- Email: [email protected]
Delayed matching in pigeons: can apparent memory loss be attributed to the delay of reinforcement of sample-orienting behavior?
Behavioural Processes 43 (1998) 1 – 10
Delayed matching in pigeons: can apparent memory loss be attributed to the delay of reinforcement of sample-orienting behavior? Thomas R. Zentall *, Tricia S. Clement, Daren H. Kaiser Department of Psychology, Uni6ersity of Kentucky, Lexington, KY 40506, USA Received 15 March 1997; received in revised form 2 September 1997; accepted 3 September 1997
Abstract In earlier research using constant-delay matching with pigeons, there is evidence that delay of reinforcement of sample-orienting behavior may contribute to the decline in matching accuracy with increasing delay between sample and comparison stimuli. In the present research using this procedure, we found that a significant decline in matching accuracy between the first and second session can occur when delays are relatively long. This effect cannot be accounted for in terms of either additional memory loss or surprise (generalization decrement) associated with the increase in delay. Furthermore, the decline in matching accuracy occurred regardless of whether the delay was inserted between samples and comparisons (where it would be expected to affect the use of sample memory in making the comparison choice response) or between comparisons and reinforcement (where it would not be expected to affect the use of sample memory in making the comparison choice response). Thus, the decrease in matching accuracy between Session 1 and 2 following an increase in delay appears to be unrelated to sample memory at the time of choice. Instead, the results suggest that delay of reinforcement of sample-orienting behavior may play an important role in the negative slope of the retention functions obtained when constant- or mixed-delay matching procedures are used to assess animal memory. © 1998 Elsevier Science B.V. All rights reserved. Keywords: Delayed matching; Memory loss; Reinforcement; Sample-orienting behavior; Pigeons
1. Introduction
* Corresponding author. Tel.: + 1 606 2574076; fax: +1 606 2576839; e-mail: [email protected]
When a delayed matching-to-sample procedure is used to study memory in animals (especially pigeons, e.g. Blough, 1959; Roberts, 1972; Zentall and Hogan, 1977), the subjects are typically
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trained to choose the left or right comparison that matches the previously presented sample. After acquisition to a high level of matching accuracy with no delay, delays are typically inserted between the offset of the sample and the onset of the comparison stimuli. In most experiments, retention functions are established by presenting the animal with sample-comparison delays of mixed duration and determining matching accuracy at each delay (i.e. each session involves both shorterand longer-delay trials, including 0-s-delay trials, as experienced during training). Findings of decreasing matching accuracy with increasing delay are generally interpreted as evidence of memory loss over time. But alternative mechanisms may produce or at least contribute to the decline in matching accuracy with increasing delay. First, Zentall (1997) has suggested that the novelty of delays inserted between samples and comparisons may lead to an ‘instructional failure’. Specifically, prior to delay test, the only empty interval that the pigeons had experienced would have been the intertrial interval. To the extent that pigeons confuse the sample-comparison delay with the intertrial interval, matching accuracy might suffer. Furthermore, the longer the delay, the greater might be the confusion. A second mechanism that could contribute to the decline in matching accuracy with increasing delay, other than true memory loss, is the increase in delay of reinforcement (see, e.g. Grice, 1948) for responding to (or orienting to) the sample stimulus. Delay of reinforcement is typically associated with the terminal response (i.e. in the case of a conditional discrimination with choice of one of the comparison stimuli) but orienting to (and often responding to) the sample stimulus plays an important role in the acquisition of a conditional discrimination (Sacks et al., 1972). In conditioning terms, the sample stimulus can be thought of as a higher-order conditioned stimulus that is associated with the presentation of comparison stimuli (the first order conditioned stimuli). The comparison stimuli are associated directly with the presentation of food. To the extent that the sample is removed in time from the comparison stimuli (and in turn from reinforcement), the sample may lose some of its strength of association
not only with the comparisons, but also with reinforcement. Even when mixed-delay procedures are used and short delay trials are mixed in with the long delay trials, the association of samples with reinforcement may be weakened, relative to what it is without delays. But how can one distinguish the decrease in matching accuracy resulting from increased sample-comparison delay produced by memory loss, either from that produced by the novelty of the delay (or a generalization decrement), or from that produced by delay of reinforcement of sample-orienting behavior? The form or pattern of the decrement in matching accuracy may suggest the mechanisms that underlie this effect. If the decrement in matching accuracy is produced by a loss of memory for the sample, one would expect to see an immediate loss of matching accuracy on the first session involving longer delays, followed perhaps by a gradual improvement in matching accuracy with continued training sessions involving the longer delays. If, however, the decrement in matching accuracy is produced by novelty or a generalization decrement resulting from the change in procedure, although one would expect a similar, immediate loss of matching accuracy, one might also expect to see a relatively rapid return to high levels of matching accuracy with continued training involving the longer delays. Finally, if the decrement in matching accuracy is produced by the increase in delay of reinforcement for sample-orienting behavior, one would expect to see a continued decrease in matching accuracy beyond the first session, as those orienting responses are weakened still further with additional exposure to the longer delays. The best procedure with which to see the possible effects of delay of reinforcement of sample orienting on matching accuracy may be one in which the duration of the delay is predictable, that is, when delays are either blocked or are signaled (i.e. the delay is of a constant duration throughout the session or a stimulus is presented that signals the duration of the delay). Jagielo and Zentall (1986) (Experiment 2) found, for example, that with a mixed-delay procedure (a mixture of 0 s and 8.0 s delay trials), the latency to respond to the sample stimulus (five responses were required
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to initiate the delay) was three times as long on signaled long delay trials as on unsignaled long delay trials. Even more convincing evidence for the effects of delay of reinforcement on sample-orienting behavior can be seen when pigeons are trained on a matching task and delays of fixed duration (within sessions) occur between sample and comparison stimuli. Jagielo and Zentall (1986) (Experiment 1) found that when they gradually increased the delay (starting with 0.5-s delays and doubling the delay for each pigeon as it attained a criterion of 90% correct or higher), at the 8.0-s delay, matching accuracy initially decreased from over 90% correct on the last session of 4.0-s-delay trials to 68.8% correct on the first session of 8.0-s-delay trials and then decreased even further on succeeding sessions. Matching accuracy for one of the four pigeons transferred to the 8.0-s delays dropped to 53% correct, and because that pigeon took over 2 h to complete the first 8.0-s delay session, it was dropped from the study. The remaining three pigeons performed at 59% correct on the second session at 8.0-s delays — a 15% decrease in matching accuracy between the first and second sessions. Another pigeon failed to complete the second session within 2 h (matching accuracy had decreased from 68% correct on Session 1 to 53% correct on Session 2) and it too was dropped from the study. A third pigeon was dropped from the study after five sessions at the 8.0-s delay, for the same reason, and on Session 5 it was performing at 43% correct. The last pigeon continued responding for nine sessions but failed to perform above 59% correct over the last six sessions. The most reasonable explanation for both the decrease in matching accuracy and the increase in time to complete a session is the increase in delay of reinforcement of sample-orienting behavior as the delay increased from 4.0 to 8.0 s. Apparently, the increase in delay of reinforcement was sufficient to interfere with the association between responding to the sample and reinforcement for making the appropriate choice of comparison stimulus. Recently, we have collected data from an experiment that involved a similar manipulation of
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delay, but which was conducted for a quite different purpose. Following 0-s-delay training, delays of a constant duration were inserted between the offset of the sample and the onset of the comparisons (Kaiser et al., 1997). For reasons of importance primarily to that study, various stimuli were presented on the center key during the delays. Furthermore, the delay stimuli were correlated with end of trial events, only some of which were tests of sample memory. The delays began at 1.0 s, and following attainment of a criterion of 90% correct matching for one session, the delays were increased first to 2.0 s and then to 4.0 s. For purposes of the present research, the data of interest are matching accuracy on the first two sessions following the transfer from 2.0-s delays to 4.0-s delays. When the delays were increased from 0 s to 1.0 s, matching accuracy declined from above 90% correct on the last 0-s delay session to 79.0% correct on the first session at the 1.0-s delay and then, as would be expected, matching accuracy rose slightly to 79.5% correct on the second session. Similarly, when the delays were increased from 1.0 s to 2.0 s, matching accuracy declined from over 90% correct on the last session at the 1.0-s delay to 77.8% correct on the first session at the 2.0-s delay and then, again, rose slightly to 78.5% correct on the second session. When the delays were increased from 2.0 s to 4.0 s, however, matching accuracy declined to 82.2% correct on the first session and then continued to decline, significantly, to 76.2% correct on the second session (a decrease of 6.0% correct), F(1,19)= 5.51, p = 0.03. Although there were certain differences in the procedures and results reported by Jagielo and Zentall (1986) and Kaiser et al. (1997), the finding of a substantial decrease in matching accuracy between the first and second session following a doubling of the delay was consistent. This finding would not be expected if the decrement in matching accuracy with increasing delay were attributable to the pigeons’ inability to remember the sample over the longer delay. Certainly, one would not expect memory for the sample to be less proficient following a session of experience with the longer delay. Similarly, the novelty of the longer delays or the generalization decrement (i.e.
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the change in stimulus conditions resulting in a change in probability of response) experienced when longer delays were encountered should have been greatest on the first session. Thus, one would not expect a decrease in matching accuracy on Session 2 attributable to the novelty of the longer delays or to the change in conditions. The most reasonable explanation for the decline in matching accuracy on the second session is the build up in aversiveness associated with acquired anticipation of the increase in delay to reinforcement. On the first session at a longer delay, a shorter delay of reinforcement for sample-orienting behavior would be anticipated. By the end of the first session, however, experience with the longer delay may be sufficient to establish an expectancy of the longer delay of reinforcement. Furthermore, this new longer delay of reinforcement would have been experienced in the context of a recently-expected shorter delay of reinforcement thus, possibly establishing conditions for negative incentive contrast (i.e. an increase in the expected delay of reinforcement). According to this theory, it is hypothesized that the new expectancy of reinforcement delay would add to whatever actual memory loss is associated with the increase in delay, to produce a further decline in matching accuracy. It is not clear why Jagielo and Zentall (1986) and Kaiser et al. (1997) did not find a similar decline in matching accuracy between Session 1 and 2 with an increase in delay from 0 s to 1.0 s, and from 1.0 s to 2.0 s, but perhaps it is because those delays do not represent a sufficiently aversive increase in delay to reinforcement to counter the presumed increase in matching accuracy attributable to the first session of experience with the longer delay. The previous experiments (Jagielo and Zentall, 1986; Kaiser et al., 1997) were not conducted for the purpose of studying the decrease in matching accuracy on the second session of transfer to a longer delay. Nor were they well suited to distinguish directly among different accounts of decreased matching accuracy with increased delay. Thus, the first purpose of the present experiment was to replicate the decline
in matching accuracy between Sessions 1 and 2 found when formerly predictable delays are increased. In the present research, to encourage the pigeons to maintain high levels of matching accuracy at longer delays and continue responding to the samples, (1) 20 responses were required to each sample prior to its offset and the start of the delay, and (2) a single cue (uninformative with regard to the correct comparison) was presented during all delays. The second purpose of the present experiment was to determine if the decrease in matching accuracy between Sessions 1 and 2 at a longer delay was associated with a memory deficit for the sample at the time of comparison choice or was associated more generally with the loss of association between samples and outcomes induced by the increased delay of reinforcement for sample-orienting behavior. To be able to make this distinction, two groups of pigeons were included in the present experiment. For Group sample-delay-comparison, the delays were inserted between the offset of the sample and the onset of the comparisons, and there was no delay between the comparison response and the food (or no food) outcome. For Group samplecomparison-delay, the delays were inserted between the comparison response and the food (or no food) outcomes and there was no delay between the offset of the sample and the onset of comparison stimuli. Thus, for the pigeons in both groups there was a comparable delay between presentation of (and responses to) the sample and reinforcement. If the loss of memory for the sample at the time of comparison choice is responsible for the effect of increasing delay on Session 2 matching accuracy, then one would expect Group sampledelay-comparison to show a larger decrease in matching accuracy on Session 2 than Group sample-comparison-delay (because the latter group would have no delay between sample and comparison stimuli). If, however, the effect is attributable primarily to the increase in delay of reinforcement of sample-orienting behavior, one might expect to find comparable decreases in matching accuracy on Session 2 in both groups.
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2. Method
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sequence of experimental trials and recorded data by way of an interface.
2.1. Subjects 2.3. Procedure The subjects were eight mixed-sex White Carneaux pigeons obtained from the Palmetto Pigeon Plant (Sumter, SC) as retired breeders (5 – 8 years old). The pigeons had all had experience with simultaneous discriminations involving red, yellow, blue, and green hues. The pigeons were housed individually in wire cages with free access to water and grit. They were maintained at 80% of their free- feeding weights throughout the experiment in a temperature controlled colony room, on a 12-h light/dark cycle.
2.2. Apparatus The experiment was conducted in a sound attenuating chamber that measured 37 cm high, 34 cm across the response panel, and 30 cm from the back wall to the response panel. Three rectangular pecking keys were mounted on the response panel. Each key was 3.2 cm wide×2.5 cm high and the keys were separated by 0.5 cm. The bottom edge of the keys was located 16.0 cm from the wire mesh floor of the chamber and behind each key was a 12-stimulus in-line projector (Model 10, Industrial Electronics Engineering, Van Nuys, CA) with 28 V, 0.1 A lamps that projected red (R) and green (G) hues (produced by Kodak Wratten filters Nos. 26 and 60, respectively) onto each of the keys. In addition, a white circle (an annulus with a 16-mm outside diameter and a 13-mm inside diameter) on a black background could be projected onto any of the three response keys. The opening to a rear mounted grain feeder was centered on the response panel, midway between the floor and the response keys. Reinforcement for correct responding consisted of 1.5-s access to Purina Pro Grains for pigeons. A shielded houselight containing a GE 1820 lamp was located 7.6 cm above the center key. The houselight provided general chamber illumination. White noise at 72 dB and an externally mounted exhaust fan provided sound masking. A microcomputer in an adjoining room controlled the
Because the pigeons had previous experience pecking hues on the response keys, they were placed directly on the 0-s delay matching task with red and green samples and comparisons (identity matching). Responding to the sample was followed immediately by illumination of the R and G comparison stimuli, one on the left, the other on the right. A single peck to the matching comparison terminated the comparison stimuli, provided reinforcement, and started the 10-s intertrial interval (ITI). A single peck to the nonmatching comparison terminated the comparison stimuli and started the ITI. All sessions consisted of 96 trials counterbalanced for sample hue and the location of a reinforced response (left or right). A noncorrection procedure was used throughout the experiment. On the first session of training, there was a 5-peck response requirement to the samples presented on the center key; on Session 2, the response requirement was increased to ten pecks, and on Session 3 it was increased to 20 pecks. All pigeons were trained on the 0-s delay matching task to a criterion of 90% correct or better, for two consecutive sessions, on both R and G sample trials. As each pigeon attained the criterion at the 0-s delay, it was assigned to one of the two groups, approximately equated for rate of 0-s delay matching acquisition. Each pigeon was then transferred to trials involving 1.0-s delays, either between the sample and comparison stimuli (Group sample-delay-comparison) or between the comparison stimuli and outcome (Group sample-comparison-delay). During all delays, the white circle was presented on the response key just pecked (i.e. on the center key for pigeons in Group sample-delay-comparison, and on the chosen comparison key for pigeons in Group samplecomparison-delay). After attainment of criterion at the 1.0-s delay, the pigeons were transferred successively to 2.0-, 4.0-, 8.0-, and 16.0-s delays when criterion at the earlier delay was met. If a pigeon did not reach criterion within 30 training
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Table 1 Matching accuracy on the first two sessions of transfer at each delay, for Group sample-delay-comparison and for Group sample-comparison-delay Group
Delay (s) 1.0
2.0
4.0
8.0
16.0
S1
S2
S1
S2
S1
S2
S1
S2
S1
S2
SDC SCD
76.5 92.8
89.8 91.0
90.5 93.5
90.8 93.0
82.0 91.2
88.5 94.0
76.8 90.0
77.2 87.0
67.7 93.7
63.3 82.0
Mean
84.6
90.4
92.0
91.9
86.6
91.2
83.4
82.1
80.7
72.6
SDC, Group sample-delay-comparison; SCD, Group sample-comparison-delay; S1, Session 1; S2, Session 2.
sessions at a particular delay, it was dropped from the experiment at that point. All pigeons that attained criterion at 8.0-s delays were tested for 10 sessions at the 16.0-s delay. In all analyses, the.05 level of statistical significance was adopted.
3. Results The groups did not differ significantly in the rate at which they acquired the original matching task with 0-s delays, F(1,6) =4.25, or the rate at which they acquired delayed matching at any of the transfer delays (1.0, 2.0, 4.0, and 8.0 s), F B 1, F(1,6) =3.43, F B 1, and F B1, respectively. Two pigeons, one in each group, failed to attain criterion at the 8.0-s delay within 30 sessions and thus, were not transferred to the 16.0-s delay. It is possible that the delay of reinforcement following comparison choice contributed to the failure to attain criterion at the 8.0-s delay. For Group sample-comparison-delay, not only might the association between comparison responding and reinforcement be weakened as the delay increases but the increasing delay may result in the inability to predict when reinforcement will occur and, thus, may lead to missed reinforcers. Such an account is unlikely, however, because only one of these pigeons came from Group sample-comparison-delay. Furthermore, the absence of reinforcement typically results in the failure to initiate a trial (i.e. a failure to respond to the sample) rather than a failure to attain criterion, and neither pigeon showed any evidence of ‘stalling’. For
purposes of the 8.0-s analysis, these two pigeons were given scores of 31 sessions. The acquisition data for pigeons in both groups are presented in Table 1. Mixed two-way analyses were performed on the transfer data at each delay with Group (samplecomparison-delay versus sample-delay-comparison) and Session (1 versus 2) as factors. Overall, the level of matching accuracy on the first two sessions of transfer for Group sample-comparison-delay was significantly higher than for Group sample-delay-comparison at the 1.0- and 8.0-s delays, F(1,6)= 6.38, and 9.50, respectively, but not at the 2.0- and 4.0-s delays, FB 1 and F(1,6)= 1.89, respectively. There was also a significant increase, overall, in matching accuracy between Session 1 and Session 2 at the 1.0-s delay, F(1,6)= 8.56, but not at the 2.0-, 4.0-, or 8.0-s delays, FB 1, F(1,6)= 3.81, FB 1, respectively. In addition, Group sample-delay-comparison showed a significantly larger improvement in matching accuracy between Sessions 1 and 2 at the 1.0-s delay, than did Group sample-comparison-delay, F(1,6)= 14.56, but not at the 2.0-, 4.0-, or 8.0-s delays, all FsB 1. The significant interaction at the 1.0-s delay can be attributed to the relatively large initial decrease in matching accuracy for Group sample-delay-comparison, produced, perhaps, by disruption of the timing of comparison choice when delays were first introduced. This conclusion is suggested by the rather rapid recovery from this initial disruption of matching accuracy by Group sample-delay-comparison. However, Group sample-comparison-de-
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lay showed no decrease in matching accuracy on the first transfer session involving 1.0-s delays thus, little improvement was possible on Session 2. As noted earlier, two of the pigeons, one in each group, failed to attain criterion at the 8.0-s delay. Thus, only three pigeons in each group were tested at the 16.0-s delay. At the 16.0-s delay, matching accuracy for Group sample-comparison-delay was significantly higher than for Group sample-delay-comparison, F(1,4) = 25.76. In addition, overall, there was a significant decrease in matching accuracy between Session 1 and Session 2, F(1, 4)= 13.32. The Group× Sessions interaction was not significant, F(1,4) = 2.80. The level of matching accuracy on the first two sessions of transfer at each delay, for each group, appears in Table 2. To better isolate the regular change in matching accuracy between Session 1 and Session 2 as a function of increasing delay, a linear trend analysis was performed on the combined data from all delays (using only data from those pigeons that had experienced all of the delays). The linear trend analysis indicated that there was a significant systematic change in the difference between matching accuracy on Sessions 1 and 2, over Table 2 Sessions to criterion at each delay, for pigeons in Group sample-delay-comparison and for Group sample-comparisondelay Group
Pigeon
Delay (s) 0.0
1.0
2.0
4.0
8.0
16.0
SDC
8837 9872 4378 3507 Mean
6 12 6 11 8.8
4 3 3 4 3.5
2 3 4 4 3.2
13 4 2 3 5.5
6 * 9 7 *
* * * * *
SCD
9888 10 060 9972 4179 Mean
14 10 13 13 12.5
4 2 4 2 3.0
2 2 3 2 2.2
13 3 6 2 6.0
6 * 8 2 *
* * 6 * *
SDC, Group sample-delay-comparison; SCD, Group samplecomparison-delay. * Indicates criterion was not attained.
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Fig. 1. Improvement in matching accuracy from Session 1 to Session 2 (S2 – S1) at each delay for Groups sample-comparison-delay and sample-delay-comparison combined.
delays, independent of group, F(1,16)= 15.08. A graphical presentation of delayed-matching accuracy on Session 2 minus that on Session 1 is presented in Fig. 1. Although a session of experience appears to have resulted in an improvement in matching accuracy at the 1-s delay, there was no such improvement at the 2-, 4-, and 8-s delays, and there was a significant decrease in matching accuracy for pigeons that were transferred to the 16-s delay.
4. Discussion Data from the present experiment (as well as those from two earlier studies) indicate that with sufficiently long delays, accuracy of delayed matching with a fixed (predictable) delay will decrease from the first transfer session (at a longer delay) to the second transfer session. Furthermore, the results of the present experiment suggest that the Session 2 decrement in matching accuracy is probably attributable to the delay of reinforcement between the sample and outcome. Although overall matching accuracy was higher when the delays were inserted between presentation of the comparison stimuli and reinforcement than when they were inserted between presentation of the sample and presentation of the com-
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parisons, comparable decrements in matching accuracy (between Sessions 1 and 2) were found for both groups. Apparently, the increased delay of reinforcement for sample-orienting behavior weakens the association between that behavior and the outcome. The weakened association may interfere with matching accuracy by decreasing attention to or responding to the sample. Alternatively, experiencing an increase in delay between sample behavior and reinforcement may induce an emotional response (e.g. frustration) in the pigeon, which in turn may disrupt matching accuracy. This interpretation of the present data is consistent with findings by McCarthy and Davison (1986) that matching accuracy declines not only when delays are inserted between samples and comparisons but also when delays are inserted between samples and outcomes. Furthermore, consistent with McCarthy and Davison’s results, the sample-comparison delay was more detrimental to matching accuracy than the comparisonoutcome delay. This difference in the slope of the retention function may reflect the actual loss in memory, independent of delay of reinforcement. On the other hand, the fact that comparable effects were found in both groups suggests that the decrease in matching accuracy on Session 2 is attributable neither to a deficit in working memory for the sample (there was negligible memory load for Group sample-comparison-delay), nor to the lack of familiarity with the novel delays. A disruption in matching accuracy attributable to memory loss or to the novelty of the longer delays (generalization decrement) would be expected to appear on the first transfer session and perhaps to actually diminish somewhat by the second session. Instead, the Session 2 decrement in matching accuracy depends on the anticipation of the longer delay which appears to take about a session to develop. This notion of delay anticipation is consistent with the finding that matching accuracy at a particular delay depends on the delay context in which memory is assessed (Hartl et al., 1996; Honig, 1987; Zentall et al., 1978). This research indicates that, independent of the actual delay on a particular trial, matching accuracy is at a higher
level when the mean (i.e. the expected) delay is shorter than when it is longer. The fact that the Session 2 decrement in matching accuracy appeared at different delays in the three experiments reported may have been produced by differences in procedure. The decline in matching accuracy on Session 2 found by Kaiser et al. (1997) appeared earlier (i.e. at 4.0-s delays) than in both the present study or in Jagielo and Zentall (1986). In Kaiser et al. (1997), however, only a small proportion of the trials in each session were delayed matching trials. In the Jagielo and Zentall experiment, all the trials were delayed matching trials (i.e. they were tests of sample memory) and the decrease in matching accuracy on Session 2 appeared when the 8.0-s delays were introduced. However, unlike in the present experiment, all of the pigeons exposed to those 8.0-s delays in the Jagielo and Zentall study showed a profound increase in latency to peck the samples. The reason for this increase in sample-response latency appears to have been the absence of a stimulus (during the delay) that could help the pigeons mediate the delay. Presentation of a stimulus on the response key during the delay may provide the pigeons with a convenient place to peck during the delays and may also make the delays more distinctive from the intertrial interval. Furthermore, in the present experiment, the sample peck requirement was 20 pecks (considerably more than the 5-peck requirement in Jagielo and Zentall (1986)). The result of these changes in the procedures used in the present experiment appears to have been that the Session 2 decrement in matching accuracy occurred later in the present experiment (i.e. at 16.0-s delays) than in earlier research and the latency to respond to the samples was not problematic, even at those long delays. Apparently, the delay at which the effect occurs depends on the training conditions, including perhaps whether or not there is a stimulus presented during the delay, the number of responses required to the sample, and the proportion of matching-to-sample trials in a session. The Session 2 decrement in matching performance is more than a curious anomaly. Effects of delay of reinforcement of sample-orienting behavior have not generally been considered as a con-
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tributor to decrements in delayed matching accuracy. However, even in experiments in which mixed delays have been used, there is evidence that nonmemorial performance deficits contribute to the delay gradients typically found. Generally, pigeons are trained on a 0-s-delayedmatching task prior to the introduction of mixed delays. Furthermore, in many experiments, some trials with 0-s delays are included among the longer delays. When one compares matching accuracy at the end of 0-s-delay training (typically pigeons are trained to a criterion of 90% correct or higher matching accuracy for one or more sessions) with that on 0-s-delay trials during the memory test with mixed delays, it is not unusual to find a decrement in matching accuracy that cannot be attributed to memory loss or to generalization decrement. For example, when we examined data collected by Sherburne and Zentall (1995), we found that the pigeons performed at 93.4% correct on the last two sessions of training and that they showed a significant decrease in matching accuracy to 81.6% correct on 0-s-delay trials (trials identical to those experienced during training), over the first ten sessions of mixed-delay testing, F(1,6)= 156.84. Similarly, when we examined data collected by Zentall et al. (1995), we found that matching accuracy was at 90.5% correct at the end of 0-s-delay training, whereas it had decreased, significantly, to 81.0% correct on 0-s-delay trials during mixed delay tests (pooled over the test sessions), F(1,11) =32.04. Thus, an effect similar to that reported in the present study can be found under conditions in which the delay is unpredictable, but in which, on average, a longer delay of reinforcement of sample-orienting behavior can be expected than that experienced during training. The decrements in matching accuracy found on Session 2 of transfer to longer delays (Jagielo and Zentall, 1986, Experiment 1; Kaiser et al., 1997; and the present study), together with the parallel findings from experiments in which mixed-delay training is provided, suggest that the anticipation of delay of reinforcement of sample-orienting behavior plays an important role in decrements in matching accuracy that result from the introduction of delays between samples and comparisons when the delayed matching procedure is used.
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When using a mixed-delay condition, one might expect that this delay-of-reinforcement variable would have a relatively constant effect on matching accuracy, over trials, within a given mixed-delay condition, because it should depend on the anticipated delay of reinforcement. If so, it would be expected to affect matching accuracy similarly at all delays and the slope of the retention function would still be a reasonable measure of memory loss. It is also possible, however, that even with a mixed-delay procedure, there are differential effects on matching accuracy at different delays. For example, at the longest delays in a mixed-delay procedure, when the delay of reinforcement would be longer than average (i.e. longer than that expected), matching accuracy may be additionally disrupted. In any case, future research in animal memory (especially that involving delayed matching) should acknowledge the possible contribution of the effect of delay of reinforcement of sample-orienting behavior to the purported decline in memory over time as evidence by a decrease in matching accuracy with increasing sample-comparison delay. Acknowledgements This research was supported by National Science Foundation Grants BNS-8418275 and BNS9019080 and National Institute of Mental Health Grant 45979 to Thomas R. Zentall. References Blough, D.S., 1959. Delayed matching in the pigeon. J. Exp. Anal. Behav. 2, 151 – 160. Grice, G.R., 1948. The relation of secondary reinforcement to delayed reward in visual discrimination learning. J. Exp. Psychol. 38, 1 – 16. Hartl, J.A., Dougherty, D.H., Wixted, J.T., 1996. Separating the effects of trial-specific and average sample-stimulus duration in delayed matching to sample in pigeons. J. Exp. Anal. Behav. 66, 231 – 242. Honig, W.K., 1987. Memory interval distribution effects in pigeons. Anim. Learn. Behav. 15, 6 – 14. Jagielo, J.A., Zentall, T.R., 1986. Predictable long-delay matching-to-sample trials result in long-latency sample responding by pigeons. Learn. Motiv. 17, 269 – 286.
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Kaiser, D.H., Sherburne, L.M., Zentall, T.R., 1997. Directed forgetting in pigeons resulting from the reallocation of memory-maintaining processes on forget-cue trials. Psychonom. Bull. Rev. (in press). McCarthy, D., Davison, M., 1986. Delayed reinforcement and delayed choice in symbolic matching to sample: Effects on stimulus discriminability. J. Exp. Anal. Behav. 46, 293– 301. Roberts, W.S., 1972. Short-term memory in the pigeon: Effects of repetition and spacing. J. Exp. Psychol. Anim. Behav. Process. 6, 217 – 237. Sacks, R.A., Kamil, A.C., Mack, R., 1972. The effects of fixed-ratio sample requirements on matching-to-sample in the pigeon. Psychonom. Sci. 26, 291–293.
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Sherburne, L.M., Zentall, T.R., 1995. Delayed matching in pigeons with food and no-food samples: Further examination of backward associations. Anim. Learn. Behav. 23, 177 – 181. Zentall, T.R., 1997. Animal memory: the role of ‘instructions’. Learn. Motiv. 28, 280 – 308. Zentall, T.R., Hogan, D.E., 1977. Short-term proactive inhibition in the pigeon. Learn. Motiv. 8, 367 – 386. Zentall, T.R., Hogan, D.E., Howard, M.M., Moore, B.S., 1978. Delayed matching in the pigeon: Effect on performance of sample-specific observing responses and differential delay behavior. Learn. Motiv. 9, 202 – 218. Zentall, T.R., Sherburne, L.M., Urcuioli, P.J., 1995. Coding of hedonic and nonhedonic samples by pigeons in many-toone delayed matching. Anim. Learn. Behav. 23, 189 – 196.
Delayed matching in pigeons: can apparent memory loss be attributed to the delay of reinforcement of sample-orienting behavior? Thomas R. Zentall *, Tricia S. Clement, Daren H. Kaiser Department of Psychology, Uni6ersity of Kentucky, Lexington, KY 40506, USA Received 15 March 1997; received in revised form 2 September 1997; accepted 3 September 1997
Abstract In earlier research using constant-delay matching with pigeons, there is evidence that delay of reinforcement of sample-orienting behavior may contribute to the decline in matching accuracy with increasing delay between sample and comparison stimuli. In the present research using this procedure, we found that a significant decline in matching accuracy between the first and second session can occur when delays are relatively long. This effect cannot be accounted for in terms of either additional memory loss or surprise (generalization decrement) associated with the increase in delay. Furthermore, the decline in matching accuracy occurred regardless of whether the delay was inserted between samples and comparisons (where it would be expected to affect the use of sample memory in making the comparison choice response) or between comparisons and reinforcement (where it would not be expected to affect the use of sample memory in making the comparison choice response). Thus, the decrease in matching accuracy between Session 1 and 2 following an increase in delay appears to be unrelated to sample memory at the time of choice. Instead, the results suggest that delay of reinforcement of sample-orienting behavior may play an important role in the negative slope of the retention functions obtained when constant- or mixed-delay matching procedures are used to assess animal memory. © 1998 Elsevier Science B.V. All rights reserved. Keywords: Delayed matching; Memory loss; Reinforcement; Sample-orienting behavior; Pigeons
1. Introduction
* Corresponding author. Tel.: + 1 606 2574076; fax: +1 606 2576839; e-mail: [email protected]
When a delayed matching-to-sample procedure is used to study memory in animals (especially pigeons, e.g. Blough, 1959; Roberts, 1972; Zentall and Hogan, 1977), the subjects are typically
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trained to choose the left or right comparison that matches the previously presented sample. After acquisition to a high level of matching accuracy with no delay, delays are typically inserted between the offset of the sample and the onset of the comparison stimuli. In most experiments, retention functions are established by presenting the animal with sample-comparison delays of mixed duration and determining matching accuracy at each delay (i.e. each session involves both shorterand longer-delay trials, including 0-s-delay trials, as experienced during training). Findings of decreasing matching accuracy with increasing delay are generally interpreted as evidence of memory loss over time. But alternative mechanisms may produce or at least contribute to the decline in matching accuracy with increasing delay. First, Zentall (1997) has suggested that the novelty of delays inserted between samples and comparisons may lead to an ‘instructional failure’. Specifically, prior to delay test, the only empty interval that the pigeons had experienced would have been the intertrial interval. To the extent that pigeons confuse the sample-comparison delay with the intertrial interval, matching accuracy might suffer. Furthermore, the longer the delay, the greater might be the confusion. A second mechanism that could contribute to the decline in matching accuracy with increasing delay, other than true memory loss, is the increase in delay of reinforcement (see, e.g. Grice, 1948) for responding to (or orienting to) the sample stimulus. Delay of reinforcement is typically associated with the terminal response (i.e. in the case of a conditional discrimination with choice of one of the comparison stimuli) but orienting to (and often responding to) the sample stimulus plays an important role in the acquisition of a conditional discrimination (Sacks et al., 1972). In conditioning terms, the sample stimulus can be thought of as a higher-order conditioned stimulus that is associated with the presentation of comparison stimuli (the first order conditioned stimuli). The comparison stimuli are associated directly with the presentation of food. To the extent that the sample is removed in time from the comparison stimuli (and in turn from reinforcement), the sample may lose some of its strength of association
not only with the comparisons, but also with reinforcement. Even when mixed-delay procedures are used and short delay trials are mixed in with the long delay trials, the association of samples with reinforcement may be weakened, relative to what it is without delays. But how can one distinguish the decrease in matching accuracy resulting from increased sample-comparison delay produced by memory loss, either from that produced by the novelty of the delay (or a generalization decrement), or from that produced by delay of reinforcement of sample-orienting behavior? The form or pattern of the decrement in matching accuracy may suggest the mechanisms that underlie this effect. If the decrement in matching accuracy is produced by a loss of memory for the sample, one would expect to see an immediate loss of matching accuracy on the first session involving longer delays, followed perhaps by a gradual improvement in matching accuracy with continued training sessions involving the longer delays. If, however, the decrement in matching accuracy is produced by novelty or a generalization decrement resulting from the change in procedure, although one would expect a similar, immediate loss of matching accuracy, one might also expect to see a relatively rapid return to high levels of matching accuracy with continued training involving the longer delays. Finally, if the decrement in matching accuracy is produced by the increase in delay of reinforcement for sample-orienting behavior, one would expect to see a continued decrease in matching accuracy beyond the first session, as those orienting responses are weakened still further with additional exposure to the longer delays. The best procedure with which to see the possible effects of delay of reinforcement of sample orienting on matching accuracy may be one in which the duration of the delay is predictable, that is, when delays are either blocked or are signaled (i.e. the delay is of a constant duration throughout the session or a stimulus is presented that signals the duration of the delay). Jagielo and Zentall (1986) (Experiment 2) found, for example, that with a mixed-delay procedure (a mixture of 0 s and 8.0 s delay trials), the latency to respond to the sample stimulus (five responses were required
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to initiate the delay) was three times as long on signaled long delay trials as on unsignaled long delay trials. Even more convincing evidence for the effects of delay of reinforcement on sample-orienting behavior can be seen when pigeons are trained on a matching task and delays of fixed duration (within sessions) occur between sample and comparison stimuli. Jagielo and Zentall (1986) (Experiment 1) found that when they gradually increased the delay (starting with 0.5-s delays and doubling the delay for each pigeon as it attained a criterion of 90% correct or higher), at the 8.0-s delay, matching accuracy initially decreased from over 90% correct on the last session of 4.0-s-delay trials to 68.8% correct on the first session of 8.0-s-delay trials and then decreased even further on succeeding sessions. Matching accuracy for one of the four pigeons transferred to the 8.0-s delays dropped to 53% correct, and because that pigeon took over 2 h to complete the first 8.0-s delay session, it was dropped from the study. The remaining three pigeons performed at 59% correct on the second session at 8.0-s delays — a 15% decrease in matching accuracy between the first and second sessions. Another pigeon failed to complete the second session within 2 h (matching accuracy had decreased from 68% correct on Session 1 to 53% correct on Session 2) and it too was dropped from the study. A third pigeon was dropped from the study after five sessions at the 8.0-s delay, for the same reason, and on Session 5 it was performing at 43% correct. The last pigeon continued responding for nine sessions but failed to perform above 59% correct over the last six sessions. The most reasonable explanation for both the decrease in matching accuracy and the increase in time to complete a session is the increase in delay of reinforcement of sample-orienting behavior as the delay increased from 4.0 to 8.0 s. Apparently, the increase in delay of reinforcement was sufficient to interfere with the association between responding to the sample and reinforcement for making the appropriate choice of comparison stimulus. Recently, we have collected data from an experiment that involved a similar manipulation of
3
delay, but which was conducted for a quite different purpose. Following 0-s-delay training, delays of a constant duration were inserted between the offset of the sample and the onset of the comparisons (Kaiser et al., 1997). For reasons of importance primarily to that study, various stimuli were presented on the center key during the delays. Furthermore, the delay stimuli were correlated with end of trial events, only some of which were tests of sample memory. The delays began at 1.0 s, and following attainment of a criterion of 90% correct matching for one session, the delays were increased first to 2.0 s and then to 4.0 s. For purposes of the present research, the data of interest are matching accuracy on the first two sessions following the transfer from 2.0-s delays to 4.0-s delays. When the delays were increased from 0 s to 1.0 s, matching accuracy declined from above 90% correct on the last 0-s delay session to 79.0% correct on the first session at the 1.0-s delay and then, as would be expected, matching accuracy rose slightly to 79.5% correct on the second session. Similarly, when the delays were increased from 1.0 s to 2.0 s, matching accuracy declined from over 90% correct on the last session at the 1.0-s delay to 77.8% correct on the first session at the 2.0-s delay and then, again, rose slightly to 78.5% correct on the second session. When the delays were increased from 2.0 s to 4.0 s, however, matching accuracy declined to 82.2% correct on the first session and then continued to decline, significantly, to 76.2% correct on the second session (a decrease of 6.0% correct), F(1,19)= 5.51, p = 0.03. Although there were certain differences in the procedures and results reported by Jagielo and Zentall (1986) and Kaiser et al. (1997), the finding of a substantial decrease in matching accuracy between the first and second session following a doubling of the delay was consistent. This finding would not be expected if the decrement in matching accuracy with increasing delay were attributable to the pigeons’ inability to remember the sample over the longer delay. Certainly, one would not expect memory for the sample to be less proficient following a session of experience with the longer delay. Similarly, the novelty of the longer delays or the generalization decrement (i.e.
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the change in stimulus conditions resulting in a change in probability of response) experienced when longer delays were encountered should have been greatest on the first session. Thus, one would not expect a decrease in matching accuracy on Session 2 attributable to the novelty of the longer delays or to the change in conditions. The most reasonable explanation for the decline in matching accuracy on the second session is the build up in aversiveness associated with acquired anticipation of the increase in delay to reinforcement. On the first session at a longer delay, a shorter delay of reinforcement for sample-orienting behavior would be anticipated. By the end of the first session, however, experience with the longer delay may be sufficient to establish an expectancy of the longer delay of reinforcement. Furthermore, this new longer delay of reinforcement would have been experienced in the context of a recently-expected shorter delay of reinforcement thus, possibly establishing conditions for negative incentive contrast (i.e. an increase in the expected delay of reinforcement). According to this theory, it is hypothesized that the new expectancy of reinforcement delay would add to whatever actual memory loss is associated with the increase in delay, to produce a further decline in matching accuracy. It is not clear why Jagielo and Zentall (1986) and Kaiser et al. (1997) did not find a similar decline in matching accuracy between Session 1 and 2 with an increase in delay from 0 s to 1.0 s, and from 1.0 s to 2.0 s, but perhaps it is because those delays do not represent a sufficiently aversive increase in delay to reinforcement to counter the presumed increase in matching accuracy attributable to the first session of experience with the longer delay. The previous experiments (Jagielo and Zentall, 1986; Kaiser et al., 1997) were not conducted for the purpose of studying the decrease in matching accuracy on the second session of transfer to a longer delay. Nor were they well suited to distinguish directly among different accounts of decreased matching accuracy with increased delay. Thus, the first purpose of the present experiment was to replicate the decline
in matching accuracy between Sessions 1 and 2 found when formerly predictable delays are increased. In the present research, to encourage the pigeons to maintain high levels of matching accuracy at longer delays and continue responding to the samples, (1) 20 responses were required to each sample prior to its offset and the start of the delay, and (2) a single cue (uninformative with regard to the correct comparison) was presented during all delays. The second purpose of the present experiment was to determine if the decrease in matching accuracy between Sessions 1 and 2 at a longer delay was associated with a memory deficit for the sample at the time of comparison choice or was associated more generally with the loss of association between samples and outcomes induced by the increased delay of reinforcement for sample-orienting behavior. To be able to make this distinction, two groups of pigeons were included in the present experiment. For Group sample-delay-comparison, the delays were inserted between the offset of the sample and the onset of the comparisons, and there was no delay between the comparison response and the food (or no food) outcome. For Group samplecomparison-delay, the delays were inserted between the comparison response and the food (or no food) outcomes and there was no delay between the offset of the sample and the onset of comparison stimuli. Thus, for the pigeons in both groups there was a comparable delay between presentation of (and responses to) the sample and reinforcement. If the loss of memory for the sample at the time of comparison choice is responsible for the effect of increasing delay on Session 2 matching accuracy, then one would expect Group sampledelay-comparison to show a larger decrease in matching accuracy on Session 2 than Group sample-comparison-delay (because the latter group would have no delay between sample and comparison stimuli). If, however, the effect is attributable primarily to the increase in delay of reinforcement of sample-orienting behavior, one might expect to find comparable decreases in matching accuracy on Session 2 in both groups.
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2. Method
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sequence of experimental trials and recorded data by way of an interface.
2.1. Subjects 2.3. Procedure The subjects were eight mixed-sex White Carneaux pigeons obtained from the Palmetto Pigeon Plant (Sumter, SC) as retired breeders (5 – 8 years old). The pigeons had all had experience with simultaneous discriminations involving red, yellow, blue, and green hues. The pigeons were housed individually in wire cages with free access to water and grit. They were maintained at 80% of their free- feeding weights throughout the experiment in a temperature controlled colony room, on a 12-h light/dark cycle.
2.2. Apparatus The experiment was conducted in a sound attenuating chamber that measured 37 cm high, 34 cm across the response panel, and 30 cm from the back wall to the response panel. Three rectangular pecking keys were mounted on the response panel. Each key was 3.2 cm wide×2.5 cm high and the keys were separated by 0.5 cm. The bottom edge of the keys was located 16.0 cm from the wire mesh floor of the chamber and behind each key was a 12-stimulus in-line projector (Model 10, Industrial Electronics Engineering, Van Nuys, CA) with 28 V, 0.1 A lamps that projected red (R) and green (G) hues (produced by Kodak Wratten filters Nos. 26 and 60, respectively) onto each of the keys. In addition, a white circle (an annulus with a 16-mm outside diameter and a 13-mm inside diameter) on a black background could be projected onto any of the three response keys. The opening to a rear mounted grain feeder was centered on the response panel, midway between the floor and the response keys. Reinforcement for correct responding consisted of 1.5-s access to Purina Pro Grains for pigeons. A shielded houselight containing a GE 1820 lamp was located 7.6 cm above the center key. The houselight provided general chamber illumination. White noise at 72 dB and an externally mounted exhaust fan provided sound masking. A microcomputer in an adjoining room controlled the
Because the pigeons had previous experience pecking hues on the response keys, they were placed directly on the 0-s delay matching task with red and green samples and comparisons (identity matching). Responding to the sample was followed immediately by illumination of the R and G comparison stimuli, one on the left, the other on the right. A single peck to the matching comparison terminated the comparison stimuli, provided reinforcement, and started the 10-s intertrial interval (ITI). A single peck to the nonmatching comparison terminated the comparison stimuli and started the ITI. All sessions consisted of 96 trials counterbalanced for sample hue and the location of a reinforced response (left or right). A noncorrection procedure was used throughout the experiment. On the first session of training, there was a 5-peck response requirement to the samples presented on the center key; on Session 2, the response requirement was increased to ten pecks, and on Session 3 it was increased to 20 pecks. All pigeons were trained on the 0-s delay matching task to a criterion of 90% correct or better, for two consecutive sessions, on both R and G sample trials. As each pigeon attained the criterion at the 0-s delay, it was assigned to one of the two groups, approximately equated for rate of 0-s delay matching acquisition. Each pigeon was then transferred to trials involving 1.0-s delays, either between the sample and comparison stimuli (Group sample-delay-comparison) or between the comparison stimuli and outcome (Group sample-comparison-delay). During all delays, the white circle was presented on the response key just pecked (i.e. on the center key for pigeons in Group sample-delay-comparison, and on the chosen comparison key for pigeons in Group samplecomparison-delay). After attainment of criterion at the 1.0-s delay, the pigeons were transferred successively to 2.0-, 4.0-, 8.0-, and 16.0-s delays when criterion at the earlier delay was met. If a pigeon did not reach criterion within 30 training
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6
Table 1 Matching accuracy on the first two sessions of transfer at each delay, for Group sample-delay-comparison and for Group sample-comparison-delay Group
Delay (s) 1.0
2.0
4.0
8.0
16.0
S1
S2
S1
S2
S1
S2
S1
S2
S1
S2
SDC SCD
76.5 92.8
89.8 91.0
90.5 93.5
90.8 93.0
82.0 91.2
88.5 94.0
76.8 90.0
77.2 87.0
67.7 93.7
63.3 82.0
Mean
84.6
90.4
92.0
91.9
86.6
91.2
83.4
82.1
80.7
72.6
SDC, Group sample-delay-comparison; SCD, Group sample-comparison-delay; S1, Session 1; S2, Session 2.
sessions at a particular delay, it was dropped from the experiment at that point. All pigeons that attained criterion at 8.0-s delays were tested for 10 sessions at the 16.0-s delay. In all analyses, the.05 level of statistical significance was adopted.
3. Results The groups did not differ significantly in the rate at which they acquired the original matching task with 0-s delays, F(1,6) =4.25, or the rate at which they acquired delayed matching at any of the transfer delays (1.0, 2.0, 4.0, and 8.0 s), F B 1, F(1,6) =3.43, F B 1, and F B1, respectively. Two pigeons, one in each group, failed to attain criterion at the 8.0-s delay within 30 sessions and thus, were not transferred to the 16.0-s delay. It is possible that the delay of reinforcement following comparison choice contributed to the failure to attain criterion at the 8.0-s delay. For Group sample-comparison-delay, not only might the association between comparison responding and reinforcement be weakened as the delay increases but the increasing delay may result in the inability to predict when reinforcement will occur and, thus, may lead to missed reinforcers. Such an account is unlikely, however, because only one of these pigeons came from Group sample-comparison-delay. Furthermore, the absence of reinforcement typically results in the failure to initiate a trial (i.e. a failure to respond to the sample) rather than a failure to attain criterion, and neither pigeon showed any evidence of ‘stalling’. For
purposes of the 8.0-s analysis, these two pigeons were given scores of 31 sessions. The acquisition data for pigeons in both groups are presented in Table 1. Mixed two-way analyses were performed on the transfer data at each delay with Group (samplecomparison-delay versus sample-delay-comparison) and Session (1 versus 2) as factors. Overall, the level of matching accuracy on the first two sessions of transfer for Group sample-comparison-delay was significantly higher than for Group sample-delay-comparison at the 1.0- and 8.0-s delays, F(1,6)= 6.38, and 9.50, respectively, but not at the 2.0- and 4.0-s delays, FB 1 and F(1,6)= 1.89, respectively. There was also a significant increase, overall, in matching accuracy between Session 1 and Session 2 at the 1.0-s delay, F(1,6)= 8.56, but not at the 2.0-, 4.0-, or 8.0-s delays, FB 1, F(1,6)= 3.81, FB 1, respectively. In addition, Group sample-delay-comparison showed a significantly larger improvement in matching accuracy between Sessions 1 and 2 at the 1.0-s delay, than did Group sample-comparison-delay, F(1,6)= 14.56, but not at the 2.0-, 4.0-, or 8.0-s delays, all FsB 1. The significant interaction at the 1.0-s delay can be attributed to the relatively large initial decrease in matching accuracy for Group sample-delay-comparison, produced, perhaps, by disruption of the timing of comparison choice when delays were first introduced. This conclusion is suggested by the rather rapid recovery from this initial disruption of matching accuracy by Group sample-delay-comparison. However, Group sample-comparison-de-
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lay showed no decrease in matching accuracy on the first transfer session involving 1.0-s delays thus, little improvement was possible on Session 2. As noted earlier, two of the pigeons, one in each group, failed to attain criterion at the 8.0-s delay. Thus, only three pigeons in each group were tested at the 16.0-s delay. At the 16.0-s delay, matching accuracy for Group sample-comparison-delay was significantly higher than for Group sample-delay-comparison, F(1,4) = 25.76. In addition, overall, there was a significant decrease in matching accuracy between Session 1 and Session 2, F(1, 4)= 13.32. The Group× Sessions interaction was not significant, F(1,4) = 2.80. The level of matching accuracy on the first two sessions of transfer at each delay, for each group, appears in Table 2. To better isolate the regular change in matching accuracy between Session 1 and Session 2 as a function of increasing delay, a linear trend analysis was performed on the combined data from all delays (using only data from those pigeons that had experienced all of the delays). The linear trend analysis indicated that there was a significant systematic change in the difference between matching accuracy on Sessions 1 and 2, over Table 2 Sessions to criterion at each delay, for pigeons in Group sample-delay-comparison and for Group sample-comparisondelay Group
Pigeon
Delay (s) 0.0
1.0
2.0
4.0
8.0
16.0
SDC
8837 9872 4378 3507 Mean
6 12 6 11 8.8
4 3 3 4 3.5
2 3 4 4 3.2
13 4 2 3 5.5
6 * 9 7 *
* * * * *
SCD
9888 10 060 9972 4179 Mean
14 10 13 13 12.5
4 2 4 2 3.0
2 2 3 2 2.2
13 3 6 2 6.0
6 * 8 2 *
* * 6 * *
SDC, Group sample-delay-comparison; SCD, Group samplecomparison-delay. * Indicates criterion was not attained.
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Fig. 1. Improvement in matching accuracy from Session 1 to Session 2 (S2 – S1) at each delay for Groups sample-comparison-delay and sample-delay-comparison combined.
delays, independent of group, F(1,16)= 15.08. A graphical presentation of delayed-matching accuracy on Session 2 minus that on Session 1 is presented in Fig. 1. Although a session of experience appears to have resulted in an improvement in matching accuracy at the 1-s delay, there was no such improvement at the 2-, 4-, and 8-s delays, and there was a significant decrease in matching accuracy for pigeons that were transferred to the 16-s delay.
4. Discussion Data from the present experiment (as well as those from two earlier studies) indicate that with sufficiently long delays, accuracy of delayed matching with a fixed (predictable) delay will decrease from the first transfer session (at a longer delay) to the second transfer session. Furthermore, the results of the present experiment suggest that the Session 2 decrement in matching accuracy is probably attributable to the delay of reinforcement between the sample and outcome. Although overall matching accuracy was higher when the delays were inserted between presentation of the comparison stimuli and reinforcement than when they were inserted between presentation of the sample and presentation of the com-
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parisons, comparable decrements in matching accuracy (between Sessions 1 and 2) were found for both groups. Apparently, the increased delay of reinforcement for sample-orienting behavior weakens the association between that behavior and the outcome. The weakened association may interfere with matching accuracy by decreasing attention to or responding to the sample. Alternatively, experiencing an increase in delay between sample behavior and reinforcement may induce an emotional response (e.g. frustration) in the pigeon, which in turn may disrupt matching accuracy. This interpretation of the present data is consistent with findings by McCarthy and Davison (1986) that matching accuracy declines not only when delays are inserted between samples and comparisons but also when delays are inserted between samples and outcomes. Furthermore, consistent with McCarthy and Davison’s results, the sample-comparison delay was more detrimental to matching accuracy than the comparisonoutcome delay. This difference in the slope of the retention function may reflect the actual loss in memory, independent of delay of reinforcement. On the other hand, the fact that comparable effects were found in both groups suggests that the decrease in matching accuracy on Session 2 is attributable neither to a deficit in working memory for the sample (there was negligible memory load for Group sample-comparison-delay), nor to the lack of familiarity with the novel delays. A disruption in matching accuracy attributable to memory loss or to the novelty of the longer delays (generalization decrement) would be expected to appear on the first transfer session and perhaps to actually diminish somewhat by the second session. Instead, the Session 2 decrement in matching accuracy depends on the anticipation of the longer delay which appears to take about a session to develop. This notion of delay anticipation is consistent with the finding that matching accuracy at a particular delay depends on the delay context in which memory is assessed (Hartl et al., 1996; Honig, 1987; Zentall et al., 1978). This research indicates that, independent of the actual delay on a particular trial, matching accuracy is at a higher
level when the mean (i.e. the expected) delay is shorter than when it is longer. The fact that the Session 2 decrement in matching accuracy appeared at different delays in the three experiments reported may have been produced by differences in procedure. The decline in matching accuracy on Session 2 found by Kaiser et al. (1997) appeared earlier (i.e. at 4.0-s delays) than in both the present study or in Jagielo and Zentall (1986). In Kaiser et al. (1997), however, only a small proportion of the trials in each session were delayed matching trials. In the Jagielo and Zentall experiment, all the trials were delayed matching trials (i.e. they were tests of sample memory) and the decrease in matching accuracy on Session 2 appeared when the 8.0-s delays were introduced. However, unlike in the present experiment, all of the pigeons exposed to those 8.0-s delays in the Jagielo and Zentall study showed a profound increase in latency to peck the samples. The reason for this increase in sample-response latency appears to have been the absence of a stimulus (during the delay) that could help the pigeons mediate the delay. Presentation of a stimulus on the response key during the delay may provide the pigeons with a convenient place to peck during the delays and may also make the delays more distinctive from the intertrial interval. Furthermore, in the present experiment, the sample peck requirement was 20 pecks (considerably more than the 5-peck requirement in Jagielo and Zentall (1986)). The result of these changes in the procedures used in the present experiment appears to have been that the Session 2 decrement in matching accuracy occurred later in the present experiment (i.e. at 16.0-s delays) than in earlier research and the latency to respond to the samples was not problematic, even at those long delays. Apparently, the delay at which the effect occurs depends on the training conditions, including perhaps whether or not there is a stimulus presented during the delay, the number of responses required to the sample, and the proportion of matching-to-sample trials in a session. The Session 2 decrement in matching performance is more than a curious anomaly. Effects of delay of reinforcement of sample-orienting behavior have not generally been considered as a con-
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tributor to decrements in delayed matching accuracy. However, even in experiments in which mixed delays have been used, there is evidence that nonmemorial performance deficits contribute to the delay gradients typically found. Generally, pigeons are trained on a 0-s-delayedmatching task prior to the introduction of mixed delays. Furthermore, in many experiments, some trials with 0-s delays are included among the longer delays. When one compares matching accuracy at the end of 0-s-delay training (typically pigeons are trained to a criterion of 90% correct or higher matching accuracy for one or more sessions) with that on 0-s-delay trials during the memory test with mixed delays, it is not unusual to find a decrement in matching accuracy that cannot be attributed to memory loss or to generalization decrement. For example, when we examined data collected by Sherburne and Zentall (1995), we found that the pigeons performed at 93.4% correct on the last two sessions of training and that they showed a significant decrease in matching accuracy to 81.6% correct on 0-s-delay trials (trials identical to those experienced during training), over the first ten sessions of mixed-delay testing, F(1,6)= 156.84. Similarly, when we examined data collected by Zentall et al. (1995), we found that matching accuracy was at 90.5% correct at the end of 0-s-delay training, whereas it had decreased, significantly, to 81.0% correct on 0-s-delay trials during mixed delay tests (pooled over the test sessions), F(1,11) =32.04. Thus, an effect similar to that reported in the present study can be found under conditions in which the delay is unpredictable, but in which, on average, a longer delay of reinforcement of sample-orienting behavior can be expected than that experienced during training. The decrements in matching accuracy found on Session 2 of transfer to longer delays (Jagielo and Zentall, 1986, Experiment 1; Kaiser et al., 1997; and the present study), together with the parallel findings from experiments in which mixed-delay training is provided, suggest that the anticipation of delay of reinforcement of sample-orienting behavior plays an important role in decrements in matching accuracy that result from the introduction of delays between samples and comparisons when the delayed matching procedure is used.
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When using a mixed-delay condition, one might expect that this delay-of-reinforcement variable would have a relatively constant effect on matching accuracy, over trials, within a given mixed-delay condition, because it should depend on the anticipated delay of reinforcement. If so, it would be expected to affect matching accuracy similarly at all delays and the slope of the retention function would still be a reasonable measure of memory loss. It is also possible, however, that even with a mixed-delay procedure, there are differential effects on matching accuracy at different delays. For example, at the longest delays in a mixed-delay procedure, when the delay of reinforcement would be longer than average (i.e. longer than that expected), matching accuracy may be additionally disrupted. In any case, future research in animal memory (especially that involving delayed matching) should acknowledge the possible contribution of the effect of delay of reinforcement of sample-orienting behavior to the purported decline in memory over time as evidence by a decrease in matching accuracy with increasing sample-comparison delay. Acknowledgements This research was supported by National Science Foundation Grants BNS-8418275 and BNS9019080 and National Institute of Mental Health Grant 45979 to Thomas R. Zentall. References Blough, D.S., 1959. Delayed matching in the pigeon. J. Exp. Anal. Behav. 2, 151 – 160. Grice, G.R., 1948. The relation of secondary reinforcement to delayed reward in visual discrimination learning. J. Exp. Psychol. 38, 1 – 16. Hartl, J.A., Dougherty, D.H., Wixted, J.T., 1996. Separating the effects of trial-specific and average sample-stimulus duration in delayed matching to sample in pigeons. J. Exp. Anal. Behav. 66, 231 – 242. Honig, W.K., 1987. Memory interval distribution effects in pigeons. Anim. Learn. Behav. 15, 6 – 14. Jagielo, J.A., Zentall, T.R., 1986. Predictable long-delay matching-to-sample trials result in long-latency sample responding by pigeons. Learn. Motiv. 17, 269 – 286.
T.R. Zentall et al. / Beha6ioural Processes 43 (1998) 1–10
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Kaiser, D.H., Sherburne, L.M., Zentall, T.R., 1997. Directed forgetting in pigeons resulting from the reallocation of memory-maintaining processes on forget-cue trials. Psychonom. Bull. Rev. (in press). McCarthy, D., Davison, M., 1986. Delayed reinforcement and delayed choice in symbolic matching to sample: Effects on stimulus discriminability. J. Exp. Anal. Behav. 46, 293– 301. Roberts, W.S., 1972. Short-term memory in the pigeon: Effects of repetition and spacing. J. Exp. Psychol. Anim. Behav. Process. 6, 217 – 237. Sacks, R.A., Kamil, A.C., Mack, R., 1972. The effects of fixed-ratio sample requirements on matching-to-sample in the pigeon. Psychonom. Sci. 26, 291–293.
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Sherburne, L.M., Zentall, T.R., 1995. Delayed matching in pigeons with food and no-food samples: Further examination of backward associations. Anim. Learn. Behav. 23, 177 – 181. Zentall, T.R., 1997. Animal memory: the role of ‘instructions’. Learn. Motiv. 28, 280 – 308. Zentall, T.R., Hogan, D.E., 1977. Short-term proactive inhibition in the pigeon. Learn. Motiv. 8, 367 – 386. Zentall, T.R., Hogan, D.E., Howard, M.M., Moore, B.S., 1978. Delayed matching in the pigeon: Effect on performance of sample-specific observing responses and differential delay behavior. Learn. Motiv. 9, 202 – 218. Zentall, T.R., Sherburne, L.M., Urcuioli, P.J., 1995. Coding of hedonic and nonhedonic samples by pigeons in many-toone delayed matching. Anim. Learn. Behav. 23, 189 – 196.