Spontaneously hypertensive rats (SHR) readily learn to vary but not repeat instrumental responses

BEHAVIORALAND NEURALBIOLOGY59, 126--135 (1993)

Spontaneously Hypertensive Rats (SHR) Readily Learn to Vary but Not Repeat InstrumentalResponses DEBORAH M.

MOOK,JOHN

JEFFREY, AND ALLEN NEURINGER1

Department of Psychology, Reed College, Portland, Oregon 97202

field environments more vigorously, and their movements are more variable than WKYs (Cierpial, Shasby, Murphy, Borom, Stewart, Swithers, & McCarty, 1989; Gentsch, Lichtsteiner, & Feer, 1987; Knardahl & Sagvolden, 1979; Moser, Moser, Wultz, & Sagvolden, 1988; van den Buuse & de Jong, 1989; Wultz et al., 1990). Possibly related to these findings, the SHRs are also more likely to approach novel objects (Danysz, Plaznik, Pucilowski, Plewako, Obersztyn & Kostowski, 1983; Delini-Stula & Hunn, 1985; Knardahl & Sagvolden, 1979; Rogers, Sink, & Hambly, 1988). This hyperactivity of SHRs is not necessarily correlated with their high blood pressure (Svensson, Harthon, & Linder, 1991); some substrains show hypertension o r hyperactivity, not both (Hendley & Ohlsson, 1991). Second, SHRs take longer to learn some tasks than WKYs and learn to lower levels of proficiency (Low, Whitehorn, & Hendley, 1984; Nomura, 1988). Both high levels of activity and learning disabilities have been reported for children diagnosed with ADDH (Bierderman, Newcorn, & Sprich, 1991; Rapport, Quinn, DuPaul, Quinn, & Kelley, 1989). SHRs do not always show learning deficits, however. For example, SHRs more readily learn to avoid or escape from aversive stimuli than WKYs (Danysz et al., 1983; Knardahl, 1986). This finding may partly be accounted for by the fact that aversive stimuli elicit different responses in the two strains-WKYs tend to freeze and SHRs tend to move (Berger & Starzec, 1988). Sensitivity to painful stimulation may also differ in the two strains (Maixner, Touw, Brody, Gebhart, & Long, 1982; see, however, Huang & Shyu, 1987). But even under some positive reinforcing conditions, SHRs learn more rapidly than WKYs, e.g., in the Hebb-William's maze (Rogers et al., 1988). Thus, a general "learning deficit" does not appear to characterize SHR performance. Low et al. (1984) may help to explain why SHRs

When spontaneously hypertensive rats (SHR) and Wystar-Kyoto normotensive control rats (WKY) were rewarded in a 12-arm radial maze (Experiment 1), the SHRs varied their arm choices more, making fewer repetition errors than the WKYs. Similarly when rewards depended on variable sequences of responses on two levers in an operant chamber (Experiment 2), SHRs' sequences were more variable than those of WKYs. A requirement for response variability was then combined with a requirement to repeat selected responses in the radial maze (Experiment 3) and operant chamber (Experiment 4). WKYs learned to repeat more readily than the SHRs, whereas SHRs varied more readily. Thus, when subjects had to repeat responses, SHRs were at a disadvantage, but when variability was adaptive, SHRs excelled. The high variability of SHRs, together with their difficulty in learning to repeat, may have parallels in children diagnosed with attention deficit disorder with hyperactivity (ADDH). © 1993 Academic Press, Inc.

INTRODUCTION Spontaneously hypertensive rats (SHR) were first studied because of their high blood pressure (Okamoto, 1969). More recently, the SHR strain has been hypothesized to serve as an animal model of h u m a n attention deficit disorder with hyperactivity, or ADDH (Wultz, Sagvolden, Moser, & Moser, 1990). There are two main sources of support for this hypothesis. First, SHRs are more active than their normotensive Wistar-Kyoto (WKY) progenitors, typically used as controls. The SHRs explore open1 Address reprint requests to Allen Neuringer, Department of Psychology, Reed College, Portland, OR 97202. We thank Gene Olson for his care of the animals and Ralph Huntley for his advice and assistance. Experiments 1 and 3 were derived from an undergraduate senior thesis submitted to Reed College by John Jeffrey. Deborah Mook was partly supported by a National Science Foundation Research Experience for Undergraduates grant. This work was partially supported by National Science Foundation Grant BNS-8707992. 126

0163-1047/93 $5.00 Copyright © 1993 by Academic Press, Inc. All rights of reproduction in any form reserved.

VARIATION AND SELECTION IN SHR AND WKY sometimes perform less successfully than WKYs, while in other situations they are more successful. When reinforcement depended on rats learning to go to the left arm of a T-maze, WKYs were more proficient than SHRs; but when reinforcement depended upon the rats varying their choices, SHRs excelled. In other words, the strain of rats interacted with reinforcement contingencies in determining whether SHRs showed a learning deficit or a learning advantage. The present four experiments attempted to test the generality of these potentially important findings. In the first two experiments, SHR and WKY rats were rewarded for varying their behaviors. In Experiment 1, a 12-arm radial maze was employed where rats had to learn to enter each arm only once per session (Olton & Samuelson, 1976). Thus, response variations were required for reinforcement, and we hypothesized that SHRs would make fewer errors than WKYs. Experiment 2 employed a quite different task involving key presses in an operant chamber. Here variations in sequences of operant responses were required for reinforcement. We again hypothesized that SHRs should perform this task with fewer errors than the WKYs. Experiments 3 and 4 combined a requirement for variability with a requirement to repeat only a subset of arms in the maze or subset of response sequences. For example, in Experiment 3, only four of the arms of the maze contained food pellets, the same four arms each day. Thus, the rats had to learn to go to a subset of arms but not repeat any one of these arms. Experiment 4 required analogous performances in the operant chamber. If WKYs more readily repeat and SHRs vary, Experiments 3 and 4 should show that WKYs are more likely to select the correct subset, but that SHRs are more likely to vary when in the subset. GENERAL M E T H O D

Subjects.

Nine male spontaneously hypertensive rats and nine male Wistar-Kyotos, obtained from the Charles Rivers Laboratories Inc. (Wilmington, MA), were 210 days old at the beginning of the experiment. They were housed two or three to a cage (40.5 × 24 × 19 cm) under a 12-h light/dark cycle, and maintained on a 22-h food deprivation schedule, with water freely available except during the experimental hour. The same subjects were used in all four experiments.

Apparatus. Two apparatuses were used. The first, a 12-arm aluminum radial maze used in Experiments 1 and 3, consisted of a 65-cm-diameter

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central arena with 12 radiating arms, 84.5 cm long x 10 cm wide × 15.5 cm high (Olton & Samuelson, 1976). Each arm contained a photocell sensor midw a y down the arm to record entries, with data automatically transmitted to an Apple Macintosh computer. An error routine assured that only one response was recorded per entry. Black plastic jar lids, 6 x 1 cm, located at the distal end of each arm, served as food receptacles. The maze was placed in a dimly lighted laboratory room, with a 15-W incandescent bulb 130 cm directly over the center of the maze; the room contained a variety of distinct spatial cues, including a cabinet, TV monitor, and partitions. Experiments 2 and 4 used nine identical modified Gerbrands operant chambers, 27 cm deep, 28 cm long, and 30 cm high. The chambers had ceiling, back wall, and front wall made of clear Plexiglas, two side walls made of aluminum, and the floor made of wire bars 1 cm apart. One side wall contained three pigeon response keys, 3 cm in diameter, 17.5 cm from the ceiling, and 9.5 cm from the floor. The keys were 9 cm apart, center to center, and could be transilluminated by white 24-V bulbs. Only the right and middle keys were used in the present research. An audio speaker was located behind the wall containing the keys. On the wall opposite the keys were two response levers, not used during this experiment, and a pellet tray, centered between the levers and 3 cm from the floor, into which 45-mg Noyes pellets were released as reinforcers. Each chamber was housed in a sound- and light-attenuating outer cubicle and connected to an Apple Macintosh computer through a Metaresearch Benchtop interface. EXPERIMENT 1: RADIAL-ARM MAZE

Me~od Procedure. Each subject was trained to obtain a 45-mg Noyes rat chow pellet from the end of each alley by progressively moving pellets down each arm until the pellets were available only in the food cups, a shaping procedure accomplished over the course of 10 sessions. The experimental procedure followed. At the beginning of a session, the subject was gently placed in the central arena of the maze facing in a random direction. There was one food pellet in each of the 12 food cups. The subject remained in the maze until each of the 12 arms had been visited at least once, i.e., until all 12 pellets had been eaten, or 10 min had elapsed. The order and time of entry into each arm were automatically

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recorded and stored for analysis. The maze was cleaned with deodorizer after each session. One session was given per day, 5 to 7 days per week. Thirty experimental sessions were provided.

Data analyses. Percent Vary, the main measure, was calculated by dividing the number of reinforced arm entries by the total number of arm entries, multiplied by 100. Thus, for example, if each arm were entered exactly once, Percent Vary would equal 100% ((12/12).100); and if 6 arms had been entered once and 6 arms entered twice, i.e., 6 repetition errors, then Percent Vary would equal 67% ([12/18].100). Percent Vary equaled the percentage of reinforced responses and thus was an index of proficiency of performance. An index of response speed was also examined, namely intertrial interval (ITI), or the times between arm choices. The median ITI value from each session was used in this analysis. Results and Discussion Figure 1 shows group average Percent Vary across the 30 sessions. A 2 x 30 (strain × sessions) analysis of variance (ANOVA) showed that SHRs responded more variably than WKYs (F(1, 16) = 4.540, p < .05), and that both strains improved across sessions (F(29, 464) = 6.077, p < .001). The interaction was not significant. WKYs responded slowly at first, often freezing in place; this finding is consistent with the neophobic responses previously reported for WKYs (e.g., Danysz et al., 1983; Knardahl & Sagvolden, 1979; Delini-Stula & Hunn, 1985). Over the course of the

experiment, however, the WKYs came to emit arm choices more rapidly than the SHRs. A 2 × 30 ANOVA showed a significant strain x session interaction (F(29, 464) = 3.406, p < .001), with SHRs responding faster initially, but WKYs more rapidly than SHRs over the final sessions. The radial arm maze task requires response variation for reinforcement: if entry into a given arm is repeated during a session, the subject is not rewarded. The main finding was that SHRs performed this task with higher accuracy than WKYs. These results are consistent with the Low et al. (1984) findings that SHRs readily vary their responses in a T-maze. In both Low et al. (1984) and the present case, the propensity of SHRs to vary was present from the outset. EXPERIMENT 2: OPERANT VARIABILITY The next experiment further tested the generality of the Experiment i findings: Are SHRs more readily reinforced than WKYs for emitting variable instrumental responses in an operant-conditioning chamber? In addition, we attempted to determine whether SHRs are more sensitive than WKYs to changes in contingencies regarding variability. An operant chamber was used to reinforce variable sequences of left and right responses. A trial consisted of four (L)eft and (R)ight key presses. If the sequence in the current trial differed from those in the previous four trials, then a food pellet was provided. On the other hand, if the current sequence repeated any of the previous four, then it was followed by a brief time-out. For example, assume that in the four previous trials a rat had emitted the sequences RRRL, RLLR, LLRR, and LRLR. If the current trial contained the sequence LLLR, a sequence which differed from each of the previous four, then the trial ended with presentation of a food pellet. On the other hand, if the current sequence had been LLRR, a repetition of one of the previous four, then a brief time-out period ensued and reinforcement was withheld. This procedure reinforces sequence variability (see Machado, 1989; Morgan & Neuringer, 1991; Neuringer, 1991; Neuringer & Huntley, 1992; Page & Neuringer, 1985). To test whether SHRs are more sensitive than WKYs to reinforcement of variations or whether, alternatively, the SHRs behave more variably independently of the reinforcement contingencies, we employed a second phase. In this "yoke" phase, reinforcement was provided independently of the subject's variability, thereby permitting, but not requiring, sequence variations. During yoke, each

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animal's pattern of reinforced and nonreinforced trials was yoked to his own previous performance in the initial "variability" phase of the experiment, with reinforcement frequencies during this yoke phase therefore identical to those in the initial phase (Neuringer & Huntley, 1992). Following yoke, the original variability contingencies were reinstated, thereby constituting an ABA design in which sequence variability was required for reinforcement in A and permitted (but not required) in B. The two main questions were (i) whether SHRs would respond more variably than WKYs under an operant sequence task and (ii) whether the two groups were differentially sensitive to variability-demanding contingencies of reinforcement. Method Procedure. The rats were autoshaped to press each of the two keys for food pellets, and then were placed on a fixed ratio (FR) schedule of reinforcement, the value of the ratio increasing to FR4 over the course of four sessions. Four responses summed across the keys were required for reinforcement. The variability schedule was then introduced, under which four presses on left and right keys constituted a trial. The sequence of L's and R's in the current trial had to differ from those in each of the previous four trials for reinforcement, a lag 4 variability contingency (Page & Neuringer, 1985). Under this contingency, the rats had to vary sequences of responses rather than arm entries.

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When the lag 4 variability contingency was met, a food pellet was presented, accompanied by a 1-s end-of-trial cue, which consisted of the darkening of the chamber and a 1000- to 200-H warbling tone. If the current sequence repeated any of the previous four sequences, a 3-s time-out occurred, consisting of the same dark chamber but with no tone and no reinforcer. After time-out or reinforcement, the two keys were reilluminated and a new trial began. Sessions terminated after 200 trials or 1 h, whichever occurred first. Twenty sessions were provided during this A phase, with the basic question being whether SHRs would behave more variably than WKYs. During the B phase, reinforcers were provided independently of sequence variability (Morgan & Neuringer, 1991; Neuringer & Huntley, 1992; Page & Neuringer, 1985). As is described below, subjects participated in Experiments 3 and 4 prior to this B phase, and therefore five additional sessions under variability lag 4 contingencies were provided (A'). Reinforcements and time-outs were then "yoked" to these five sessions of continued variability training. During the first yoke session, each rat was yoked to its own fifth (most recent) session of variability. During the second session, animals were yoked to the fourth session of variability, and so on. During the sixth yoke session, animals were again yoked to the last variability session. This yoking cycle was repeated 3 times, creating 15 yoke sessions. During a yoke session, each trial was followed by the same outcome (time-out or reward) that the subject had experienced during the equivalent trial in the variability session. For example, if a given subject had been rewarded after its 12th trial in the variability session, the subject was rewarded after the 12th trial during the associated yoke session regardless of whether or not the sequence in that trial differed from the previous four sequences. Thus, the subject received the same number and pattern of rewards and time-outs as during the variability phase, but without variability being required. Under this procedure subjects served as their own controls. Immediately following this yoke phase there was a return for 20 additional sessions to the variability, lag 4 contingencies identical to the initial A phase. The first A phase of this experiment followed immediately after Experiment 3, reported below, and phases B and the return to phase A after Experiment 4. This order was employed so that all of the radial-maze studies occurred in one block and all of the operant studies in a second block, and that radial-maze and operant studies paralleled one another. Thus, the order of presentation was Experiment 1; Experiment 3; Experiment 2, phase A;

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Experiment 4; Experiment 2, phases B and return to A. The exposition departs from this order for reasons of clarity of presentation.

Data analysis. Percent Vary was again the main measure and was calculated as follows: the number of sequences in a session that differed from each of the previous 4 sequences was divided by the total number of sequences (or trials) in the session and the result was multiplied by 100 to obtain a percentage. During the variability (A) phases, Percent Vary equaled the percentage of reinforced trials. During the yoke (B) phase, Percent Vary equaled the percentage of trials that would have been reinforced if the lag 4 contingencies had been in place. ITI was defined as the median time between trials in a session. Repeated equipment failure in one of the operant chambers caused us to remove two of the subjects (one SHR and one WKY) from the data analysis. Results and Discussion Figure 2 shows the mean Percent Vary for both groups under each of the phases. To simplify statistical analysis, we calculated an average of each subject's performance during the last five sessions in each of the three main phases, and these averages were used in a 2 x 3 ANOVA (strain x phase). Because the variability phase just prior to yoke (A') contained only five sessions, it was excluded from this statistical analysis, an exclusion which does not influence the main findings. SHRs showed an overall higher level of variation than WKYs (F(1, 14) = 10.813, p < .01). The contingencies also exerted a significant effect (F(2, 28) = 78.076, p < .001), with both strains showing lower levels of variation in the yoke condition (B) than those under the varaability conditions (A). There was also a significant strain x phase interaction (F(2, 28) = 9.175, p < .001). Simple effects analyses showed no strain difference in the first variability phase, whereas SHRs behaved more variably than WKYs during yoke (F(1, 14) = 11.498, p < 0.01) and during the final variability phase (F(1, 14) = 4.914, p < .05). We also compared decreases in variability during the yoke phase (B) relative to the variability phases (A). Average performances (over the last five sessions) during the yoke phase were subtracted from an overall average of the two variability phases (the last five sessions in each case) for each group of animals, w h e n reinforcement no longer depended on sequence variability in the yoke phase, WKY's level of variability decreased more than did SHR's (t(14) = 3.25, p < .01).

The results of the yoke (B) phase show that SHRs' level of response variability is high even when the reinforcement contingencies do not demand variability. The elevation is also evident in the A' phase preceding, and the A phase following yoke. The two groups did not, however, differ significantly when they initially experienced the variability contingencies (initial A). Whether the latter is a robust finding must be explored in future work. A comparison between experimental (A) and yoke (B) phases shows that both strains responded significantly more variably when variations were required than when not. As was the case at the end of Experiment 1, WKYs responded more rapidly than SHRs. WKY's ITIs were significantly shorter than SHR's over the last five sessions of each of the three phases (F(1, 16) = 208.521, p < .001). Thus, although the SHR's may be generally more active than WKYs (see Introduction), by the end of Experiment 1 and throughout the present experiment, the SHRs were less likely to perform "on task," i.e., to emit responses which could engender reinforcement. The basic findings were as follows. (a) When high levels of response variability were required for reinforcement, both SHRs and WKYs increased variability or maintained it a high level. In other words, both groups were affected by contingencies that required variability. (b) When reinforcement was provided independently of response variations, SHRs responded more variably than WKYs. This confirms and extends the Low et al. (1984) findings that SHRs have a higher baseline level of variability than do WKYs. (c) The WKY's variability changed more as a function of contingencies than the SHR's. Thus, although SHRs "naturally" behave more variably, WKYs are more sensitive to the contingencies. These two factors combined "natural," or baseline, levels of variability and sensitivity to contingencies--appear to exert important influence on performances by these two strains. EXPERIMENT 3: SELECTION AND VARIATION IN THE 12-ARM RADIAL MAZE We hypothesize that strain and contingencies interact to determine important behavioral differences between SHR and WKY. In particular, because of a high baseline tendency to vary, SHRs may perform more successfully when behavioral variability is reinforced, whereas WKYs may be more successful when particular responses must be repeated for reinforcement. The next experiment tested this hypothesis by requiring both repetition

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and variation for reinforcement. Entries into only a subset of four adjacent alleys of the radial maze could be reinforced but, within that subset, repetitions were never reinforced. Thus, subjects had to learn always to select members of the given subset but not to repeat any given response.

.Method Procedure. Four adjacent arms of the radial :maze were baited during each session, these four being the same throughout the experiment. The remaining eight arms were always empty. Each of the four baited arms contained three 45-mg Noyes pellets, thus keeping the total number of pellets that could be obtained per session the same as in Experiment 1. In all other respects, the procedure was identical to Experiment 1 with 15 sessions provided, each session terminating when all pellets had been eaten. Data analyses. The two dependent measures were Percent Selection and Percent Vary within the subset. Percent Selection was calculated by dividing number of entries into the "correct" subset of arms by the total number of arm entries multiplied by 100. The numerator included both reinforced and nonreinforced (or repeated) arm entries into the correct subset. Percent Vary within the subset was calculated by dividing the number of reinforced arm entries by total number of entries into the correct subset multiplied by 100. Thus, a high value for Percent Selection indicated that the rat learned to run to the four potentially reinforced arms and to avoid entering the other eight arms; a high value for Percent Vary indicated that the rat tended not to reenter a previously reinforced arm within the selected subset. Results and Discussion Figure 3, top, shows Percent Selection of the subset by both groups across the 15 sessions of the experiment. A 2 x 15 (strain x sessions) ANOVA showed that the WKYs were more likely to select the correct subset (F(1, 16) = 10.808, p < .01), and that both groups improved across sessions (F(14, 224) = 15.729, p < .001). A significant strain x session interaction (F(14, 224) = 2.402, p < .01) indicated that the difference between the two strains increased across sessions. Thus, WKYs learned more rapidly and to a higher level than SHRs to select members of the correct subset of arlTlS.

Figure 3, bottom, shows the Percent Vary data,

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i.e., percentage of choices within the correct subset which differed from previous choices. The SHRs were more likely to vary than the WKYs (F(1, 16) = 21.856, p < .001), with neither session nor interaction effects being significant. Thus both hypotheses were supported. Once again, SHRs' level of variability remained consistently above that of the WKYs, indicating a "general" elevation of variability. However, the WKYs better learned to select a correct subset of arms than did the SHRs. As in the previous two experiments, the WKYs responded more rapidly--they were more frequently on task than the SHRs, the difference between strains being significant (F(1, 16) = 10.485, p <.01). EXPERIMENT 4: SELECTION AND VARIATION IN THE OPERANT TASK Experiment 4 paralleled Experiment 3 in that the rats now had to select from among 4 of 16 possible operant sequences but, analogous to Experiment 3, they could not repeat the just-emitted sequence, i.e.,

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Method Procedure. The procedure was essentially the same as the variability phases in Experiment 2 except that only sequences RRRR, RRRL, RRLR, and RRLL could be reinforced. These are sequences 0 through 3. A sequence in this subset was reinforced only if it differed from the previous sequence (whether that previous sequence was from within or without the correct subset). Thus, a lag 1 variability contingency was in effect (rather t h a n the tag 4 contingency in Experiment 2). Fifteen sessions were provided. Data analysis. Percent Selection was defined as number of trials in which a member of the subset was emitted divided by total trials multiplied by 100. Percent Vary was defined as number of reinforced trials divided by total number of within-subset trials multipled by 100. A high Percent Vary would be obtained if relatively many within-subset trials were preceded either by a different withinsubset sequence or by any other (nonsubset) sequence.

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Results and Discussion Figure 4, top, shows that the WKYs selected members of the correct subset more frequently t h a n did the SHRs (F(1, 16) = 6.912, p < .05). Performances of both groups improved across sessions (F(14, 224) = 14.440, p < .001), and the interaction was not significant. Figure 4, bottom, shows Percent Vary within the correct subset. Neither strain nor session differences were significant, but the strain × sessions interaction was (F(14, 224) = 3.940, p < .001). To further explore this interaction, averages were computed across the first three and the last three sessions, and these averages compared separately for each group. For the SHRs, variability decreased significantly across sessions (F(1, 8) = 6.448, p < .05), whereas for the WKYs, variability increased (F(1, 8) = 12.036, p < .01). As in Experiment 3, WKYs were significantly more likely to select members of the potentially reinforced subset. However, whereas the WKY's acquisition curve was steeper than the SHR's in Experiment 3--the interaction between strain and ses-

sions was significant--acquisition curves were equally steep in the current experiment. Future research should explore reasons for this difference between the two experiments. Note that the particular sequences in the potentially reinforced subset-RRRR, RRRL, RRLR, and RRLL--required relatively few alterations, this possibly contributing to the constant advantage demonstrated by the WKYs. Also as in Experiment 3, the SHRs varied their within-subset responses more than did the WKYs during the initial sessions. However, by the end of the experiment, this effect had reversed, with the WKYs varying more than the SHRs. This reversal may partly be due to the fact t h a t a relatively "easy" lag 1 variability contingency was employed which permitted subjects to alternate between any two sequences, a repetition strategy at which WKYs excel. Further analyses showed that WKYs had, in fact, learned with relatively high probability to alternate between two sequences, generally sequences 0 (RRRR) and 3 (RRLL) or 0 and 1 (RRRL). For example, one WKY subject emitted a 0 sequence fol-

VARIATIONAND SELECTIONIN SHR AND WKY lowed by a 3 sequence during 23% of trials over the ]Last 3 sessions, and 3 followed by 0 during another 23%. To give a sense of this performance, here are that subject's final 50 sequences in the experiment: 303030310073030703030303031030303106063030133030306. Eight of the 9 WKYs showed alternation ,patterns during more than 20% of the trials (sum of sequence a followed by sequence b, and b followed by a), whereas only 1 of 9 SHRs attained this level. Thus, one reason that WKYs appeared to be more ~'variable" than SHRs by the end of this experiment was that the lag 1 "variability" contingency could be met by repeatedly alternating between 2 sequences. Finally, as in the previous 3 experiments, WKYs responded "on task" more frequently than did the SHRs, the difference in ITIs being significant (F(1, 16) = 5.480, p < .05). GENERAL DISCUSSION We tested the hypothesis that SHRs are more readily reinforced for varying their responses than WKYs, whereas WKYs are more readily reinforced for selectively repeating responses or patterns. The results generally supported this hypothesis, originally suggested by Low et al. (1984). SHRs made fewer errors than WKYs in a 12-arm radial maze (Experiment 1) as well as in an operant task where variable response sequences were reinforced (Experiment 2). Both of these cases required behavioral variability for reinforcement. SHRs also responded more variably under operant baseline conditions, where rewards were presented independently of response variability. Two additional experiments required that subjects select a subset of arms in the radial maze (Experiment 3), or subset of sequences in the operant task (Experiment 4). Variations within the subset were again required, and therefore two questions could be asked concurrently: (a) can WKYs learn to select members of a potentially reinforced subset of responses more frequently than SHRs and (b) will the SHRs vary their responses within the subset more than the WKYs? The answer in Experiment 3 was "yes" to both of these questions: WKYs were more likely than SHRs to select members of the subset whereas SHRs were more likely to vary their choices within the subset. Experiment 4 replicated the "selection" result in the operant chamber: WKYs were more likely to select the 4 correct (out of a possible 16) sequences. As in Experiment 3, the SHRs were also more likely to meet the variability criterion than the WKYs during the initial sessions. However, by the end of the experiment, this effect

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had reversed, with the WKYs varying more than the SHRs. This reversal may partly be due to the fact that the lag 1 variability contingency permitted subjects to alternate between any two sequences, a repetition strategy at which WKYs excelled. Both strains increased their variability across sessions in the radial-arm maze, a situation where variability is required; both responded variably in the operant chamber when reinforcement depended upon variability; and both responded at much lower levels of variability when it was not required. Thus, both strains were sensitive to reinforcement of variability. However, as indicated above, SHRs generally behaved more variably than the WKYs in these two quite different situations. This difference appears to be due to a generally high baseline, or "natural," level of variability in SHRs. Both strains were also sensitive to reinforcement of selected responses, increasing their choices of the reinforced subset of arms in the radial maze and the reinforced subset of sequences in the operant chamber. However, the WKYs were more likely to repeat these reinforced selections than the SHRs. In brief, while both SHRs and WKYs could successfully be reinforced for varying or repeating, SHRs were more likely to vary and WKYs to repeat. Lastly, at the beginning of Experiment 1, WKYs responded very slowly, this possibly related to a neophobic response. Future research must take transient neophobic responses into account when comparing SHRs with WKYs. Initial comparisons may not be representative of later performances. By the end of Experiment 1, and throughout all of the remaining experiments, WKYs responded consistently faster than the SHRs, both in the radial maze and in the operant chambers. Thus, although many studies have shown that SHRs are more "active" than WKYs, this activity does not translate into higher rates of "on task" behaviors. Quite the contrary, the SHRs engaged in a potentially reinforced task less frequently than WKYs, this occurring whether SHRs were reinforced with higher or lower probability than the WKYs. Note that their low response rates may have contributed to the SHR's high variability (Neuringer, 1991), suggesting that one way to overcome possible "problems" caused by variability would be to train (or otherwise induce) SHRs to engage more frequently in "on task" behaviors. The potential importance of this research, together with Low et al. (1984), is that SHRs show "learning deficits" only when a specific response or set of responses must be repeated. On the other hand, when behavioral variability is rewarded, the

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SHRs may respond more successfully than WKYs. The "deficit" therefore depends upon an interaction between strain of rat and environmental contingencies. This finding may be relevant to children diagnosed with ADDH who also have been observed to behave more variably than normals (e.g., Hynd, Nieves, Connor, Stone, Town, Becker, Lahey, & Lorys, 1989). A high baseline variability in ADDH children may be analogous to the high baseline levels of variability in the SHRs, leading to a prediction that when variability is adaptive, ADDH children might excel. One way to test this hypothesis is suggested by Holman, Goetz, and Baer's (1977) research on the reinforcement of behavioral creativity in children. The present results may also help to explain apparently inconsistent results in the animal literature on this topic. For example, Rogers et al. (1988) reported that SHRs learn the Hebb-Williams maze tasks more readily than WKYs, this result apparently inconsistent with others showing superior learning by WKYs (e.g., Low et al. 1984; Nomura, 1988). The WKYs in Rogers et al. may have been exhibiting behaviors similar to those in the present studies, i.e., repeating just-reinforced responses. This tendency to repeat may be adaptive in some situations, such as in Low et al., Experiment 2, but not in others, such as succeeding trials in the HebbWilliams maze where the location of barriers changes following reinforcement. The SHRs' propensity toward variation may also help to explain behaviors observed in the open field. SHRs generally ambulate more in the open field, as evidenced by their crossing more squares than WKYs (Cierpial et al., 1989; Gentsch et al., 1987; Knardahl & Sagvolden, 1979; Moser et al., 1988; van den Buuse & de Jong, 1989; Wultz et al., 1990). WKYs, on the other hand, remain near walls and ambulate less (Gentsch et al. 1987; Knardahl & Sagvolden, 1979; Moser et al., 1988; van den Buuse & de Jong, 1989; Wultz et al., 1990). These findings have been attributed to higher levels of general activity in SHRs or to higher levels of neophobic responses in WKYs (Rogers et al., 1988). In addition, the SHRs' tendency toward variable behaviors might cause them to cross more squares and enter different parts of the open field than WKYs. This tendency to vary may also help to explain the SHRs' high likelihood of exploring novel objects (Danysz et al., 1983; Delini-Stula & Hunn, 1985; Knardahl & Sagvolden, 1979; Rogers et al., 1988). The differential propensity of SHRs and WKYs to be reinforced for varying versus repeating may therefore help to explain

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