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Backward conditoning as an inhibitory procedure
LEARNING
AND
MOTIVATION
Backward
2, l-11
( 1971)
Conditoning SHEPARD
as an
SIEGEL’
AND
McMaster
inhibitory
MICHAEL
Procedure1
I~OMJAN
University
Four independent groups of subjects received classical conditioning acquisition following exposure to the CS, the US, both in a noncontingent manner, or both in a backward-paired manner (the US always immediately preceding the CS ). A fifth group received no preconditioning experience with the conditioning stimuli. In both the conditioned suppression situation with rats (Experiment 1) and the eyelid conditioning situation with rabbits (Experiment 2), preconditioning experience with the conditioning stimuli retarded acquisition. This retardation was most pronounced in subjects which had preexposure to the CS and the US in a backward-paired manner, suggesting that the backward contingency produced inhibitory tendencies in excess of those expected simply on the basis of any nonassociative effects of adaptation to the CS and US.
Based on studies by Krestovnikov, Pavlov originally concluded that conditioning could occur only if the onset of the CS preceded the onset of the US: “If this order is reversed, the unconditioned stimulus being applied first and the neutral second, the conditioned reflex cannot be established at all” (Pavlov, 1927, p. 27). Subsequent developments suggested to several investigators, including Pavlov, that a CS used in a backward conditioning situation may actually acquire inhibitory properties (see Konorski, 1948; Pavlov, 1928). On the basis of recent contingency models of classical conditioning, it would be expected that the backward CS would acquire inhibitory properties. That is, backward pairing, like forward pairing, involves an arrangement of contingencies between the conditioning stimuli, but in the backward-paired case the CS is paired with US absence (Rescorla, 1967), and a relatively long period free of the US, the intertrial interval (Moscovitch & LoLordo, lQ68). Retardation of excitatory conditioning has been suggested as a measure of the inhibitory nature of a CS (e.g., Hammond, 1968; Rescorla, 1969a), and it has been reported that both Kreps and Podkopayev, working in ‘This research Research Council ‘Requests for chology, McMaster
was supported by Research Grant APA 0298 from the of Canada. reprints should be sent to Shepard Siegel, Department University, Hamilton, Ontario, Canada. 1
@ 1971
by
Academic
Press,
Inc.
National of
Psy-
2
SIEGEL
AND
DOMJAN
Pavlov’s laboratory, found that backward pairings of the CS and US decreased the effectiveness of that CS when it was subsequently paired with the US in a forward manner (results translated and reported by Razran, 1956). However, as pointed out by Rescorla ( I969b), retardation of acquisition may be due to factors other than the inhibitory nature of the CS. The relevant effect of preconditioning experience with backward-paired presentations of the CS and US may be to habituate S’s orientation or attentional responses to these stimuli, which must be reestablished during subsequent, forward-paired training before conditioning can occur. Indeed, it has been demonstrated in many classical conditioning situations, using a variety of human and infrahuman Ss, that preacquisition exposure to the conditioning stimuli prior to paired CS-US presentations during acquisition can affect the rate of subsequent learning. For example, a number of investigators have demonstrated that presentations of the CS prior to conditioning serve to decrease the effectiveness of that CS when it is subsequently paired with a US during conditioning (for reviews, see Cantor, 1969; Siegel, in press). Similarly, it has also been reported that preconditioning presentations of the US retard acquisition both in the eyelid conditioning (e.g., Taylor, 1956) and in the conditioned suppression situations (Kamin, 1961). With a few exceptions (e.g., Lubow & Siebert, 1969), such findings have frequently been interpreted as resulting from adaptational, attentional, or other nonassociative factors (Kamin, 1961; Rescorla, 1969b). Thus, it is possible that poor acquisition performance following backward exposure to the conditioning stimuli may result from nonassociative effects of such preconditioning presentations, rather than from the acquisition of inhibitory response tendencies. If this were the case, it would be expected that preexposure to both the CS and the US in a noncontingent manner would have a deleterious effect on acquisition that is similar to the effect of preexposure to these stimuh in a backward manner. In the present investigation, the effects of backward conditioning on subsequent excitatory acquisition were compared to the effects of preconditioning experience with the CS, the US, and both conditionin&, stimuli in a noncontingent manner. The effects of such preexposure were studied in conditioned suppression with rats (Experiment 1) and in the eyelid conditioning situation with rabbits (Experiment 2). EXPERIMENT
1
Method Subjects and apparatus. The Ss were 49, c~perillrentali) naive, 90-lOOday-old, male, albino rats, obtained from Hormone Assay Company,
INHIBITION
AND
BACKWARD
CONDITIONING
3
Chicago, Ill. Individual Ss were run in one of four identical Lehigh Valley Skinner boxes (Model 1316), each equipped with two retractable bars. The right bar was retracted throughout the experiment, only the left bar being used. Subjects were housed in individual cages, with water freely available in the cages and Skinner boxes. The CS consisted of a 2-min presentation of a 1400-Hz tone, interrupted 4 times per second, The cue lights in the Skinner box, located over each bar, pulsated on and off in synchrony with the interrupted tone. The US, a LO-mA, 0.5-set electric shock delivered to the grid floor of the Skinner box, was generated by a Lehigh Valley constant current shock generator ( Model 113-04). Design. The investigation consisted of three phases: (1) preliminary bar-press training, (2) preconditioning stimulus exposure, and (3) conditioned suppression training. Subjects differed only in their treatment during the preconditioning stimulus exposure phase of the experiment. Five independent groups of rats received this preexposure to either the CS (Group CS), the US (Group US), both the CS and the US in a backward-paired manner (Group BKD), both the CS and US presented in a random manner (Group RDM), or neither the CS nor the US (Group N). Originally 10 Ss were assigned to each group, but one S in Group BKD died during the course of the investigation. Procedure. All Ss were gradually reduced to the 7540% of ad L&turn weight at which they were maintained throughout the investigation. They were shaped to press the bar for .045-g food pellets, and then received a total of 12 daily sessions of VI training. In a systematic manner, the reinforcement schedule was changed from VI: 30 set to VI: 2 min, and the daily session length was extended from 1 to 2 hr. Subjects were fed after each daily session. Following this preliminary training, Ss received their preconditioning exposure to the conditioning stimuli. This preexposure was delivered during two 6.5-hr sessions conducted on alternate days. For all Ss, the bar and no food pellets were delivered. was retracted during preexposure, Subjects in Group US received the 0.5-set shock US at 15-min intervals, and Ss in Group CS recei\Ted the 2-min CS at 15-min intervals, 25 presentations being made during each preexposure session. Subjects in Group BKD were treated like Ss in Group CS except the US was presented simultaneously with the onset of the CS. Subjects in Group RDM were treated like Ss in Group CS, except the US was presented 25 times during each session; each of the 780 successive 0.5-min segments of each 6.5-hr session had an equal probability of starting with the 0.5-set US. Group N Ss, although they were placed in the chamber, were not presented with either of the conditioning stimuli. ‘The sequence of US presentations to Croup RDM was obtained from a table of
4
SIEGEL
AND
DOMJAN
Following preexposure, Ss received conditioned suppression training during three 2-hr sessions (one session every other day) with the bar again extended into the Skinner box and the VI: 2-min schedule in effect. During each session the 2-min CS, terminating with the 0.9set US, were presented every 30 min. Thus, Ss received four such CS-US pairings during each of the 3 days of conditioned suppression training.
Results During acquisition of conditioned suppression, Ss’ performance on each trial was expressed as a “suppression ratio,” calculated according to the formula A/A + B, where A is the number of bar presses during the 2-min period in which the CS was presented, and B is the number of bar presses during the 2-min period immediately prior to CS onset. Thus, a suppression ratio of 0.50 indicates that the CS has no effect on response rate, and lower ratios indicate increasing amounts of CSelicited response suppression. All reported multigroup comparisons were based on the nonparametric Kruskal-Wallis analysis of variance, and comparisons between two groups were based on the nonparametric Mann-Whitney U test. The 0.05 rejection region was adopted throughout. The mean suppression ratios for each of five groups on each of the 3 days of acquisition are presented in Fig. 1. As indicated in Fig. 1, the groups differed in their rate of acquisition of the conditioned suppression response. This difference between groups was statistically significant [H (4) = 11.83]. Examination of Fig. 1 also shows that the group which had no exposure to either the CS or US prior to acquisition (Group N) acquired the suppression response the fastest. In contrast, almost no acquisition was evidenced over the 3-day training period for the group which received the backward pairing of the conditioning stimuli prior to acquisition (Group BKD). The difference between Groups N and BKD was highly significant ( U = 4.5). The groups which were exposed to either the CS-alone (Group CS), the US-alone (Group US ), or both these stimuli randomly presented (Group random numbers, and the same sequence was used for all Ss. After completion of the experiment, we examined the sequence employed since, with only 50-W presentations, it seemed possible that, without constraints, there might have been a tendency for the unconditioned stimuli to predominantly occur either immediately prior to, during, or subsequent to the CS. This did not appear to be the case. Of the total of 50 preconditioning US presentations administered to Group RDM, a total of 4 occurred sometime during a 2min CS, 5 occurred sometime during the 2 min period immediately prior to a CS, and 4 occurred sometime during the 2 min period immediately subsequent to a CS.
INHIBITION
AND
BACKWARD
5
CONDITIONING
50 -
.40 0 I= 2 g wl kl % 2 z 2 t
FIG. 1. Mean acquisition.
suppression
.30 -
.20 -
.lO -
ratio
for
each
group
on each
of the
three
days
of
RDM) prior to acquisition all acquired the suppression response at approximately the same rate, which was intermediate between Groups N and BKD. Individual comparisons indicated that the differences bctween Groups CS, US, and RDM did not approach statistical significance, but these groups conditioned significantly faster than Group BKD, and significantly slower than Group N. It is possible that the relevant effect of the various preconditioning exposures, at least for those groups which received preconditioning exposure to the unsignalled US, might be to inhibit the base line rate of operant performance, and thus affect acquisition speed via a disinhibiting mechanism (see Brimer & Kamin, 1963) or a “chronic fear” mechanism (see Seligman, 1968). This did not appear to be the case in the present investigation. Analyses of the pre-CS rates during conditioned suppression training indicated that group differences did not approach statistical significance (all p values > .20), based either on overall acquisition performance, or based on the first day of suppression training when it would be expected that group differences would be most pronounced (see Brimer & Kamin, 1963). Discussion The finding that preexposure to the CS has a detrimental effect on acquisition of the conditioned suppression response is an extension of the
6
SIEGEL
AND
DOMJAN
“latent inhibition” phenomenon described by Lubow and Moore ( 1959), and confirms previous findings obtained by others in the conditioned suppression situation (e.g., Anderson, Wolf, & Sullivan, 1969). The finding that preexposure to the US retards acquisition confirms the findings of Kamin ( 1961). Although later work suggested that unsignalled US preexposure inhibits base line performance, thus confounding analyses of the effects of such preexposure on acquisition of the conditioned suppression response (Brimer & Kamin, 1963; Seligman, 1968)) this was not found to be the case in the present investigation. It should be noted that the procedures of the present investigation would be expected to minimize the disrupting effects of the preexposure on base line performance: base line pretraining was very extensive (12 days of VI training), and preconditioning exposures were conducted in a situation in which operant base line responding could not occur. The acquisition performance of Group RDM was approximately the same as that of Groups CS and US. It should be noted, however, that programming exigencies constrained the schedule of US presentation for Group RDM; the US-US interval was always a multiple of 30 sec. Group BKD was most severely retarded in acquisition, with little suppression evidenced even at the end of training. Experiment 2 was designed to assess the reliability of these findings using a different conditioning preparation. In addition, the treatment of Group RDM in Experiment 2 was such that no constraints were placed on the interval between successive US presentations. EXPERIMENT
2
Method Subjects and apparatus. The Ss were 57 experimentally naive, male, New Zealand white rabbits, weighing 2-3 kg. Conditioning was carried out in one of six, identical sound-attenuated chambers, with S placed in a restraining box within the chamber. The outer eyelid response was recorded with a modification of the technique described by Gormezano (1966). Briefly, movement of Ss’ left outer eyelid was conducted, via to the shaft of a microtorque poa string and pulley arrangement, tentiometer. Voltage changes through this potentiometer were graphically recorded and provided a measure of conditioned and unconditioned eyelid activity. The US consisted of a lOO-msec, 200-V, ac shock, delivered through a pair of chronically implanted titanium wire electrodes, mounted approximately 1 cm apart and 1 cm below the left eye. The CS was a 500-msec, 2000-Hz tone at 82 dB above .002 dyne/cm’. Background
INHIBITION
AND
BACKWARD
CONDITIONING
7
white noise was presented throughout the experimental sessions, except for the 500-msec periods of CS presentation, Experimental design and procedure. The design was analogous to that used in Experiment 1, with five independent groups differing only in their exposure to the conditioning stimuli prior to acquisition, being preexposed to 550 presentations of either the CS (Group CS), the US (Group US), both the CS and the US in a backward manner (Group BKD), both the CS and the US in a random manner (Group RDM), or neither (Group N). Twelve Ss were assigned to each of Groups CS and US, and 11 Ss to Groups N, BKD, and RDM. Each S participated in the experiment for 11 daily, 100-min sessions. On Days 1 and ‘3, Ss were systematically adapted to the restraint and eyelid recording apparatus. The Ss in Group N were simply further restrained in the conditioning apparatus without any CS or US presentations on Days 3-7, as well as the first 50 min of the Day 8 session. The other groups were preexposed to the conditioning stimuli during this period. The Ss in Groups CS and US received 100 CS and 100 US presentations, respectively, for Days 3-7, and 50 during the first half of the Day 8 session. The interval between successive presentations of the conditioning stimuli for these groups was either 0.5, 1.0, or 1.5 min (average: 1 min), the different intervals presented in a mixed order. Group BKD was treated like Group CS, except that the lOO-msec US terminated immediately before the onset of the 500-msec CS on 90% of the preexposure trials. Since there is some suggestion of the existence of backward conditioning in the eyelid conditioning situation (e.g., Switzer, 1930), every 19th preexposure trial for Group BKD consisted of a CS-alone test trial to assess the eyelid activity elicited by the CS in the absence of the UR elicited by the immediately preceding ITS. Group RDM was treated like Group CS except that 100 presentations of the US (50 on day 8) were randomly distributed in each session. Each of the 60,000 successive, lOO-msec intervals of each daily 100-min session had an equal probability of containing the lOO-msec US. On Day 8, following the last preexposure presentation (or the 50th min of restraint for Group N), acquisition started for all Ss; the lOO-msec US was presented immediately upon termination of th(! 500-msec CS. Subjects received 50 such acquisition trials on Day 8, and 100 additional acquisition trials on each of Days 9-11. Results As was the case in Experiment 1, all multigroup differences were assessed with the nonparametric Kruskal-Wallis analysis of variance, all
8
SIEGEL
AND
DOMJAN
comparisons between two groups were assessed with the Mann-Whitney U test, and the .05 rejection region was adopted throughout, Preexposure. The groups did not differ in eyelid activity during preexposure, nor did any group show any eyelid activity in excess of the 13% spontaneous blink rate that would be expected from this preparation (e.g., Schneiderman, Fuentes, & Gormezano, 1962; Siegel, in press). Thus, no evidence of “backward conditioning” was obtained in Group BKD. Acquisition. The acquisition performance of all groups, in successive blocks of 25 acquisition trials, is shown in Fig. 2. The difference between groups was statistically significant [H (4) = 39.961. Individual comparisons indicated that Group BKD was most severely retarded in the acquisition of the CR, the difference between Group BKD and each of the other groups being statistically significant. As may be seen in Fig. 2, Groups CS and US did not differ in acquisition performance, but each of them conditioned significantly faster than Groups RDM and BKD, and significantly slower than Group N. Discussion The finding that eyelid CRs did not develop during preexposure for Group BKD is in contrast to some findings suggesting that backward CRs can be obtained (e.g., Switzer, 1930), but is in agreement with the
BLOCKS
for
FIG. 2. Mean each group.
percentage Connected
CRs points
during indicate
OF
25
TRIALS
successive blocks of 25 acquisition blocks within a daily session.
trials
INHIBITION
AND
BACKWARD
CONDITIONING
9
majority of investigations of backward conditioning in the eyelid conditioning situation ( see Kimble, 1961) . Although there is some evidence suggesting that the eyelid (and nictitating membrane) conditioning situation is especially resistant to preexposure effects (e.g., Perlmuter, 1966; Suboski, DiLollo, & Gormeznno, 1964), the present results indicate that such effects can bca demonstrated. The finding that preexposure to the CS retards acquisition confirms previous results obtained in the eyelid conditioning situation with both human ( Schnur & Ksir, 1969) and rabbit (Siegel, lQ69a,b) subjects. The finding that preexposure to the US retards acquisition also confirms previous eyelid conditioning results ( e.g., Taylor, 1956). One finding of this eyelid conditioning investigation which is in contrast with the previous conditioned suppression investigation is the relatively poor acquisition performance of Group RDM compared with the acquisition performance of Groups CS and US. This may be due to any combination of several factors. The important distinction may involve the different random schedules usecl in the two experiments, or the obvious parametric, procedural, and species differences between the two conditioning situations. The finding in the present experiment that Group BKD was most severely retarded in the acquisition of the CR confirms the results of Experiment 1. Indeed, with the exception of the relatively poor performance of Group RDM, the present eyelid conditioning data demonstrates the same ranking of the magnitude of deleterious effects of various preexposure conditions as the previous conditioned suppression data. CONCLUSIONS
In both the conditioned suppression situation with rats (Experiment 1) and the eyelid conditioning situation with rabbits (Experiment 2), it has been demonstrated that preexposure to the CS and/or the US has a deleterious effect on subsequent acquisition. Furthermore, acquisition is retarded to a greater extent when the CS and US are presented in a backward-paired manner during preexposure than when either of these stimuli is presented alone, or when they are both presented in a noncontingent manner. Thus, it would appear that the backward contingency produces inhibitory tendencies which retard subsequent acquisition, and such inhibition is not readily interpretable simply on the basis of non-associative effects of preconditioning experience with the conditioning stimuli. These findings are congruent with recent contingency formulations of classical conditioning (Rescorla, lQ67) in which it is hy-
10
SIEGEL
AND
pothesized that stimuli negatively active inhibitory properties.
DOMJAN
correlated
with
the
US
acquire
REFERENCES ANDERSON, D. C., WOLF, D., & SULLIVAN, P. Pre-conditioning exposures to the CS: Va.riation in place of testing. Psychonomic Science, 1969, 14, 233-235. BRIMER, C. J., & KAMIN, L. J. Disinhibition, habituation, sensitization, and the conditioned emotional response. Journal of Comparative and Physiological Psychology, 1963, 56, 508-516. CANTOR, G. N. Stimulus familiarization effect and the change effect in children’s motor task behavior. Psychological Bulletin, 1969, 71, 144-160. GORMEZANO, I. Classical conditioning. In J. B. Sidowski (Ed.), Experimental methods and instrumentation in psychology. New York: McGraw-Hill, 1966. HAMMOND, L. J. Retardation of fear acquisition by a previously inhibitory CS. Journal of Comparative and Physiological Psychology, 1968, 66, 756-759. KAMIN, L. J. Apparent adaptation effects in the acquisition of a conditioned emotional response. Canadian Journal of Psychology, 1961, 15, 176-188. KIMBLE, G. A. Hilgard and Marquis’ conditioning and learning. New York: AppletonCentury-Crofts, 1961. KONORSKI, J. Conditioned reflexes and neuron organization. Cambridge; Cambridge University Press, 1948. LUBOW, R. E., & MOORE, A. U. Latent inhibition: The effect of nonreinforced preexposure to the conditioned stimulus. Journal of Comparative and Physiological Psychology, 1959, 52, 415-419. LUBOW, R. E., & SIEBERT, L. Latent inhibition within the CER paradigm. Journal of Comparative and Physiological Psychology, 1969, 68, 136-138. MOSCOVITCH, A., & LoLonno, V. M. Role of safety in the Pavlovian backward fear conditioning procedure. Journal of Comparative and Physiological Psychology, 1968, 66, 673-678. PAVLOV, I. P. Conditioned rejZeres. London: Oxford University Press, 1927. PAVLOV, I. P. Lectures on conditioned repexes. New York: International Press, 1928. PERLMUTER, L. C. Effect of CS manipulations on the conditioned eyelid response: Compounding, generalization, the inter-CS-interval and preexposure. Psychonomic Monograph Supplements, 1966, 1, 271-286. RAZRAN, G. Backward conditioning. Psychological Bulletin, 1956, 53, 55-69. RESCORLA, R. A. Pavolvian conditioning and its proper control procedures. Psychological Review, 1967, 74, 71-60. RBSCORLA, R. A. Conditioned inhibition of fear resulting from negative CS-US contingencies. Journal of Comparative and Physiological Psychology, 1969, 67, 504509. (a) RESCORLA, R. A. Pavlovian conditioned inhibition. Psychological B&tin, 1969, 72, 77-94. (b) SCHNEIDERMAN, N., FUENTES, I., & GORMEZANO, I. Acquisition and extinction of the classically conditioned eyelid response in the albino rabbit, Science, 1962, 136, 650-652. SCHNUR, P., & KSIR, C. J. Latent inhibition in human eyelid conditioning. Journal of Experimental Psychology, 1969, 80, 388489. SELIGMAN, M. E. P. Chronic fear produced by unpredictable shock. Journal of Comparative and Physiological Psychology, 1968, 66, 402-W.
INHIBITION
AND
BACKWARD
CONDITIONING
11
SIEGEL, S. Effects of CS habituation on eyelid conditioning. Journal of Comparative and Physiological Psychology, 1969, 68, 245-248. (a) SIEGEL, S. Generalization of latent inhibition. Journal of Comparative and Physiological Psychology, 1969, 69, 157-159. (b) SIEGEL, S. Latent inhibition and eyelid conditioning. In A. H. Black & W. F. Prokasy, (Eds.), Classical conditioning II, New York: Appleton-Century-Crofts, in press. SUBOSKI, M. C., DILOLLO, V., & GORME~ ‘30, I. Effects of unpaired pre-acquisition exposure of CS and UCS on classic conditioning of the nictitating membrane response of the albino rabbit. Psyc,. !l:qical Reports, 1964, 15, 571-576. SWITZER, S. A. Backward conditioning of thr ‘id reflex. Journal of Experimental Psychology, 1930, 13, 76-97. TAYLOR, J. A. Level of conditioning and in, of the adapting stimulus. Journal of Experimental Psychology, 1956, 51, 130. (Received
April
30,
1970)
AND
MOTIVATION
Backward
2, l-11
( 1971)
Conditoning SHEPARD
as an
SIEGEL’
AND
McMaster
inhibitory
MICHAEL
Procedure1
I~OMJAN
University
Four independent groups of subjects received classical conditioning acquisition following exposure to the CS, the US, both in a noncontingent manner, or both in a backward-paired manner (the US always immediately preceding the CS ). A fifth group received no preconditioning experience with the conditioning stimuli. In both the conditioned suppression situation with rats (Experiment 1) and the eyelid conditioning situation with rabbits (Experiment 2), preconditioning experience with the conditioning stimuli retarded acquisition. This retardation was most pronounced in subjects which had preexposure to the CS and the US in a backward-paired manner, suggesting that the backward contingency produced inhibitory tendencies in excess of those expected simply on the basis of any nonassociative effects of adaptation to the CS and US.
Based on studies by Krestovnikov, Pavlov originally concluded that conditioning could occur only if the onset of the CS preceded the onset of the US: “If this order is reversed, the unconditioned stimulus being applied first and the neutral second, the conditioned reflex cannot be established at all” (Pavlov, 1927, p. 27). Subsequent developments suggested to several investigators, including Pavlov, that a CS used in a backward conditioning situation may actually acquire inhibitory properties (see Konorski, 1948; Pavlov, 1928). On the basis of recent contingency models of classical conditioning, it would be expected that the backward CS would acquire inhibitory properties. That is, backward pairing, like forward pairing, involves an arrangement of contingencies between the conditioning stimuli, but in the backward-paired case the CS is paired with US absence (Rescorla, 1967), and a relatively long period free of the US, the intertrial interval (Moscovitch & LoLordo, lQ68). Retardation of excitatory conditioning has been suggested as a measure of the inhibitory nature of a CS (e.g., Hammond, 1968; Rescorla, 1969a), and it has been reported that both Kreps and Podkopayev, working in ‘This research Research Council ‘Requests for chology, McMaster
was supported by Research Grant APA 0298 from the of Canada. reprints should be sent to Shepard Siegel, Department University, Hamilton, Ontario, Canada. 1
@ 1971
by
Academic
Press,
Inc.
National of
Psy-
2
SIEGEL
AND
DOMJAN
Pavlov’s laboratory, found that backward pairings of the CS and US decreased the effectiveness of that CS when it was subsequently paired with the US in a forward manner (results translated and reported by Razran, 1956). However, as pointed out by Rescorla ( I969b), retardation of acquisition may be due to factors other than the inhibitory nature of the CS. The relevant effect of preconditioning experience with backward-paired presentations of the CS and US may be to habituate S’s orientation or attentional responses to these stimuli, which must be reestablished during subsequent, forward-paired training before conditioning can occur. Indeed, it has been demonstrated in many classical conditioning situations, using a variety of human and infrahuman Ss, that preacquisition exposure to the conditioning stimuli prior to paired CS-US presentations during acquisition can affect the rate of subsequent learning. For example, a number of investigators have demonstrated that presentations of the CS prior to conditioning serve to decrease the effectiveness of that CS when it is subsequently paired with a US during conditioning (for reviews, see Cantor, 1969; Siegel, in press). Similarly, it has also been reported that preconditioning presentations of the US retard acquisition both in the eyelid conditioning (e.g., Taylor, 1956) and in the conditioned suppression situations (Kamin, 1961). With a few exceptions (e.g., Lubow & Siebert, 1969), such findings have frequently been interpreted as resulting from adaptational, attentional, or other nonassociative factors (Kamin, 1961; Rescorla, 1969b). Thus, it is possible that poor acquisition performance following backward exposure to the conditioning stimuli may result from nonassociative effects of such preconditioning presentations, rather than from the acquisition of inhibitory response tendencies. If this were the case, it would be expected that preexposure to both the CS and the US in a noncontingent manner would have a deleterious effect on acquisition that is similar to the effect of preexposure to these stimuh in a backward manner. In the present investigation, the effects of backward conditioning on subsequent excitatory acquisition were compared to the effects of preconditioning experience with the CS, the US, and both conditionin&, stimuli in a noncontingent manner. The effects of such preexposure were studied in conditioned suppression with rats (Experiment 1) and in the eyelid conditioning situation with rabbits (Experiment 2). EXPERIMENT
1
Method Subjects and apparatus. The Ss were 49, c~perillrentali) naive, 90-lOOday-old, male, albino rats, obtained from Hormone Assay Company,
INHIBITION
AND
BACKWARD
CONDITIONING
3
Chicago, Ill. Individual Ss were run in one of four identical Lehigh Valley Skinner boxes (Model 1316), each equipped with two retractable bars. The right bar was retracted throughout the experiment, only the left bar being used. Subjects were housed in individual cages, with water freely available in the cages and Skinner boxes. The CS consisted of a 2-min presentation of a 1400-Hz tone, interrupted 4 times per second, The cue lights in the Skinner box, located over each bar, pulsated on and off in synchrony with the interrupted tone. The US, a LO-mA, 0.5-set electric shock delivered to the grid floor of the Skinner box, was generated by a Lehigh Valley constant current shock generator ( Model 113-04). Design. The investigation consisted of three phases: (1) preliminary bar-press training, (2) preconditioning stimulus exposure, and (3) conditioned suppression training. Subjects differed only in their treatment during the preconditioning stimulus exposure phase of the experiment. Five independent groups of rats received this preexposure to either the CS (Group CS), the US (Group US), both the CS and the US in a backward-paired manner (Group BKD), both the CS and US presented in a random manner (Group RDM), or neither the CS nor the US (Group N). Originally 10 Ss were assigned to each group, but one S in Group BKD died during the course of the investigation. Procedure. All Ss were gradually reduced to the 7540% of ad L&turn weight at which they were maintained throughout the investigation. They were shaped to press the bar for .045-g food pellets, and then received a total of 12 daily sessions of VI training. In a systematic manner, the reinforcement schedule was changed from VI: 30 set to VI: 2 min, and the daily session length was extended from 1 to 2 hr. Subjects were fed after each daily session. Following this preliminary training, Ss received their preconditioning exposure to the conditioning stimuli. This preexposure was delivered during two 6.5-hr sessions conducted on alternate days. For all Ss, the bar and no food pellets were delivered. was retracted during preexposure, Subjects in Group US received the 0.5-set shock US at 15-min intervals, and Ss in Group CS recei\Ted the 2-min CS at 15-min intervals, 25 presentations being made during each preexposure session. Subjects in Group BKD were treated like Ss in Group CS except the US was presented simultaneously with the onset of the CS. Subjects in Group RDM were treated like Ss in Group CS, except the US was presented 25 times during each session; each of the 780 successive 0.5-min segments of each 6.5-hr session had an equal probability of starting with the 0.5-set US. Group N Ss, although they were placed in the chamber, were not presented with either of the conditioning stimuli. ‘The sequence of US presentations to Croup RDM was obtained from a table of
4
SIEGEL
AND
DOMJAN
Following preexposure, Ss received conditioned suppression training during three 2-hr sessions (one session every other day) with the bar again extended into the Skinner box and the VI: 2-min schedule in effect. During each session the 2-min CS, terminating with the 0.9set US, were presented every 30 min. Thus, Ss received four such CS-US pairings during each of the 3 days of conditioned suppression training.
Results During acquisition of conditioned suppression, Ss’ performance on each trial was expressed as a “suppression ratio,” calculated according to the formula A/A + B, where A is the number of bar presses during the 2-min period in which the CS was presented, and B is the number of bar presses during the 2-min period immediately prior to CS onset. Thus, a suppression ratio of 0.50 indicates that the CS has no effect on response rate, and lower ratios indicate increasing amounts of CSelicited response suppression. All reported multigroup comparisons were based on the nonparametric Kruskal-Wallis analysis of variance, and comparisons between two groups were based on the nonparametric Mann-Whitney U test. The 0.05 rejection region was adopted throughout. The mean suppression ratios for each of five groups on each of the 3 days of acquisition are presented in Fig. 1. As indicated in Fig. 1, the groups differed in their rate of acquisition of the conditioned suppression response. This difference between groups was statistically significant [H (4) = 11.83]. Examination of Fig. 1 also shows that the group which had no exposure to either the CS or US prior to acquisition (Group N) acquired the suppression response the fastest. In contrast, almost no acquisition was evidenced over the 3-day training period for the group which received the backward pairing of the conditioning stimuli prior to acquisition (Group BKD). The difference between Groups N and BKD was highly significant ( U = 4.5). The groups which were exposed to either the CS-alone (Group CS), the US-alone (Group US ), or both these stimuli randomly presented (Group random numbers, and the same sequence was used for all Ss. After completion of the experiment, we examined the sequence employed since, with only 50-W presentations, it seemed possible that, without constraints, there might have been a tendency for the unconditioned stimuli to predominantly occur either immediately prior to, during, or subsequent to the CS. This did not appear to be the case. Of the total of 50 preconditioning US presentations administered to Group RDM, a total of 4 occurred sometime during a 2min CS, 5 occurred sometime during the 2 min period immediately prior to a CS, and 4 occurred sometime during the 2 min period immediately subsequent to a CS.
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50 -
.40 0 I= 2 g wl kl % 2 z 2 t
FIG. 1. Mean acquisition.
suppression
.30 -
.20 -
.lO -
ratio
for
each
group
on each
of the
three
days
of
RDM) prior to acquisition all acquired the suppression response at approximately the same rate, which was intermediate between Groups N and BKD. Individual comparisons indicated that the differences bctween Groups CS, US, and RDM did not approach statistical significance, but these groups conditioned significantly faster than Group BKD, and significantly slower than Group N. It is possible that the relevant effect of the various preconditioning exposures, at least for those groups which received preconditioning exposure to the unsignalled US, might be to inhibit the base line rate of operant performance, and thus affect acquisition speed via a disinhibiting mechanism (see Brimer & Kamin, 1963) or a “chronic fear” mechanism (see Seligman, 1968). This did not appear to be the case in the present investigation. Analyses of the pre-CS rates during conditioned suppression training indicated that group differences did not approach statistical significance (all p values > .20), based either on overall acquisition performance, or based on the first day of suppression training when it would be expected that group differences would be most pronounced (see Brimer & Kamin, 1963). Discussion The finding that preexposure to the CS has a detrimental effect on acquisition of the conditioned suppression response is an extension of the
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“latent inhibition” phenomenon described by Lubow and Moore ( 1959), and confirms previous findings obtained by others in the conditioned suppression situation (e.g., Anderson, Wolf, & Sullivan, 1969). The finding that preexposure to the US retards acquisition confirms the findings of Kamin ( 1961). Although later work suggested that unsignalled US preexposure inhibits base line performance, thus confounding analyses of the effects of such preexposure on acquisition of the conditioned suppression response (Brimer & Kamin, 1963; Seligman, 1968)) this was not found to be the case in the present investigation. It should be noted that the procedures of the present investigation would be expected to minimize the disrupting effects of the preexposure on base line performance: base line pretraining was very extensive (12 days of VI training), and preconditioning exposures were conducted in a situation in which operant base line responding could not occur. The acquisition performance of Group RDM was approximately the same as that of Groups CS and US. It should be noted, however, that programming exigencies constrained the schedule of US presentation for Group RDM; the US-US interval was always a multiple of 30 sec. Group BKD was most severely retarded in acquisition, with little suppression evidenced even at the end of training. Experiment 2 was designed to assess the reliability of these findings using a different conditioning preparation. In addition, the treatment of Group RDM in Experiment 2 was such that no constraints were placed on the interval between successive US presentations. EXPERIMENT
2
Method Subjects and apparatus. The Ss were 57 experimentally naive, male, New Zealand white rabbits, weighing 2-3 kg. Conditioning was carried out in one of six, identical sound-attenuated chambers, with S placed in a restraining box within the chamber. The outer eyelid response was recorded with a modification of the technique described by Gormezano (1966). Briefly, movement of Ss’ left outer eyelid was conducted, via to the shaft of a microtorque poa string and pulley arrangement, tentiometer. Voltage changes through this potentiometer were graphically recorded and provided a measure of conditioned and unconditioned eyelid activity. The US consisted of a lOO-msec, 200-V, ac shock, delivered through a pair of chronically implanted titanium wire electrodes, mounted approximately 1 cm apart and 1 cm below the left eye. The CS was a 500-msec, 2000-Hz tone at 82 dB above .002 dyne/cm’. Background
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white noise was presented throughout the experimental sessions, except for the 500-msec periods of CS presentation, Experimental design and procedure. The design was analogous to that used in Experiment 1, with five independent groups differing only in their exposure to the conditioning stimuli prior to acquisition, being preexposed to 550 presentations of either the CS (Group CS), the US (Group US), both the CS and the US in a backward manner (Group BKD), both the CS and the US in a random manner (Group RDM), or neither (Group N). Twelve Ss were assigned to each of Groups CS and US, and 11 Ss to Groups N, BKD, and RDM. Each S participated in the experiment for 11 daily, 100-min sessions. On Days 1 and ‘3, Ss were systematically adapted to the restraint and eyelid recording apparatus. The Ss in Group N were simply further restrained in the conditioning apparatus without any CS or US presentations on Days 3-7, as well as the first 50 min of the Day 8 session. The other groups were preexposed to the conditioning stimuli during this period. The Ss in Groups CS and US received 100 CS and 100 US presentations, respectively, for Days 3-7, and 50 during the first half of the Day 8 session. The interval between successive presentations of the conditioning stimuli for these groups was either 0.5, 1.0, or 1.5 min (average: 1 min), the different intervals presented in a mixed order. Group BKD was treated like Group CS, except that the lOO-msec US terminated immediately before the onset of the 500-msec CS on 90% of the preexposure trials. Since there is some suggestion of the existence of backward conditioning in the eyelid conditioning situation (e.g., Switzer, 1930), every 19th preexposure trial for Group BKD consisted of a CS-alone test trial to assess the eyelid activity elicited by the CS in the absence of the UR elicited by the immediately preceding ITS. Group RDM was treated like Group CS except that 100 presentations of the US (50 on day 8) were randomly distributed in each session. Each of the 60,000 successive, lOO-msec intervals of each daily 100-min session had an equal probability of containing the lOO-msec US. On Day 8, following the last preexposure presentation (or the 50th min of restraint for Group N), acquisition started for all Ss; the lOO-msec US was presented immediately upon termination of th(! 500-msec CS. Subjects received 50 such acquisition trials on Day 8, and 100 additional acquisition trials on each of Days 9-11. Results As was the case in Experiment 1, all multigroup differences were assessed with the nonparametric Kruskal-Wallis analysis of variance, all
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comparisons between two groups were assessed with the Mann-Whitney U test, and the .05 rejection region was adopted throughout, Preexposure. The groups did not differ in eyelid activity during preexposure, nor did any group show any eyelid activity in excess of the 13% spontaneous blink rate that would be expected from this preparation (e.g., Schneiderman, Fuentes, & Gormezano, 1962; Siegel, in press). Thus, no evidence of “backward conditioning” was obtained in Group BKD. Acquisition. The acquisition performance of all groups, in successive blocks of 25 acquisition trials, is shown in Fig. 2. The difference between groups was statistically significant [H (4) = 39.961. Individual comparisons indicated that Group BKD was most severely retarded in the acquisition of the CR, the difference between Group BKD and each of the other groups being statistically significant. As may be seen in Fig. 2, Groups CS and US did not differ in acquisition performance, but each of them conditioned significantly faster than Groups RDM and BKD, and significantly slower than Group N. Discussion The finding that eyelid CRs did not develop during preexposure for Group BKD is in contrast to some findings suggesting that backward CRs can be obtained (e.g., Switzer, 1930), but is in agreement with the
BLOCKS
for
FIG. 2. Mean each group.
percentage Connected
CRs points
during indicate
OF
25
TRIALS
successive blocks of 25 acquisition blocks within a daily session.
trials
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majority of investigations of backward conditioning in the eyelid conditioning situation ( see Kimble, 1961) . Although there is some evidence suggesting that the eyelid (and nictitating membrane) conditioning situation is especially resistant to preexposure effects (e.g., Perlmuter, 1966; Suboski, DiLollo, & Gormeznno, 1964), the present results indicate that such effects can bca demonstrated. The finding that preexposure to the CS retards acquisition confirms previous results obtained in the eyelid conditioning situation with both human ( Schnur & Ksir, 1969) and rabbit (Siegel, lQ69a,b) subjects. The finding that preexposure to the US retards acquisition also confirms previous eyelid conditioning results ( e.g., Taylor, 1956). One finding of this eyelid conditioning investigation which is in contrast with the previous conditioned suppression investigation is the relatively poor acquisition performance of Group RDM compared with the acquisition performance of Groups CS and US. This may be due to any combination of several factors. The important distinction may involve the different random schedules usecl in the two experiments, or the obvious parametric, procedural, and species differences between the two conditioning situations. The finding in the present experiment that Group BKD was most severely retarded in the acquisition of the CR confirms the results of Experiment 1. Indeed, with the exception of the relatively poor performance of Group RDM, the present eyelid conditioning data demonstrates the same ranking of the magnitude of deleterious effects of various preexposure conditions as the previous conditioned suppression data. CONCLUSIONS
In both the conditioned suppression situation with rats (Experiment 1) and the eyelid conditioning situation with rabbits (Experiment 2), it has been demonstrated that preexposure to the CS and/or the US has a deleterious effect on subsequent acquisition. Furthermore, acquisition is retarded to a greater extent when the CS and US are presented in a backward-paired manner during preexposure than when either of these stimuli is presented alone, or when they are both presented in a noncontingent manner. Thus, it would appear that the backward contingency produces inhibitory tendencies which retard subsequent acquisition, and such inhibition is not readily interpretable simply on the basis of non-associative effects of preconditioning experience with the conditioning stimuli. These findings are congruent with recent contingency formulations of classical conditioning (Rescorla, lQ67) in which it is hy-
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pothesized that stimuli negatively active inhibitory properties.
DOMJAN
correlated
with
the
US
acquire
REFERENCES ANDERSON, D. C., WOLF, D., & SULLIVAN, P. Pre-conditioning exposures to the CS: Va.riation in place of testing. Psychonomic Science, 1969, 14, 233-235. BRIMER, C. J., & KAMIN, L. J. Disinhibition, habituation, sensitization, and the conditioned emotional response. Journal of Comparative and Physiological Psychology, 1963, 56, 508-516. CANTOR, G. N. Stimulus familiarization effect and the change effect in children’s motor task behavior. Psychological Bulletin, 1969, 71, 144-160. GORMEZANO, I. Classical conditioning. In J. B. Sidowski (Ed.), Experimental methods and instrumentation in psychology. New York: McGraw-Hill, 1966. HAMMOND, L. J. Retardation of fear acquisition by a previously inhibitory CS. Journal of Comparative and Physiological Psychology, 1968, 66, 756-759. KAMIN, L. J. Apparent adaptation effects in the acquisition of a conditioned emotional response. Canadian Journal of Psychology, 1961, 15, 176-188. KIMBLE, G. A. Hilgard and Marquis’ conditioning and learning. New York: AppletonCentury-Crofts, 1961. KONORSKI, J. Conditioned reflexes and neuron organization. Cambridge; Cambridge University Press, 1948. LUBOW, R. E., & MOORE, A. U. Latent inhibition: The effect of nonreinforced preexposure to the conditioned stimulus. Journal of Comparative and Physiological Psychology, 1959, 52, 415-419. LUBOW, R. E., & SIEBERT, L. Latent inhibition within the CER paradigm. Journal of Comparative and Physiological Psychology, 1969, 68, 136-138. MOSCOVITCH, A., & LoLonno, V. M. Role of safety in the Pavlovian backward fear conditioning procedure. Journal of Comparative and Physiological Psychology, 1968, 66, 673-678. PAVLOV, I. P. Conditioned rejZeres. London: Oxford University Press, 1927. PAVLOV, I. P. Lectures on conditioned repexes. New York: International Press, 1928. PERLMUTER, L. C. Effect of CS manipulations on the conditioned eyelid response: Compounding, generalization, the inter-CS-interval and preexposure. Psychonomic Monograph Supplements, 1966, 1, 271-286. RAZRAN, G. Backward conditioning. Psychological Bulletin, 1956, 53, 55-69. RESCORLA, R. A. Pavolvian conditioning and its proper control procedures. Psychological Review, 1967, 74, 71-60. RBSCORLA, R. A. Conditioned inhibition of fear resulting from negative CS-US contingencies. Journal of Comparative and Physiological Psychology, 1969, 67, 504509. (a) RESCORLA, R. A. Pavlovian conditioned inhibition. Psychological B&tin, 1969, 72, 77-94. (b) SCHNEIDERMAN, N., FUENTES, I., & GORMEZANO, I. Acquisition and extinction of the classically conditioned eyelid response in the albino rabbit, Science, 1962, 136, 650-652. SCHNUR, P., & KSIR, C. J. Latent inhibition in human eyelid conditioning. Journal of Experimental Psychology, 1969, 80, 388489. SELIGMAN, M. E. P. Chronic fear produced by unpredictable shock. Journal of Comparative and Physiological Psychology, 1968, 66, 402-W.
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SIEGEL, S. Effects of CS habituation on eyelid conditioning. Journal of Comparative and Physiological Psychology, 1969, 68, 245-248. (a) SIEGEL, S. Generalization of latent inhibition. Journal of Comparative and Physiological Psychology, 1969, 69, 157-159. (b) SIEGEL, S. Latent inhibition and eyelid conditioning. In A. H. Black & W. F. Prokasy, (Eds.), Classical conditioning II, New York: Appleton-Century-Crofts, in press. SUBOSKI, M. C., DILOLLO, V., & GORME~ ‘30, I. Effects of unpaired pre-acquisition exposure of CS and UCS on classic conditioning of the nictitating membrane response of the albino rabbit. Psyc,. !l:qical Reports, 1964, 15, 571-576. SWITZER, S. A. Backward conditioning of thr ‘id reflex. Journal of Experimental Psychology, 1930, 13, 76-97. TAYLOR, J. A. Level of conditioning and in, of the adapting stimulus. Journal of Experimental Psychology, 1956, 51, 130. (Received
April
30,
1970)