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Short-term incidental memory for irrelevant cues
Behavioural Processes 64 (2003) 41–48
Short-term incidental memory for irrelevant cues Jonathan M. Reed∗ , Lisa D. Ellington, Robert B. Graham, Larry W. Means Department of Psychology and Program in Neuroscience, East Carolina University, Greenville, NC 27858, USA Received 19 February 2003; received in revised form 19 February 2003; accepted 17 April 2003
Abstract A new analysis of previously published studies of delayed matching-to-sample (DMTS) water-escape and the results of a new food-reinforced discrimination study are presented. In both cases, male Sprague–Dawley rats demonstrated short-term incidental memory for irrelevant cues in the context of two-alternative forced-choice problems that required learning about relevant cues. In the DMTS experiments, relevant and irrelevant cues were place or brightness. In the discrimination experiment, the relevant cues were place, brightness or a visual–tactile maze insert. In all experiments, after the rats attained high-level performance, consistently making choices with respect to the relevant stimuli, response latencies to the correct relevant cue were shorter when the irrelevant cue value(s) was the same as on the immediately preceding trial. These latency differences are interpreted as indicating that the rats demonstrated short-term incidental memory for the irrelevant cues. This mnemonic phenomenon resembles priming, an implicit form of memory. © 2003 Elsevier B.V. All rights reserved. Keywords: Incidental memory; Priming; Implicit memory; Delayed matching-to-sample; Discrimination learning; Water maze; Cross maze
1. Introduction It has long been known that discrimination learning involves learning first which cues are relevant and then which value of the relevant cue is associated with reinforcement (Sutherland and Mackintosh, 1971). Once the relevant cues are determined, the other cues become irrelevant. Presumably, the subject’s attention becomes focused on the relevant cues. Once subjects are consistently making correct choices, it seems reasonable to assume that the irrelevant cues no longer affect behavior. However, during training and subsequent testing of rats on delayed matching-to-sample (DMTS) water-escape problems, we noticed that re∗ Corresponding author. Tel.: +1-25-232-862-44; fax: +1-25-232-865-53. E-mail address: [email protected] (J.M. Reed).
sponse latencies seemed to be greater when making the correct choice on the test portion of the trial, i.e. going to the positive value of the relevant stimulus, involved going to a different value of the irrelevant stimulus than was experienced on the sample portion of the trial. That is, although irrelevant cues did not appear to influence choice accuracy, they did influence response latency. It is well documented that rats have long-term incidental memories for stimuli that remain constant and to which they are exposed repeatedly or for an extended period of time. Examples of long-term incidental memory would include habituation (Thompson and Spencer, 1966), latent learning (Thistlewaite, 1951; Tolman and Honzik, 1930), CS preexposure effect (Lipp et al., 1992; Lublow and Moore, 1959), sensory preconditioning (Brogden, 1939; Wynne and Brogden, 1962) and homecage stimulus exposure
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facilitated discrimination learning (Gibson et al., 1958; Hall, 1979). Do rats also have short-term incidental memory for specific cue values that change from one trial to next and are only briefly experienced?
2. Experiment 1: DMTS and short-term incidental memory In search of evidence for short-term incidental memory, we re-examined data from two previously published DMTS water-escape studies (Graham et al., 1998; Means et al., 1997). Did irrelevant cues influence response latencies in animals consistently making correct choices? In both studies, male Sprague–Dawley rats were required to learn two-alternative DMTS problems in a water maze in the presence of two cues. To solve one of the problems, on test swims, rats in a place-learning group (Group P) needed to return to the spatial location of the escape platform experienced on the sample swim (Graham et al., 1998). To solve the other problem, rats in a brightness-learning group (Group B) needed to return to the choice section that matched the sample swim brightness value (Graham et al., 1998; Means et al., 1997). In both problems, brightness and spatial location varied independently. Thus, the untrained cue was irrelevant (i.e. paired with the correct response on 50% of the trials). 2.1. Method Complete procedural details are given in the original publications (Graham et al., 1998; Means et al., 1997). Both studies were conducted in a circular tank divided into a start compartment and two-choice compartments by a stainless steel barrier. The tank was placed in a dark room with a 25 W white incandescent light mounted above the escape platform in each of the two-choice compartments. On any given swim, the cue light of the “bright” choice compartment provided the only light in the room. Also, on both tasks each trial consisted of a forced-choice sample phase, a 5 m retention interval, and a two-alternative free-choice test phase. During the sample phase, the subject was released in the start compartment and a sliding panel was positioned to prevent entrance into the incorrect choice compartment. The rat was permitted to swim to
the correct choice compartment where it would mount the escape platform. The rat remained on the platform while data were recorded and was then returned to its home cage for the duration of the retention interval. During the test phase, the rat was released at the same starting location, but the sliding panels were positioned to permit access to both choice compartments. If a rat first entered the incorrect choice compartment, a sliding panel was positioned to retain the rat in the compartment for 30 s, after which the panel was reopened, allowing the rat to swim back through the start compartment to the platform in the correct choice compartment. The rats were trained to a criterion of nine correct test choices on 10 consecutive trials. Response choices and latencies were recorded for all trials. 2.2. Results Data from both groups of rats were submitted to an analysis to determine if short-term memory for irrelevant cues was in evidence. It was reasoned that if a rat remembered the irrelevant cue from the information phase of a trial, it would swim faster in the test phase of that trial if the correct location was associated with the same as opposed to the opposite irrelevant cue value. In other words, remembering the irrelevant cue would hasten performance on trials where the cue values were the same for both phases of a trial. Thus, latency scores obtained by subjects during the 10 trials on which the rats attained the criterion of 9 correct responses on 10 consecutive trials were used to obtain a ratio. The ratio, mean latency on “same” trials divided by mean latency on “opposite” trials, was computed for each subject. Following the above-stated reasoning, ratios less than 1 would be consistent with the rat remembering the irrelevant cue presented in the preceding trial phase. Trials on which subjects made errors were excluded from the analysis. For both Experiments 1 and 2, means of median response latency ratios were compared to a value of 1 using an alpha level of 0.05 and theory-appropriate, directional, single-sample t tests. Fig. 1 shows means of median response latency ratios on criterion trials of rats that attained criterion on the DMS water-escape task when place was the relevant cue (Group P), when brightness was the relevant cue (Group B), and when both groups were combined.
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3. Experiment 2: discrimination and short-term incidental memory The purpose of the present study was to test the robustness of this finding. Thus, three groups of rats were trained in a “+”-shaped maze in which either spatial location, response-generated cues (left or right turn), or a maze insert was relevant while the other cues were irrelevant. Is short-term incidental memory that we observed in DMTS water-escape also evidenced in a food-reinforced, two-choice discrimination where there are two irrelevant cue dimensions? 3.1. Method Fig. 1. Mean of median latency ratios of rats on the nine test runs for which they made correct choices while attaining criterion in Experiment 1 (Graham et al., 1998; Means et al., 1996). Incorrect choice trials were omitted. Latency ratios are presented for the place-learning rats (Group P, left), the brightness-learning rats (Group B, middle), and for both groups combined (right). Brackets indicate the standard errors of the means. The broken line corresponds to a latency ratio expected if animals were equally fast when irrelevant cues present during test phases were the same as or different from those present during the information phase.
For Group P (Graham et al., 1998), 5 of the 10 rats had median latency ratios less than 1 (M = 0.931, S.E.M. = 0.139). The mean latency ratio, however, was not significantly less than 1, t(9) < 1.0. It is likely that this failure to find a statistically significant difference for this group was due to the small sample size and insufficient power (the probability of correctly rejecting the null hypothesis was only 0.17). For Group B (Graham et al., 1998; Means et al., 1997), 16 of the 18 rats had median latency ratios less than 1 (M = 0.811, S.E.M. = 0.083), and the mean latency ratio was significantly less than 1, t(17) = 2.263. Because the type of relevant cue encountered (place or brightness) was immaterial to the determination of whether or not the rats demonstrated implicit memory for irrelevant cues, the data were also collapsed across the two groups. When data from all 28 rats were examined (M = 0.854, S.E.M. = 0.072), mean latency ratios were significantly below 1, t(27) = 2.013. Clearly, response latencies on the DMTS water-escape problems were affected by the irrelevant cues even though rats were using relevant cues to make accurate responses.
3.1.1. Participants Thirty male Sprague–Dawley rats weighing approximately 225 g at the beginning of the study were used as subjects. They were housed individually in plastic cages in a room maintained at 23±2 ◦ C with a 12/12-h light/dark cycle with lights turned on at 07:00 h. The rats had water available continuously and were given lab chow to maintain them at their 85% ad lib weight, which was increased by 5 g each week. 3.1.2. Apparatus A gray, elevated (90 cm above the floor) T-maze was used for all behavioral testing. The stem and both goal arms were 9.5 cm wide. The stem was 37 cm long and the goal arms were each 50 cm long. The entire maze had a 2 cm high border. A circular 1 cm deep food well was located at the end of each goal arm. An insert was placed in the appropriate goal arm for each trial. The insert was white, 36-cm long and 9.5-cm wide, and had three 2-cm high hurdles. The floor of the insert was covered with 7-cm hardware cloth. The maze was placed in a room providing many extramaze cues including a table, large stimulus cards mounted on two walls, and a wall-mounted air conditioner. 3.1.3. Procedure The rats were given 4 days of maze adaptation during which nine Cocoa Puffs® (General Mills Sales, Inc.) were distributed on the maze, including one in each of the two food wells. All adaptation and subsequent training sessions began at 09:00 h, which was 2 h after the lights were turned on. During each adaptation session, a rat was released at the starting
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Fig. 2. Examples of maze arrangements during two consecutive trials in Experiment 2. The Ss indicate starting locations, shaded rectangles indicate maze insert placements, and circles indicate reinforcement placements. For each example, the relationship between the relevant cue and the reinforcement is identical for the study and test phases whereas the relationships among the irrelevant cues and the reinforcement are opposite for the two trials.
position of the stem and allowed to explore the maze for 5 m or until it had eaten all the Cocoa Puffs. Upon completion of adaptation, 10 rats were randomly assigned to each of three explicit discrimination groups: Group P, turn learning (Group T), and visual–tactile insert learning (Group V). The two maze arrangements for each of the groups are shown in Fig. 2. Rats in Group P had to go to the same physical location in the room to obtain reinforcement. The location of the visual–tactile maze insert or the turn required, which were changed on a semi-random schedule, were irrelevant. Rats in Group T had to make the same right or left turn at the choice point to attain the reinforcement. The location of the maze insert and the physical location of the reinforcement were irrelevant. Rats in Group V had to always enter either the arm with the visual–tactile insert or the arm without the insert to obtain food. Turn and place were irrelevant. Thus, all three types of choice cues were available for each of the discrimination groups, but only one type was relevant with respect to the location of the reinforcement. The two irrelevant cues were always present to potentially influence the rats’ behavior. On a semi-random half of the trials both of
the irrelevant cues were arranged the same as on the preceding trial, whereas on the other half both of the irrelevant cues were arranged opposite as the preceding trial. No trial involved one irrelevant cue being the same and one being opposite as on the preceding trial. Each rat was given eight trials per day 5 days per week for 12 days, for a total of 96 trials. The rats were tested in squads of five and had inter-trial intervals of approximately 5 m. Each trial consisted of placing the rat in the start box such that it faced directly away from the choice point. The rat was then permitted to make a choice, when a barrier was placed behind the rat to prevent retracing or a second choice. All correct choices were reinforced with two Cocoa Puffs placed in the appropriate food well. A stopwatch was used to measure response latencies. The stopwatch was always terminated when the rat made a choice, entire body, excluding the tail, in a goal arm. During the first block of 24 trials the timer was activated at the time the rat was released. Because of considerable variability in the time it took rats to orient to the choice point, the timer was not activated until the rat oriented to the choice point for the last three blocks of 24 trials. The rat was left on the goal arm while the choice and response latency were being recorded. Following each daily session the rats were weighed and fed their appropriate ration. 3.2. Results 3.2.1. Acquisition Nearly all rats acquired their respective explicit discrimination problems and the groups did not differ significantly. Fig. 3 shows the mean percent correct choices made by each of the three groups over the four blocks of trials. A Group × Block mixed-factors ANOVA on the percent correct choices resulted in only a significant Block effect, F(3, 81) = 44.6, P = 0.000. Post hoc Fisher’s least squares tests revealed that performance on Block 1 differed from performance on Block 2 which differed from Block 3 (P < 0.05 in each case). Blocks 3 and 4 did not differ from one another. 3.2.2. Irrelevant cues One rat in Group T and two rats in each of the other two groups failed to achieve 90% correct choices over the last two blocks of 24 trials and, therefore, their data
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Fig. 3. Mean percentage correct choices made by animals in Experiment 2 while explicitly learning about the relevant cues.
were not included in the analysis of the influence of the irrelevant cues. Following the procedure described above, a median latency ratio (same/opposite) was determined for each of the remaining subjects based on the last two blocks of trials. Only correct choice trial latencies were used to determine the ratios. Recall that a latency ratio <1.0 indicates that rats made correct choices faster on trials where the irrelevant stimuli were the same as opposed to opposite as the immediately preceding trial. Fig. 4 shows means of median latency ratios for all three groups. For Group P (M = 0.923, S.E.M. = 0.050), Group T (M = 0.938, S.E.M. = 0.040), and Group V (M = 0.919, S.E.M. = 0.033), six of the eight rats, six of nine rats, and eight of eight rats had latency ratios less than 1, respectively. Latency ratios were not significantly different from 1 for Group P (t(7) = 1.537) or Group T (t(8) = 1.531), but these tests were associated with rather low power (the probability of correctly rejecting the null hypothesis was 0.33 in both cases). By contrast, for Group V (power = 0.66), latency ratios were significantly less than 1, t(7) = 2.374. In addition, when the data from all three groups were combined, latency ratios were significantly less than 1, t(25) = 3.128. This final outcome was considered the most revealing because examination of short-term incidental memory for irrelevant cues was not expected to depend upon the type of relevant cue associated with a particular group. Clearly, most rats in all three discrimination groups had shorter response latencies on trials where
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Fig. 4. Mean of median latency ratios of rats on the last 48 trials during which animals were making at least 90% correct choices in Experiment 2. Incorrect choices were omitted. Latency ratios for the place-learning rats (Group P, far left), for the turn-learning rats (Group T, middle left), for the visual–tactile-learning rats (Group V, middle right), and for all three groups (far right) are presented. Brackets indicate the standard errors of the means. The broken line corresponds to a latency ratio expected if animals were equally fast when the relationship between the response and an irrelevant cue were the same or different on consecutive trials.
the irrelevant cue values were the same as on the immediately preceding trial. In contrast, rats did not make more correct responses on “same” trials (M = 97.038, S.E.M. = 1.622) than on “different” trials (M = 98.538, S.E.M. = 0.506), t(25) < 1.0.
4. General discussion Rats demonstrated short-term incidental memory for irrelevant cues in both the DMTS water-escape paradigm and the two-choice food-reinforced discrimination paradigm. The former task requires memory for trial-dependent cue values, sometimes called working memory (Honig, 1978; Olton et al., 1979), whereas the later task requires memory only for a given cue value independent of trial, referred to as reference memory (Honig, 1978). Response latencies to relevant cues were shorter when an irrelevant cue shared the same relationship to the response that it did during the preceding response compared to when the relationship between the irrelevant cue and the response had changed. Because rats exhibited short-term incidental memory in two types of tasks differing in number of irrelevant cue dimensions, reinforcement,
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and mnemonic requirements, it appears that the phenomenon is quite robust. A similar finding has recently been reported (Kesner, 1998). He used a between-subjects design to examine explicit and what he termed implicit learning in rats. All animals were trained with a sequence of 12 forced responses in a 12-arm radial maze. Three or four of the responses involved a repeated response (i.e. a second visit to a maze location). In the explicit learning group, reinforcement was available only on the first visit to a particular maze location. Thus, the relationship between the location cues and the availability of reinforcement “instructed” rats to remember which locations they had visited previously. In the implicit learning group, reinforcement was available on all visits to maze locations. For these rats, the relationship between location cues and the availability of reinforcement was irrelevant and, therefore, memory for location was incidental. Thus, the learning situation (i.e. the relationship between environmental cues and the availability of reinforcement) was used to manipulate the instructional set that the animals received. Intentional explicit memory for location was indicated by longer maze-running latencies for repeated locations compared to latencies for nonrepeated locations. In contrast, the implicit group showed implicit memory for location as indicated by shorter maze-running latencies for repeated locations compared to nonrepeated locations. Clearly, the phenomenon Kesner called implicit memory is very similar to what we are calling short-term incidental memory. The present demonstrations of short-term incidental memory do not permit one to know the underlying mechanism. The experimental procedures employed permit some potential explanations to be dismissed. Short-term incidental memory is not due to iconic or sensory memory (Sperling, 1960), as the 5-min retention interval far exceeds the demonstrated duration of sensory memory. In addition, it is not due to differential reinforcement of the irrelevant cue values as all irrelevant cue values are reinforced on 50% of the trials. To some extent, our demonstrations of short-term incidental memory resemble findings from studies of matching-to-sample (MTS) performance of pigeons. The observation that pigeons select correct element choices more often when responding to element samples (line orientation or color) compared to when they are responding to compound samples (line orienta-
tion and color) is called the element superiority effect (e.g. Cook et al., 1992; Lamb, 1988; Maki and Leith, 1973). One way of accounting for the element superiority effect is via the generalization decrement hypothesis (e.g. Brown and Morrison, 1990; Grant and MacDonald, 1986; Langley and Riley, 1993; Roberts and Grant, 1978; Santi et al., 1982). According to this view, “control by compound samples is reduced due to the lack of an exactly matching comparison stimulus” (Maki et al., 1976). In our Experiment 1, MTS performance benefited when samples exactly matched correct choices. In the discrimination experiment (Experiment 2), a similar advantage for exact matches was also exhibited. This discrimination advantage is analogous to the MTS advantage if one views each discrimination trial as equivalent to a sample and one views each subsequent discrimination trial as equivalent to a matching test. Thus, in both experiments, one might interpret the reported advantages according to a generalization decrement account. Unlike reports of the element superiority effect, however, the performance advantage was not related to greater accuracy, but rather faster responding. The fact that our “same” trial advantage applies to response latencies but not to response accuracy is a primary reason for characterizing the advantage as an incidental rather than intentional memory phenomenon. As pointed out above, the intent of an animal subject must be inferred from the contingencies to which it is responding. In the present experiments the rats were reinforced with either food or water-escape for going to a particular stimulus value. Because all latency scores included in the analyses were based on correct choice trials made when the animals were performing at a 90% correct choice level, it can be assumed that the intent of the rat was to enter the choice arm or section containing the relevant cue, i.e. the cue that had been associated with reinforcement on every prior approach to that cue. This being the case, any change in response associated with the irrelevant cues must have been incidental. The incidental influence of irrelevant cues on response latencies of rats is similar to priming observed in humans (Schacter et al., 1993) and, perhaps, animals (Blough, 1991; Langley et al., 1996). Priming is enhanced stimulus processing resulting from prior exposure to the stimulus or exposure to a similar or
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related stimulus. For example, people identify strings of letters as words more quickly when the word presentations are repeated (Just and Carpenter, 1980). It is thought that the initial presentation of a word activates a mental representation of the word. This activation persists and thereby allows one to respond to the same word more quickly when it is encountered again. In the studies we described, the irrelevant cues can be viewed as priming events. When the properties of these priming events match those present during a subsequent test trial, a type of repetition priming occurs. That is, the rats’ performance is enhanced as a result of prior exposure to these cues. Because the priming cues are irrelevant, however, their influence might best be described as contextual priming. Priming is considered a form of implicit (nondeclarative) memory for three reasons. First, the priming events can enhance performance even when primes are presented below the threshold of conscious identification (Marcel, 1983). Second, priming-based enhancement is noted when the priming events can no longer be consciously recalled (Tulving et al., 1982). Third, priming effects are entirely normal in amnesic patients whose declarative memory is impaired due to damage to medial temporal lobe memory structures (Hamann and Squire, 1997). Because short-term memory shares many properties with priming, a form of implicit memory, and because the intention of a rat cannot be known beyond what is determined by the reinforcement contingencies to which it is responding, short-term incidental memory may be viewed as an analog for the study of implicit memory in nonhuman subjects. Studies of human amnesia indicate that conscious recollection does not always accompany normal memory-based task performance (Hamann and Squire, 1997). Amnesic patients with damage to the medial temporal lobe or midline diencephalon exhibit impairments on recall and recognition tests that require conscious recollection. The same patients, by contrast, exhibit normal priming and other memory-based abilities that do not depend upon conscious recollection. It has been suggested, therefore, that the brain structures damaged in amnesic patients support explicit memory but that different brain areas support implicit memory. Thus, these studies link the phenomalogically different memory forms to anatomically distinct
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neural substrates. An obvious test of our supposition that short-term incidental memory is an infrahuman analog of human priming or implicit learning, is to test in animals with a compromised medial temporal lobe whether short-term incidental memory is preserved on a task where the explicit memory is impaired.
Acknowledgements Supported by a grant from the East Carolina University Research/Creative Activity Committee to LWM. References Blough, P.M., 1991. Selective attention and search images in pigeons. J. Exp. Psychol.: Anim. Behav. Proc. 17, 292–295. Brogden, W.J., 1939. Sensory preconditioning. J. Exp. Psychol. 25, 323–332. Brown, M.F., Morrison, S.K., 1990. Element and compound matching-to-sample performance in pigeons: the roles of information load and training history. J. Exp. Psychol.: Anim. Behav. Proc. 16, 185–192. Cook, R.G., Riley, D.A., Brown, M.F., 1992. Spatial and configural factors in compound stimulus processing by pigeons. Anim. Learn. Behav. 20, 41–55. Gibson, E.J., Walk, R.D., Pick Jr., H.L., Tighe, T.J., 1958. The effect of prolonged exposure to visual patterns on learning to discriminate similar and different patterns. J. Comp. Physiol. Psychol. 51, 584–587. Graham, R.B., Navey, B.R., Bass, E.W., Holsten, R.D., Means, L.W., 1998. A comparison of visual- and response-generated cues in a spatial DMTS task for rats. Physiol. Behav. 63, 635– 642. Grant, D.S., MacDonald, S.E., 1986. Matching to element and compound samples in pigeons: the role of sample coding. J. Exp. Psychol.: Anim. Behav. Proc. 12, 160–171. Hall, G., 1979. Exposure learning in young and adult laboratory rats. Anim. Behav. 27, 586–591. Hamann, S.B., Squire, L.R., 1997. Intact priming for novel perceptual representations in amnesia. J. Cogn. Neurosci. 9, 699–713. Honig, W.K., 1978. Studies of working memory in the pigeon. In: Hulse, S.H., Fowler, H., Honig, W.K. (Eds.), Cognitive Processes in Animal Behavior. Erlbaum, Hillsdale, NJ. Just, M.A., Carpenter, P.A., 1980. A theory of reading: from eye fixations to comprehension. Psychol. Rev. 87, 329–354. Kesner, R.P., 1998. Neurobiological views of memory. In: Martinez, J.L., Kesner, R.P. (Eds.), Neurobiology of Learning and Memory. Academic Press, San Diego. Lamb, M.R., 1988. Selective attention: effects of cueing on the processing of different types of compound stimuli. J. Exp. Psychol.: Anim. Behav. Proc. 14, 96–104.
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Langley, C.M., Riley, D.A., 1993. Limited capacity information processing and pigeon matching-to-sample: testing alternative hypotheses. Anim. Learn. Behav. 21, 226–232. Langley, C.M., Riley, D.A., Bond, A.B., Goel, N., 1996. Visual search for natural grains in pigeons (Columba livia): search images and selective attention. J. Exp. Psychol.: Anim. Behav. Proc. 22, 139–151. Lipp, O.V., Siddle, D.A.T., Vaitl, D., 1992. Latent inhibition in humans: single cue conditioning revisited. J. Exp. Psychol.: Anim. Behav. Proc. 18, 115–125. Lublow, R.E., Moore, A.U., 1959. Latent inhibition: the effect of nonreinforced preexposure to the conditional stimulus. J. Comp. Physiol. Psychol. 52, 415–419. Maki Jr., W.S., Leith, C.R., 1973. Shared attention in pigeons. J. Exp. Anal. Behav. 19, 345–349. Maki Jr., W.S., Riley, D.A., Leith, C.R., 1976. The role of test stimuli in matching to compound sample by pigeons. Anim. Learn. Behav. 4, 13–21. Marcel, A.J., 1983. Conscious and unconscious perception: an approach to the relations between phenomenal experience and perceptual processes. Cogn. Psychol. 15, 238–300. Means, L.W., Long, M., Jones, T.A., Curtis, W.C., 1997. Rats perform better on spatial than brightness delayed matching-to-sample water-escape due to an unlearned bias to use spatial cues. Physiol. Behav. 60, 1239–1245. Olton, D.S., Becker, J.T., Handelmann, G.E., 1979. Hippocampus, space and memory. Behav. Brain Sci. 2, 313–365.
Roberts, W.A., Grant, D.S., 1978. Interaction of sample and comparison stimuli in delayed matching-to-sample with pigeons. J. Exp. Psychol.: Anim. Behav. Proc. 4, 68–82. Santi, A., Grossi, V., Gibson, M., 1982. Differences in matchingto-sample performance with element and compound sample stimuli in pigeons. Learn. Motiv. 13, 240–256. Schacter, D.L., Chiu, C.-Y.P., Ochsner, K.N., 1993. Implicit memory: A selective review. Annu. Rev. Neurosci. 16, 159–182. Sperling, G. 1960. The information available in brief visual presentations. Psychol. Monogr. 74 (Whole No. 498). Sutherland, R.P., Mackintosh, N.J., 1971. Mechanisms of Animal Discrimination Learning. Academic Press, New York. Thistlewaite, D., 1951. A critical review of latent learning and related experiments. Psychol. Bull. 48, 97–129. Thompson, R.F., Spencer, W.A., 1966. Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol. Rev. 73, 16–43. Tolman, E.C., Honzik, C.H., 1930. Introduction and removal of reward, and maze performance in rats. Univ. California Publ. Psychol. 4, 257–275. Tulving, E., Schacter, D.L., Stark, H.A., 1982. Priming effects in word-fragment completion are independent of recognition memory. J. Exp. Psychol.: Learn. Memory Cogn. 8, 336– 342. Wynne, J.D., Brogden, W.J., 1962. Effect upon sensory preconditioning of backward, forward, and trace preconditioning training. J. Exp. Psychol. 64, 422–423.
Short-term incidental memory for irrelevant cues Jonathan M. Reed∗ , Lisa D. Ellington, Robert B. Graham, Larry W. Means Department of Psychology and Program in Neuroscience, East Carolina University, Greenville, NC 27858, USA Received 19 February 2003; received in revised form 19 February 2003; accepted 17 April 2003
Abstract A new analysis of previously published studies of delayed matching-to-sample (DMTS) water-escape and the results of a new food-reinforced discrimination study are presented. In both cases, male Sprague–Dawley rats demonstrated short-term incidental memory for irrelevant cues in the context of two-alternative forced-choice problems that required learning about relevant cues. In the DMTS experiments, relevant and irrelevant cues were place or brightness. In the discrimination experiment, the relevant cues were place, brightness or a visual–tactile maze insert. In all experiments, after the rats attained high-level performance, consistently making choices with respect to the relevant stimuli, response latencies to the correct relevant cue were shorter when the irrelevant cue value(s) was the same as on the immediately preceding trial. These latency differences are interpreted as indicating that the rats demonstrated short-term incidental memory for the irrelevant cues. This mnemonic phenomenon resembles priming, an implicit form of memory. © 2003 Elsevier B.V. All rights reserved. Keywords: Incidental memory; Priming; Implicit memory; Delayed matching-to-sample; Discrimination learning; Water maze; Cross maze
1. Introduction It has long been known that discrimination learning involves learning first which cues are relevant and then which value of the relevant cue is associated with reinforcement (Sutherland and Mackintosh, 1971). Once the relevant cues are determined, the other cues become irrelevant. Presumably, the subject’s attention becomes focused on the relevant cues. Once subjects are consistently making correct choices, it seems reasonable to assume that the irrelevant cues no longer affect behavior. However, during training and subsequent testing of rats on delayed matching-to-sample (DMTS) water-escape problems, we noticed that re∗ Corresponding author. Tel.: +1-25-232-862-44; fax: +1-25-232-865-53. E-mail address: [email protected] (J.M. Reed).
sponse latencies seemed to be greater when making the correct choice on the test portion of the trial, i.e. going to the positive value of the relevant stimulus, involved going to a different value of the irrelevant stimulus than was experienced on the sample portion of the trial. That is, although irrelevant cues did not appear to influence choice accuracy, they did influence response latency. It is well documented that rats have long-term incidental memories for stimuli that remain constant and to which they are exposed repeatedly or for an extended period of time. Examples of long-term incidental memory would include habituation (Thompson and Spencer, 1966), latent learning (Thistlewaite, 1951; Tolman and Honzik, 1930), CS preexposure effect (Lipp et al., 1992; Lublow and Moore, 1959), sensory preconditioning (Brogden, 1939; Wynne and Brogden, 1962) and homecage stimulus exposure
0376-6357/$ – see front matter © 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0376-6357(03)00077-9
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facilitated discrimination learning (Gibson et al., 1958; Hall, 1979). Do rats also have short-term incidental memory for specific cue values that change from one trial to next and are only briefly experienced?
2. Experiment 1: DMTS and short-term incidental memory In search of evidence for short-term incidental memory, we re-examined data from two previously published DMTS water-escape studies (Graham et al., 1998; Means et al., 1997). Did irrelevant cues influence response latencies in animals consistently making correct choices? In both studies, male Sprague–Dawley rats were required to learn two-alternative DMTS problems in a water maze in the presence of two cues. To solve one of the problems, on test swims, rats in a place-learning group (Group P) needed to return to the spatial location of the escape platform experienced on the sample swim (Graham et al., 1998). To solve the other problem, rats in a brightness-learning group (Group B) needed to return to the choice section that matched the sample swim brightness value (Graham et al., 1998; Means et al., 1997). In both problems, brightness and spatial location varied independently. Thus, the untrained cue was irrelevant (i.e. paired with the correct response on 50% of the trials). 2.1. Method Complete procedural details are given in the original publications (Graham et al., 1998; Means et al., 1997). Both studies were conducted in a circular tank divided into a start compartment and two-choice compartments by a stainless steel barrier. The tank was placed in a dark room with a 25 W white incandescent light mounted above the escape platform in each of the two-choice compartments. On any given swim, the cue light of the “bright” choice compartment provided the only light in the room. Also, on both tasks each trial consisted of a forced-choice sample phase, a 5 m retention interval, and a two-alternative free-choice test phase. During the sample phase, the subject was released in the start compartment and a sliding panel was positioned to prevent entrance into the incorrect choice compartment. The rat was permitted to swim to
the correct choice compartment where it would mount the escape platform. The rat remained on the platform while data were recorded and was then returned to its home cage for the duration of the retention interval. During the test phase, the rat was released at the same starting location, but the sliding panels were positioned to permit access to both choice compartments. If a rat first entered the incorrect choice compartment, a sliding panel was positioned to retain the rat in the compartment for 30 s, after which the panel was reopened, allowing the rat to swim back through the start compartment to the platform in the correct choice compartment. The rats were trained to a criterion of nine correct test choices on 10 consecutive trials. Response choices and latencies were recorded for all trials. 2.2. Results Data from both groups of rats were submitted to an analysis to determine if short-term memory for irrelevant cues was in evidence. It was reasoned that if a rat remembered the irrelevant cue from the information phase of a trial, it would swim faster in the test phase of that trial if the correct location was associated with the same as opposed to the opposite irrelevant cue value. In other words, remembering the irrelevant cue would hasten performance on trials where the cue values were the same for both phases of a trial. Thus, latency scores obtained by subjects during the 10 trials on which the rats attained the criterion of 9 correct responses on 10 consecutive trials were used to obtain a ratio. The ratio, mean latency on “same” trials divided by mean latency on “opposite” trials, was computed for each subject. Following the above-stated reasoning, ratios less than 1 would be consistent with the rat remembering the irrelevant cue presented in the preceding trial phase. Trials on which subjects made errors were excluded from the analysis. For both Experiments 1 and 2, means of median response latency ratios were compared to a value of 1 using an alpha level of 0.05 and theory-appropriate, directional, single-sample t tests. Fig. 1 shows means of median response latency ratios on criterion trials of rats that attained criterion on the DMS water-escape task when place was the relevant cue (Group P), when brightness was the relevant cue (Group B), and when both groups were combined.
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3. Experiment 2: discrimination and short-term incidental memory The purpose of the present study was to test the robustness of this finding. Thus, three groups of rats were trained in a “+”-shaped maze in which either spatial location, response-generated cues (left or right turn), or a maze insert was relevant while the other cues were irrelevant. Is short-term incidental memory that we observed in DMTS water-escape also evidenced in a food-reinforced, two-choice discrimination where there are two irrelevant cue dimensions? 3.1. Method Fig. 1. Mean of median latency ratios of rats on the nine test runs for which they made correct choices while attaining criterion in Experiment 1 (Graham et al., 1998; Means et al., 1996). Incorrect choice trials were omitted. Latency ratios are presented for the place-learning rats (Group P, left), the brightness-learning rats (Group B, middle), and for both groups combined (right). Brackets indicate the standard errors of the means. The broken line corresponds to a latency ratio expected if animals were equally fast when irrelevant cues present during test phases were the same as or different from those present during the information phase.
For Group P (Graham et al., 1998), 5 of the 10 rats had median latency ratios less than 1 (M = 0.931, S.E.M. = 0.139). The mean latency ratio, however, was not significantly less than 1, t(9) < 1.0. It is likely that this failure to find a statistically significant difference for this group was due to the small sample size and insufficient power (the probability of correctly rejecting the null hypothesis was only 0.17). For Group B (Graham et al., 1998; Means et al., 1997), 16 of the 18 rats had median latency ratios less than 1 (M = 0.811, S.E.M. = 0.083), and the mean latency ratio was significantly less than 1, t(17) = 2.263. Because the type of relevant cue encountered (place or brightness) was immaterial to the determination of whether or not the rats demonstrated implicit memory for irrelevant cues, the data were also collapsed across the two groups. When data from all 28 rats were examined (M = 0.854, S.E.M. = 0.072), mean latency ratios were significantly below 1, t(27) = 2.013. Clearly, response latencies on the DMTS water-escape problems were affected by the irrelevant cues even though rats were using relevant cues to make accurate responses.
3.1.1. Participants Thirty male Sprague–Dawley rats weighing approximately 225 g at the beginning of the study were used as subjects. They were housed individually in plastic cages in a room maintained at 23±2 ◦ C with a 12/12-h light/dark cycle with lights turned on at 07:00 h. The rats had water available continuously and were given lab chow to maintain them at their 85% ad lib weight, which was increased by 5 g each week. 3.1.2. Apparatus A gray, elevated (90 cm above the floor) T-maze was used for all behavioral testing. The stem and both goal arms were 9.5 cm wide. The stem was 37 cm long and the goal arms were each 50 cm long. The entire maze had a 2 cm high border. A circular 1 cm deep food well was located at the end of each goal arm. An insert was placed in the appropriate goal arm for each trial. The insert was white, 36-cm long and 9.5-cm wide, and had three 2-cm high hurdles. The floor of the insert was covered with 7-cm hardware cloth. The maze was placed in a room providing many extramaze cues including a table, large stimulus cards mounted on two walls, and a wall-mounted air conditioner. 3.1.3. Procedure The rats were given 4 days of maze adaptation during which nine Cocoa Puffs® (General Mills Sales, Inc.) were distributed on the maze, including one in each of the two food wells. All adaptation and subsequent training sessions began at 09:00 h, which was 2 h after the lights were turned on. During each adaptation session, a rat was released at the starting
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Fig. 2. Examples of maze arrangements during two consecutive trials in Experiment 2. The Ss indicate starting locations, shaded rectangles indicate maze insert placements, and circles indicate reinforcement placements. For each example, the relationship between the relevant cue and the reinforcement is identical for the study and test phases whereas the relationships among the irrelevant cues and the reinforcement are opposite for the two trials.
position of the stem and allowed to explore the maze for 5 m or until it had eaten all the Cocoa Puffs. Upon completion of adaptation, 10 rats were randomly assigned to each of three explicit discrimination groups: Group P, turn learning (Group T), and visual–tactile insert learning (Group V). The two maze arrangements for each of the groups are shown in Fig. 2. Rats in Group P had to go to the same physical location in the room to obtain reinforcement. The location of the visual–tactile maze insert or the turn required, which were changed on a semi-random schedule, were irrelevant. Rats in Group T had to make the same right or left turn at the choice point to attain the reinforcement. The location of the maze insert and the physical location of the reinforcement were irrelevant. Rats in Group V had to always enter either the arm with the visual–tactile insert or the arm without the insert to obtain food. Turn and place were irrelevant. Thus, all three types of choice cues were available for each of the discrimination groups, but only one type was relevant with respect to the location of the reinforcement. The two irrelevant cues were always present to potentially influence the rats’ behavior. On a semi-random half of the trials both of
the irrelevant cues were arranged the same as on the preceding trial, whereas on the other half both of the irrelevant cues were arranged opposite as the preceding trial. No trial involved one irrelevant cue being the same and one being opposite as on the preceding trial. Each rat was given eight trials per day 5 days per week for 12 days, for a total of 96 trials. The rats were tested in squads of five and had inter-trial intervals of approximately 5 m. Each trial consisted of placing the rat in the start box such that it faced directly away from the choice point. The rat was then permitted to make a choice, when a barrier was placed behind the rat to prevent retracing or a second choice. All correct choices were reinforced with two Cocoa Puffs placed in the appropriate food well. A stopwatch was used to measure response latencies. The stopwatch was always terminated when the rat made a choice, entire body, excluding the tail, in a goal arm. During the first block of 24 trials the timer was activated at the time the rat was released. Because of considerable variability in the time it took rats to orient to the choice point, the timer was not activated until the rat oriented to the choice point for the last three blocks of 24 trials. The rat was left on the goal arm while the choice and response latency were being recorded. Following each daily session the rats were weighed and fed their appropriate ration. 3.2. Results 3.2.1. Acquisition Nearly all rats acquired their respective explicit discrimination problems and the groups did not differ significantly. Fig. 3 shows the mean percent correct choices made by each of the three groups over the four blocks of trials. A Group × Block mixed-factors ANOVA on the percent correct choices resulted in only a significant Block effect, F(3, 81) = 44.6, P = 0.000. Post hoc Fisher’s least squares tests revealed that performance on Block 1 differed from performance on Block 2 which differed from Block 3 (P < 0.05 in each case). Blocks 3 and 4 did not differ from one another. 3.2.2. Irrelevant cues One rat in Group T and two rats in each of the other two groups failed to achieve 90% correct choices over the last two blocks of 24 trials and, therefore, their data
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Fig. 3. Mean percentage correct choices made by animals in Experiment 2 while explicitly learning about the relevant cues.
were not included in the analysis of the influence of the irrelevant cues. Following the procedure described above, a median latency ratio (same/opposite) was determined for each of the remaining subjects based on the last two blocks of trials. Only correct choice trial latencies were used to determine the ratios. Recall that a latency ratio <1.0 indicates that rats made correct choices faster on trials where the irrelevant stimuli were the same as opposed to opposite as the immediately preceding trial. Fig. 4 shows means of median latency ratios for all three groups. For Group P (M = 0.923, S.E.M. = 0.050), Group T (M = 0.938, S.E.M. = 0.040), and Group V (M = 0.919, S.E.M. = 0.033), six of the eight rats, six of nine rats, and eight of eight rats had latency ratios less than 1, respectively. Latency ratios were not significantly different from 1 for Group P (t(7) = 1.537) or Group T (t(8) = 1.531), but these tests were associated with rather low power (the probability of correctly rejecting the null hypothesis was 0.33 in both cases). By contrast, for Group V (power = 0.66), latency ratios were significantly less than 1, t(7) = 2.374. In addition, when the data from all three groups were combined, latency ratios were significantly less than 1, t(25) = 3.128. This final outcome was considered the most revealing because examination of short-term incidental memory for irrelevant cues was not expected to depend upon the type of relevant cue associated with a particular group. Clearly, most rats in all three discrimination groups had shorter response latencies on trials where
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Fig. 4. Mean of median latency ratios of rats on the last 48 trials during which animals were making at least 90% correct choices in Experiment 2. Incorrect choices were omitted. Latency ratios for the place-learning rats (Group P, far left), for the turn-learning rats (Group T, middle left), for the visual–tactile-learning rats (Group V, middle right), and for all three groups (far right) are presented. Brackets indicate the standard errors of the means. The broken line corresponds to a latency ratio expected if animals were equally fast when the relationship between the response and an irrelevant cue were the same or different on consecutive trials.
the irrelevant cue values were the same as on the immediately preceding trial. In contrast, rats did not make more correct responses on “same” trials (M = 97.038, S.E.M. = 1.622) than on “different” trials (M = 98.538, S.E.M. = 0.506), t(25) < 1.0.
4. General discussion Rats demonstrated short-term incidental memory for irrelevant cues in both the DMTS water-escape paradigm and the two-choice food-reinforced discrimination paradigm. The former task requires memory for trial-dependent cue values, sometimes called working memory (Honig, 1978; Olton et al., 1979), whereas the later task requires memory only for a given cue value independent of trial, referred to as reference memory (Honig, 1978). Response latencies to relevant cues were shorter when an irrelevant cue shared the same relationship to the response that it did during the preceding response compared to when the relationship between the irrelevant cue and the response had changed. Because rats exhibited short-term incidental memory in two types of tasks differing in number of irrelevant cue dimensions, reinforcement,
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and mnemonic requirements, it appears that the phenomenon is quite robust. A similar finding has recently been reported (Kesner, 1998). He used a between-subjects design to examine explicit and what he termed implicit learning in rats. All animals were trained with a sequence of 12 forced responses in a 12-arm radial maze. Three or four of the responses involved a repeated response (i.e. a second visit to a maze location). In the explicit learning group, reinforcement was available only on the first visit to a particular maze location. Thus, the relationship between the location cues and the availability of reinforcement “instructed” rats to remember which locations they had visited previously. In the implicit learning group, reinforcement was available on all visits to maze locations. For these rats, the relationship between location cues and the availability of reinforcement was irrelevant and, therefore, memory for location was incidental. Thus, the learning situation (i.e. the relationship between environmental cues and the availability of reinforcement) was used to manipulate the instructional set that the animals received. Intentional explicit memory for location was indicated by longer maze-running latencies for repeated locations compared to latencies for nonrepeated locations. In contrast, the implicit group showed implicit memory for location as indicated by shorter maze-running latencies for repeated locations compared to nonrepeated locations. Clearly, the phenomenon Kesner called implicit memory is very similar to what we are calling short-term incidental memory. The present demonstrations of short-term incidental memory do not permit one to know the underlying mechanism. The experimental procedures employed permit some potential explanations to be dismissed. Short-term incidental memory is not due to iconic or sensory memory (Sperling, 1960), as the 5-min retention interval far exceeds the demonstrated duration of sensory memory. In addition, it is not due to differential reinforcement of the irrelevant cue values as all irrelevant cue values are reinforced on 50% of the trials. To some extent, our demonstrations of short-term incidental memory resemble findings from studies of matching-to-sample (MTS) performance of pigeons. The observation that pigeons select correct element choices more often when responding to element samples (line orientation or color) compared to when they are responding to compound samples (line orienta-
tion and color) is called the element superiority effect (e.g. Cook et al., 1992; Lamb, 1988; Maki and Leith, 1973). One way of accounting for the element superiority effect is via the generalization decrement hypothesis (e.g. Brown and Morrison, 1990; Grant and MacDonald, 1986; Langley and Riley, 1993; Roberts and Grant, 1978; Santi et al., 1982). According to this view, “control by compound samples is reduced due to the lack of an exactly matching comparison stimulus” (Maki et al., 1976). In our Experiment 1, MTS performance benefited when samples exactly matched correct choices. In the discrimination experiment (Experiment 2), a similar advantage for exact matches was also exhibited. This discrimination advantage is analogous to the MTS advantage if one views each discrimination trial as equivalent to a sample and one views each subsequent discrimination trial as equivalent to a matching test. Thus, in both experiments, one might interpret the reported advantages according to a generalization decrement account. Unlike reports of the element superiority effect, however, the performance advantage was not related to greater accuracy, but rather faster responding. The fact that our “same” trial advantage applies to response latencies but not to response accuracy is a primary reason for characterizing the advantage as an incidental rather than intentional memory phenomenon. As pointed out above, the intent of an animal subject must be inferred from the contingencies to which it is responding. In the present experiments the rats were reinforced with either food or water-escape for going to a particular stimulus value. Because all latency scores included in the analyses were based on correct choice trials made when the animals were performing at a 90% correct choice level, it can be assumed that the intent of the rat was to enter the choice arm or section containing the relevant cue, i.e. the cue that had been associated with reinforcement on every prior approach to that cue. This being the case, any change in response associated with the irrelevant cues must have been incidental. The incidental influence of irrelevant cues on response latencies of rats is similar to priming observed in humans (Schacter et al., 1993) and, perhaps, animals (Blough, 1991; Langley et al., 1996). Priming is enhanced stimulus processing resulting from prior exposure to the stimulus or exposure to a similar or
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related stimulus. For example, people identify strings of letters as words more quickly when the word presentations are repeated (Just and Carpenter, 1980). It is thought that the initial presentation of a word activates a mental representation of the word. This activation persists and thereby allows one to respond to the same word more quickly when it is encountered again. In the studies we described, the irrelevant cues can be viewed as priming events. When the properties of these priming events match those present during a subsequent test trial, a type of repetition priming occurs. That is, the rats’ performance is enhanced as a result of prior exposure to these cues. Because the priming cues are irrelevant, however, their influence might best be described as contextual priming. Priming is considered a form of implicit (nondeclarative) memory for three reasons. First, the priming events can enhance performance even when primes are presented below the threshold of conscious identification (Marcel, 1983). Second, priming-based enhancement is noted when the priming events can no longer be consciously recalled (Tulving et al., 1982). Third, priming effects are entirely normal in amnesic patients whose declarative memory is impaired due to damage to medial temporal lobe memory structures (Hamann and Squire, 1997). Because short-term memory shares many properties with priming, a form of implicit memory, and because the intention of a rat cannot be known beyond what is determined by the reinforcement contingencies to which it is responding, short-term incidental memory may be viewed as an analog for the study of implicit memory in nonhuman subjects. Studies of human amnesia indicate that conscious recollection does not always accompany normal memory-based task performance (Hamann and Squire, 1997). Amnesic patients with damage to the medial temporal lobe or midline diencephalon exhibit impairments on recall and recognition tests that require conscious recollection. The same patients, by contrast, exhibit normal priming and other memory-based abilities that do not depend upon conscious recollection. It has been suggested, therefore, that the brain structures damaged in amnesic patients support explicit memory but that different brain areas support implicit memory. Thus, these studies link the phenomalogically different memory forms to anatomically distinct
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neural substrates. An obvious test of our supposition that short-term incidental memory is an infrahuman analog of human priming or implicit learning, is to test in animals with a compromised medial temporal lobe whether short-term incidental memory is preserved on a task where the explicit memory is impaired.
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