saki, Grastyan, Molnir, Tveritskaya, & Haub-enreiser, 1979a; Buzsaiki et al., 1981). Follow-ing appetitive conditioning, the CS previouslypaired with food was paired with an electricshock to the neck region of the cat. As a conse-quence, the previously established OR towardthe CS source markedly diminished (Figure 2).When rewarded trials were interspersed amongaversive trials, CS-directed tendencies variedsystematically according to the opposite con-sequences of the same CS (Figure 5).

Recent experiments of Hearst and his col-leagues (Hearst & Franklin, 1977; Karpicke,Christoph, Peterson, & Hearst, 1977) also em-phasize the importance of CS localizability inaversive situations. In the Karpicke et al.study, rats performed an intermittently rein-forced operant response and received periodicpresentation of a visual CS for foot shock lo-cated either very near or far from the operantmanipulandum (Experiments 4 and 5). Pres-entations of the near CS resulted in markedsuppression of the operant response, whereasthe far CS was without effect. Periodic obser-vations revealed that the rats of both groupstended to restrict their activities to parts ofthe apparatus away from the CS source. Simi-lar withdrawal from a localized CS was alsoobtained in pigeons when the CS predictedthe absence of food (Hearst Sc Franklin, 1977;Jenkins & Boakes, 1973).An alternative to avoidance of the aversive

CS is elimination of its source from the sub-ject's environment. Hudson (1950) observedthat rats often sprayed bedding material to-ward and over (i.e., buried) stimulus objectsassociated with an aversive US. Localizability

OR

21 'x , / ' A * */ t R - rpeuwarhd1 J9 ' \t/ * ~~~~~5P -punishment

R P P P P RR P P PP P P R R

blocks of 5 t r a I s

Fig. 5. Orienting scores (OR, right ordinate) and thenumber of escape attempts (left ordinate) during suc-cessive food-reinforced (R) and shock-reinforced (P)blocks of trials within a single session in cat M 16.Note the inverse relationship between OR and escapeattempts.

of the CS source is prerequisite to this buryingresponse (Pinel & Treit, 1978). Calhoun (1963)described numerous examples of burying be-havior as a viable defensive response of rodentsin the wild. More research is required toelucidate how animals cope with aversive CSs.The available evidence suggests that subjectsdo not approach or make contacts with thesource of CS, but rather behavior is directedaway from signals of aversive CSs.These same studies provide support for the

view that it is not the novelty, uncertainty, ormismatch of the CS that attracts or repels thesubject. The acquired affective "charge" (i.e.,rewarding or aversive) seems to be the relevantdimension.

STIMULUS-REINFORCER VERSUSRESPONSE-REINFORCER

CONTINGENCIESIt is common practice to make a distinction

between Pavlovian and instrumental proce-dures. The Pavlovian procedure, by definition,is a response-independent paradigm, whereasin the instrumental (or operant) procedure, oc-currence of the reinforcer depends on the prioroccurrence of a specified response (Hearst,1975; Konorski, 1948, 1967; Rescorla & Solo-mon, 1967; Skinner, 1938). Both proceduresinvolve temporal sequences of events: stimulus-response-reinforcer. Because the US used in aPavlovian arrangement can usually serve alsoas an instrumental reinforcer, a response thatoccurs in the presence of the CS might beadventitiously reinforced and emerge as a con-sequence of instrumental rather than Pavlov-ian contingencies (Amsel, 1972; Herrnstein ScLoveland, 1972; Jenkins, 1977; Kimble, 1961;Konorski, 1967; Schwartz & Williams, 1972;Skinner, 1948, 1969). The CS-directed behavioroccurs on the first occasion for some unspeci-fied reason, is accidentally contiguous in timewith the occurrence of the US, is strengthenedby an instrumental contingency, and is thusmore likely to occur again. This results inrepetitive, stereotyped "superstitious" (Skin-ner, 1969) or "parasitic" (Konorski, 1967) be-havior. Indeed, preliminary training in aninstrumental procedure might facilitate the ac-quisition of the autoshaped key peck (Davol,Steinhauer, Sc Lee, 1977; Jenkins, 1977;Schwartz, 1973). The adventitious reinforce-ment hypothesis arose from a tacit assumption

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GYoRGY BUZSAKI

that response-reinforcer contingencies aresomehow more fundamental than stimulus-re-inforcer contingencies (Staddon, 1977). If the''superstitious" instrumental reinforcement isresponsible for the emergence and mainte-nance of the conditioned OR and autoshapedkey pecking, then the theoretical value of thephenomenon is zero.One way to distinguish between the Pavlov-

ian and the adventitious-instrumental accountsof autoshaping is to make the occurrence ofthe key-pecking response physically impossibleduring training. Such an experiment was re-ported by Breland and Breland (1961). Chick-ens were trained in an operant box to pull aloop for food reinforcement. This response atthe same time released a small ball (CS) in aminiature baseball field placed alongside thetraining box. When they removed the cagefor photography,

chickens that had been well conditionedin this behavior became wildly excitedwhen the ball started to move. Theywould jump up on the playing field, chasethe ball all over the field, even knock it offon the floor and chase it around, peckingit in every direction, although they neverhad access to the ball before. This be-havior was so persistent and so disruptive,in spite of the fact that it was never rein-forced [italics mine], that we had to rein-state the cage. (p. 683)

A more formal experiment of this kind wasdone by Kirby, Muir, and Moore (cited inMoore, 1973). After extended training withan inaccessible but visible CS key, the pigeonswere given access to the key during unrein-forced test trials. "When the key was firstilluminated, eight of the nine animals ap-proached it within seconds" (p. 164). Similarbehavior was observed by Zentall and Hogan(1975), Wasserman, Hunter, Gutowski, &Bader (1975), and Pavlov (see above). A secondprocedure relevant to the evaluation of Pav-lovian vs. instrumental contingencies is theomission-training procedure (Sheffield, 1965),in which reinforcement occurs only on thosetrials in which the CR did not occur. Theomission procedure has resulted in rathermixed results. In all studies the omission con-tingency diminished CS approach tendencies.However, the magnitude of the effect variesgreatly across studies. In the majority of theexperiments, despite reduction of the auto-

shaped response, the omission procedure nevereliminated completely approach to a CS forfood (Atnip, 1977; Barrera, 1974; Bilbrey &Winokur, 1973; Davey, Oakley, & Cleland,1981; Griffin & Rashotte, 1973; Jenkins et al.,1978; Locurto, Terrace, & Gibbon, 1976;Lucas, 1975; Patten & Rudy, 1967; Peden,Browne, & Hearst, 1977; Stiers & Silberberg,1974; Wasserman, 1973; Williams & Williams,1969; Woodward, Ballinger, & Bitterman,1974). In other studies an omission contin-gency completely eliminated signal-centeredresponses (Boakes, 1977; Gamzu Sc Schwam,1974; Powell & Kelly, 1976; Wessells, 1974;Woodruff & Williams, 1976).

In addition, Jenkins (1973) and Wessells(1974) criticized the validity of omission-train-ing results. They argued that although keypecking per se results in loss of reinforcement,prepecking approach tendencies such as orien-tation might be adventitiously reinforced oneach trial. Such a modified operant interpreta-tion, they suggest, could handle the omissionfor pecking results. One potential problemwith this kind of reasoning is that of infiniteregress. If all overt behavior is punished byomission of food, movement antecedents (e.g.,perception or subjective evaluation of the CS)might still be consistently reinforced (Peden,Browne, & Hearst, 1977). Both Dickinson andMackintosh (1978) and Staddon (1977) arguethat the finding that CS-directed movementscan be modified by their consequences doesnot force the conclusion that acquisition ofthe response depended on accidentally presentinstrumental contingencies (see also Jenkins,1977; Locurto, 1981).We used a different rationale to examine the

possibility of the adventitious operant ac-count. Rats were trained under signal (SD) +reward (Rd) spatial-contiguity condition.Whether the animal learned to approach thesame place in the apparatus (Rd) or the samesingle cue (SD) was determined by testingunder SD-Rd spatial discontiguity conditionslong after performance had been stabilized. Inthis test the animal could approach either SDor Rd but not both. Note that the initial con-dition mimics the alimentary conditions ex-perienced by animals in their normal habitat.Because under natural circumstances the stim-uli signaling food and the food itself are in-separable, an animal approaching the relevantstimulus ipso facto approaches food. In the

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p L p09SD-Rd -b SD4+Rd

1=p

LSD

pDM

SD+Rd - SD-RdFig. 6. Schematic of the experimental design. LS, loudspeaker delivering the discriminative signal (SD); DM,

drinking magazine delivering water reward (Rd); L, lever; P, photocell.

laboratory, however, we can separate the cuefrom its significate.The animals were trained in a straight alley

to repeatedly press a lever placed at one endof the alley until a discriminative tone signal(SD) appeared and then to run for a water re-ward (Rd) available at the other end (Figure6). The SD was automatically switched onafter a random number of lever presses (2 to 6;VR4). The acoustic signal was delivered byone of the two miniature loudspeakers placedabove the lever and drinking magazine, re-spectively. Light beams and phototransistorswere located 30 cm from both the lever paneland the magazine panel. The following behav-ioral measures were recorded: lever-press dura-tion, start time (latency from SD onset to thebreaking of the lightbeam close to the lever),run time (time elapsed between breaking ofthe two successive photobeams), return time(time elapsed from the end of water availabil-ity to the next lever press), session time (dura-tion of a session to complete 20 trials), ap-proaches to the magazine in the absence of SD(intertrial runs), lever-press perseveration (ad-ditional lever presses after SD onset), the num-ber of occurrences of grooming and rearing,the number of fecal boli, and lever-press to-pography.

In the initial phase of the experiment, forone group of rats the SD was presented fromthe loudspeaker above the drinking magazine(i.e., spatially contiguous with reward); an-other group was trained with SD deliveredthrough the loudspeaker above the lever (spa-tially discontiguous condition). Both groups

were trained for ten consecutive days. In thenext phase of the experiment, the sites of SDdeliveries were reversed. The issue was whetherchanging the source of the acoustic conditionedsignal has any effect on behavior.The principal findings are shown in Figure

7. The spatial location of the signal had adifferential effect on the two groups. The ini-tially discontiguous group spent more time inthe lever area after presentation of the signaland perseverated more. When SD was pre-sented from above the water magazine, thelatency to leave the lever area decreased inthis group. The major question of interest wasthe behavioral change of the initially contig-uous group in the second phase of the experi-ment. Positioning SD above the lever causedsignificant increases of lever-press duration,start time, perseveration, rearing, intertrialrun, and defecation measures. After the pre-sentation of SD, some animals ran down thealley and returned without drinking and re-sumed lever pressing. The explanation offeredfor the results was that the rats learned toapproach the SD and maintained this behaviorthroughout conditioning. Spatial discontiguityof SD and reward merely helped to uncoverthis signal-directed tendency (Buzsaki et al.,1 979b).Since the direction and topography of motor

behavior during testing under the SD-Rd dis-contiguity condition was markedly differentfrom the behavior learned under the SD + Rdcontiguity condition, adventitious instrumen-tal contigencies could play no role in the de-termination of SD-controlled behavior. Several

475

0

GYORGY BUZSAKI

5

-4u

w 3.E

_6 2 -0

1 -

o-

r) O (SD -Rd)- (SD- Rd)

* 1 (5D. Rd) -(SD-Rd)

R\

g~~~~~~~~O 0a

-0

CRF 1 2 3 4 5 6 7 8 9 10 1 2 3 4 5Fig. 7. Total time (start + run times) and lever-press

perseveration measures during successive sessions for thediscontiguous-contiguous (unfilled circles and col-umns) and contiguous-discontiguous (filled circles andcolumns) groups. CRF is last session of continuous rein-forcement stage. Note that SD rearrangement differen-tially affects the two groups.

other observations argue against an adventi-tious reinforcement account in the present ex-periment. Many responses (e.g., sniffing, rear-ing), more prevalent than OR to SD in the firstsession, were eliminated by the end of training,although these classes of behavior were ini-tially more proximal (both in space and time)to the reinforcer than SD-directed activities.On the basis of the "superstitious" account,one might expect that rats would have rearedand sniffed with increasing probability closeto the magazine. Likewise OR to SD wouldhave dropped out since responding to SD hadno direct associative linkage with water rein-forcement. However, the opposite was found.We can conclude that some contingencies areeffective in controlling some responses but notother responses, and that certain kinds of be-havior (e.g., conditioned OR, sign tracking)occur with both response-independent andresponse-dependent procedures. These findingsare important for at least one reason. Theydemonstrate that the artificial separation ofcue and significate is not a requirement for theemergence and maintenance of the conditionedorienting response. Spatial separation is a toolbut not a cause! Quite the contrary seems to bethe case: pigeons approach the CS less oftenwhen the CS and US are far apart than whenclose together (Peden et al., 1977). Associationsare more easily acquired between events thatare spatially contiguous (Testa, 1975), but notimpossible when they are separated (Grastyan

& Vereczkei, 1974). An instance of this unnatu-ral situation was recently studied in humanneonates (Alegria & Noirot, 1978). Head, eye,mouth, and crying responses were recorded inbreast-fed and bottle-fed babies. A breast-fedbaby, when in his mother's arm (whether it isthe left or right), will find the nipple of thebreast by orienting the upper lip towards thesource of the mother's voice (CS + US spatialcontiguity). For a bottle-fed baby the situa-tion is quite different. A right-handed motheralmost always takes the baby in her left arm,the bottle in the right hand, and gives it to thebaby with the wrist slightly turned towardsthe body. As a consequence, the baby will findthe "nipple" by mouthing to the left, that isin the direction opposite to the source of themother's voice (CS-US spatial discontiguity).Breast-fed babies were found to orient bothhead and mouth in the same direction. Bottle-fed babies were likely to orient their headstowards the voice looking for a face, but ori-ented their mouths in the opposite direction.Thus, the experiment demonstrated that themother's voice did not simply trigger suckingbehavior (TER), but it was consistently pre-ceded by orienting toward the voice (INI).

THE "WHERE IS IT?" REFLEXThe theory of how associations in Pavlovian

conditioning are translated into performanceis still inadequately developed (Boakes, 1977).Although it seems obviously adaptive to sali-vate or flex one's leg in anticipation of food ora painful stimulus to the foot, one mightquestion the adaptive significance of the auto-shaped OR in a response-independent labo-ratory situation. Instead of continuing thedebate about the priority of Pavlovian or in-strumental contingencies in signal directed be-havior, it might be more fertile to examinethe phenomenon under investigation from anevolutionary perspective.

Orientation implies directing the sensoriumto improve conditions to perceive and evaluatethe evoking signal. It is contended that theperceptual system is anatomically "wired" tothe motor components of the OR, and possiblyat certain phylogenetic levels the two may beindistinguishable. Orientating movements oflower phyla (taxis) offer such examples. TheOR, I suggest, is elicited by a biologicallyrelevant stimulus. By "relevant" is meant that

476


the animal is capable of reacting to it, ap-proaching it, investigating its important fea-tures, or avoiding it. Implicit in this formu-lation is that both novel and learned stimuliare capable of eliciting an OR, provided theycontain biologically relevant information."Key" stimuli of the ethologists provide numer-ous examples of the former class of stimuli(Eibl-Eibesfeldt, 1951; Ewert, 1976; Kovach,1971; Lorenz, 1969; Ploog, 1970; Tinbergen,1951). The persistence of signal-centered be-havior in learning situations, summarized inthis review, illustrates the conditionability ofthe OR.A primary goal of behavior is to avoid harm-

ful situations and approach beneficial ones(Arnold, 1960; Glickman & Schniff, 1967;Grastyan, Szab6, Molnair, & Kolta, 1968; Mar-tin & Levey, 1978; Troland, 1928; Young,1961). In organisms where appropriate re-sponding to stimuli involves position changes,a prerequisite of reaction is adequate localiza-tion of the stimulus. Translation of the per-ceived information into a spatially orientedmotor reaction requires that the evoking signal(i.e., its source) must have been spatially lo-cated. "Passive" perception of an attractiveconspecific, prey, or a predator in the environ-ment would be of little benefit without thecapability of the organism to localize andreact upon the perceived item. The neuronalsubstrate for stimulus localization has devel-oped very early in evolutionary history, if onejudges it from its location at the subcorticallevel. It is phylogenetically older than thespecific pattern-recognition systems (Ewert,1976; Schneider, 1969). The separability oflocalization and recognition is illustrated bythe finding that following ablation of the su-perior colliculus, the golden hamster is notcapable of localizing patterns in space, al-though it can still distinguish them. In thereverse type of experiment following corticallesions, pattern recognition is eliminated, butlocalization remains intact (Schneider, 1969).

In nature, activity is a prerequisite of anykind of food-procuring. I suggest that thisconcomitantly evolved action system, whichgives meaningfulness to the perceptual system,constitutes the orienting response. The ques-tion "what is it?" (Pavlov, 1927) thus must becomplemented by a simultaneous enquiry:"where is that thing?" Both questions implythat the animal is interpreting its environ-

ment, not by automatic associations but byactively responding.From the above it follows that the function

of the CS is not merely to signal the probabil-ity of US occurrence, but also to serve as a"sign post" in the environment to guide theanimal. The spatial contingency of CS andUS (i.e., their constant spatial relation) makesthe CS a signal for US occurrence. Recognitionof the guiding feature of the CS may finallydiscredit the validity of the distinction be-tween classical and instrumental conditioning.According to Skinner (1935), respondents "re-quire no external point of reference in theirelicitation or description," in contrast to oper-ants which "require points of reference fortheir elicitation" (p. 68). The vast literatureon signal-directed behavior provides evidencethat this differentiation is no longer tenable.

It is therefore not surprising that hungryanimals engage in a variety of activities insituations predicting food (Falk, 1961; Stad-don, 1977; Staddon & Simmelhag, 1971). Con-ditioning trials provide the opportunity forthe subject to discover the predictors of theUS. Any stimulus change or situation that hasalready been correlated with feeding will uponsubsequent occurrence trigger food-searchingmechanisms, provided the animal is hungry.We supposed elsewhere that under the effectof positive reinforcement the predictor (CS)becomes a new goal independent of theprimary reinforcer (BuzsAki et al., 1980;Grastyan & Vereczkei, 1974; see also Rescorla,1980). Within this conceptual frame the CSis no longer viewed as a substitute or surrogateof the US, but as a new goal with a capacitythat goes beyond the specific goal (US) thathad given rise to it. Detection of a significantfeature (CS) in the environment induces stim-ulus-centered responses, and this behavior fur-ther increases the likelihood that previouslyunperceived features of the signal source andits environment will be detected. By approach-ing the CS source various new attributes (e.g.,shadow, echo, smell, size, its distance, its rela-tion to other objects), not experienced from adistal position, will be learned.When all potentially important features of

the predictor (CS) are discovered (i.e., the bio-logically relevant attributes of the signal sourceare learned), the autoshaped OR will be re-stricted to contextually important features ofthe CS. As a consequence, the "amplitude" of

477

478 GYORGY BUZSAKI

the OR may decrease. Since the relevance ofthe predictor never disappears so long as theCS-US relationship remains unchanged, theOR will be sustained, even though overt be-havioral components might no longer be de-tected. The fact that the OR may be rela-tively inaccessible to the observer late inconditioning raises problems of measurementbut does not detract from the potential orga-nizing force of the concept.As discussed above, the present formulation

of the autoshaped response differs from thestimulus or object substitution concepts ofdirected action (Hearst & Jenkins, 1974). Itdoes not depend on speculations aboutwhether the mechanism involved in the re-sponse is classical conditioning, stimulus gen-eralization, or anything else. It was shown thatconditioned signal-directed responses occur inan identical fashion in response-dependentand response-independent paradigms regard-less of the absence of strict Pavlovian con-tingencies. The concept of conditioned OR isat variance also with the conditional releasehypothesis of the autoshaped response (Wood-ruff & Williams, 1976). This hypothesis sug-gests that consummatory fixed-action patternsare released by signals for impending rein-forcing stimuli. In contrast to the rigidity offixed-action patterns (Hinde, 1970) the con-ditioned OR shows a rich variability in itsform determined primarily by the type andlocation of the CS. The learned-release hy-pothesis cannot answer the question of whythe CS, which is claimed to release the fixed-action pattern, becomes the target of that be-havior (Jenkins, Barrera, Ireland, & Wood-side, 1978).

Stimuli predicting danger, pain, or threat tolife will repel the organism from the source ofthese stimuli. Some investigators suggest thatavoidant behavior of this sort is mediated byspecial preprogrammed systems that operateindependently of conventional learning pro-cesses (Bolles, 1970; Burstein, 1977; Garcia &Ervin, 1968). The available evidence suggeststhat, indeed, animals tend to withdraw fromaversive CSs. This negative sign-tracking(Green, 1978; Leclerc & Reberg, 1980; Pedenet al., 1977; Wesp, Lattal, & Poling, 1977;Boakes, Note 1) decreases the likelihood thatthe animal will learn its detailed features.More research is needed, however, to elucidate

the nature of behavior evoked by stimuli pre-dicting aversive USs.

Briefly, I suggest that the cat knows moreabout the mouse than vice versa.

FINAL COMMENTThe purpose of the present review was to

point out that research on the function andcausation of directed action began consider-ably earlier than it is usually dated with thediscovery of autoshaping. Investigations ofthe OR began simultaneously with the dis-covery of the conditioned reflex. Although thetheoretical emphasis in Eastern Europeanliterature has been on the perceptual, infor-mation-processing, and response-directingmechanisms that the OR is claimed to control,most of the Western literature has been con-cerned with the parametric description of afew (almost exclusively vegetative) parametersduring the evocation, habituation, and reevo-cation of the OR (Siddle & Spinks, 1979). Thismight explain why research on autoshapingand the OR has progressed independently andhave had virtually no impact on each other.Since both lines of research have accumulateda considerable amount of valuable data inconnection with learning and conditioning,future research might profit greatly by com-bining the two approaches.

REFERENCE NOTE1. Boakes, R. A. Personal communication, 1978.

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