BEHAVIORALAND NEURALBIOLOGY52, 152--169 (1989)
Avoidance Performance in Rat Enhanced by Postlearning Paradoxical Sleep Deprivation PASCALE GISQUET-VERRIER
D~partement de Psychophysiologie, CNRS, 91190 Gif-sur-Yvette, France AND CARLYLE SMITH 1
Department of Psychology, Trent University, Peterborough, Ontario K9J 7B8, Canada This series of experiments investigates possible relations between increases in paradoxical sleep (PS), persisting for several days after an avoidance training, and improvement of retention performance that occurred 3 days following partial training in a brightness discrimination Y-maze shock-avoidance task. SpragueDawley rats were trained in the Y-maze and PS deprived for 24 h either immediately or 24, 48, or 72 h following initial training. Contrary to what was expected, the results indicated that PSD immediately following the training session enhanced the avoidance performance after a 7-day retention interval. PSD at later times had no effect. Experiment 2 indicated that this effect was obtained only for PS-deprived animals and not for those placed in the PSD situation, but on larger platforms. Thus enhancement of the avoidance performance was not due to increases in stress or arousal caused by PSD-associated factors. Experiment 3 showed that the facilitative effect of a non-delayed 24-h PSD was obtained immediately thereafter as well as 24 h later, demonstrating that this effect was not due to any PS rebound which might have occurred following the PSD. Alternative explanations for these unexpected results are discussed. © 1989Academic Press, Inc.
There is now a large body of evidence establishing relations between paradoxical sleep (PS) and memory. It has been found in a variety of animals that PS increases over normal levels occur after successful learning has taken place (Bloch, Hennevin, & Leconte, 1979; Smith, 1985). PS deprivation (PSD) at the times of extra PS following training result in learning deficits (Bloch, 1970; Fishbein and Gutwein, 1978; McGrath and Cohen, 1978; Pearlman, 1979; Smith, 1985). It has been further Send requests for reprints to Pascale Gisquet-Verrier, Department de Psychophysiologie, LPN2, CNRS, 91190 Gif-sur-Yvette, France. 152 0163-1047/89 $3.00 Copyright© 1989by AcademicPress, Inc. All rightsof reproductionin any formreserved.
RETENTION PERFORMANCE ENHANCED BY PSD
demonstrated that these PSD vulnerable times, called PS windows (Smith, 1985), not only can manifest shortly after training, but also can appear hours and even days after the end of training. For example, in one study, rats trained in a two-way shuttle box avoidance task exhibited above normal levels of PS for up to 7 days after the end of training (Smith and Lapp, 1986). In this identical situation, PSD-induced learning deficits occurred 9-12 h after the first training session and 48-72 h after the end of the last training session (Smith and Kelly, 1988; Smith and Lapp, 1986). Recently, it has been shown that following partial training in a brightness discrimination Y-maze shock-avoidance task, retention performance was improved after a 3-day interval without any additional practice (Gisquet-Verrier and Alexinsky, 1988). Because the improvement was observed 72 h after the initial training, it was hypothesized that PS may have performed an important function prior to this second period as has been observed in the shuttlebox study. In order to determine where these PS windows might be operating in the Y-maze shock-avoidance task, it was decided to introduce a 24-h PSD at time delays of 0 (immediate), 1, 2, or 3 days following initial training. GENERAL METHOD
Subjects The subjects were naive male Sprague-Dawley rats obtained from the Iffa-Credo (Lyon) rearing center, 50-57 days old, and weighing 250 g at their arrival in the laboratory. They were housed in pairs, in wire-mesh cages, and had free access to food and water throughout the experiment.
Apparatus Training and testing were carried out in a fully automated black Perspex Y-maze with arms 13 cm wide x 60 cm long x 38 cm high and a 25cm equilateral choice area. A 40-W lamp was located at the end of each arm. The floor consisted of 3 mm diameter grids, spaced 9 mm apart. A shock generator (Campden, Model 521S), set to deliver scrambled shock, provided the incentive for learning. Photocells placed at 1 cm (proximal), 20 cm (medial), and 30 cm (distal) from the entrance of each arm were connected to an Apple II microprocessor which piloted the light sequence and the length of the intertrial interval and recorded latencies and the sequence of visited arms. The maze was housed in a darkened room, adjacent to the colony room.
Procedure Three days before the beginning of the pretraining session rats were handled two at a time for 5 consecutive min. The day before pretraining, handling was performed similarly with each individual rat.
GISQUET-VERRIER AND SMITH
Pretraining On Day 1, the rats, in groups of 6, were given 15 min free exploration in the entirely lighted maze. On Day 2, each rat was placed alone in the lighted maze and allowed to explore the apparatus for a 5-min period.
Training Training began on the following day. All animals were given 15 training trials according to the following procedure: each rat was placed in the starting lighted arm of the Y-maze for 20 s. The door closing the start arm (and used only on the first trial) was then opened, the light was turned off, and another arm was lighted. Five seconds later, an electric shock was applied to the grid floor in the whole maze, except the terminal 30 cm of the lighted arm. Throughout the experiment, the amplitude of the electrical shock was adjusted for each animal to just below the " c r y " level which corresponded to the minimal level for eliciting a rapid response (between 0.3 and 0.5 mA). The rat had to run to the lighted arm in order to escape the footshock. The time elapsed from the lighting of a new goal arm, until the subject crossed the proximal photobeam of the initial arm was defined as the start latency. Time elapsed until the subject crossed the distal photobeam of the new goal arm was defined as the response latency. When the animal crossed the medial photobeam of an arm, this arm was considered as having been visited. An incorrect response was scored when the rat entered at least 11 cm into one of the dark alleys, before escaping into the lighted alley. Animals that failed to respond within 60 s were manually pushed into the lighted arm. A response latency of 60 s was then scored. The rat remained in the safe compartment for a 20-s period which constituted the intertrial interval. An exit from the lighted alley led to shock. The goal alley on one given trial served as the start alley for the next trial. The sequence of correct right and left turns in the Y-maze was determined according to the following pseudorandom schedule: L - L R - L - R - R - L - R - R - L - R - L - L - R - R . Rats responding with mean latencies greater than 30 s during the five last training trials were discarded. After completion of the 15 training trials, control rats were removed from the maze and returned to their home cages where they remained for the time corresponding to their training-to-test interval (TTI). Rats were exposed to PSD for a 24-h period either immediately following training or after 24, 48, or 72 h following training.
Testing At the end of their retention interval, the animals were given 25 retraining trials under the same conditions as during the initial training
RETENTION PERFORMANCE ENHANCED BY PSD
with the light arm positioned according to the following sequence: L R-R-R-L-L-R-L-L-L-R-L-L-R-L-R-R-R-L-L-R-R-L-R-R.
Behavioral Measures Throughout training and testing, start latencies, response latencies, and sequences of visited arms were recorded for each trial. As pointed out in a recent paper (Gisquet-Verrier & Alexinsky, 1988), real avoidance response is difficult to obtain in our training situation, considering the length of the CS-UCS interval (5 s) relative to the size of the apparatus, as well as the low number of training trials (15). Toward that aim, attempts to avoid which correspond to exits from the initial arm, during the CS-UCS interval and which constitute the first stage toward an avoidance response, have also been considered. A response latency of less than 5 s permitted avoidance of the shock and was scored 2. When the start latency was less than 5 s, it was considered as an attempt to avoid the shock and was scored 1. The response latencies, the number of errors, and the avoidance scores were pooled in blocks of five trials for training and testing. A logarithmic transformation was applied to the response latencies for statistical analyses. Savings in avoidance responses were measured by the differences between the mean score of the first testing block and that of the last training block and constituted our index of retention (Gisquet-Verrier and Alexinsky, 1988).
Paradoxical Sleep Deprivation The paradoxical sleep deprivation was performed using the "swimming pool" technique. The animals were placed inside large plastic garbage pails which were closed with a cover. Water filled the pails to a level just below the base of the inverted pot. The pots had a base of 78 mm and a height of 120 mm. It was impossible for the animals to attain the relaxed posture of PS for more than few seconds without falling, becoming wet, and thus aroused. Control analyses on the PS deprivation indicated that PS was reduced by 95% whereas slow wave sleep was reduced by only 10%, when compared with the sleep baseline obtained in the same animals during the 2 days preceding PSD. In experiment 2, larger control platforms (diameter of 210 mm) were also used in order to control for the more general effects of the PSD situation without interrupting PS itself. Animals were placed in the PSD or pseudo-PSD situation for a period of 24 h. Following the PSD, animals were returned to their home cages until the time of the retention test. Animals for which retention was examined immediately following the PSD were completely dried before being placed in the Y-maze (This period never exceeded 8 min, during which animals always remained fully awake.)
GISQUET-VERRIER A N D SMITH EXPERIMENT
Subjects and Method Eighty male Sprague-Dawley rats served as subjects in this experiment. Five animals were discarded because of their poor training performance. The 75 remaining animals were trained before being assigned to one of the five experimental groups (n = 15). Nondeprived control animals (Group NPSD) were not subjected to any PSD. The other animals were PS deprived either immediately following training (Group PSDO) or after a 24-h (Group PSD24), 48-h (Group PSD48), or 72-h (Group PSD72) delay. All the animals were tested for retention 7 days after initial training.
Results Initial training: The analyses of variance performed on the three blocks of the training period and among the five experimental groups showed a significant effect of repetition on response latencies, errors, and avoidances (p < .005 to p < .001), indicating an ongoing acquisition process, but no initial differences between the groups (Fig. la).
PSD 24 NPSD NPSD
F]6. 1. (a) Mean number of avoidance responses obtained during training and retraining (occurred 7 days later) for each experimental condition. Non-PSD animals (Group NPSD) and PSD animals with the treatment introduced either immediately (Group PSDO) or 24 h (Group PSD24), 48 h (Group PSD48), or 72 h (Group PSD72) following initial training. (b) Mean score (-+SEM) of savings in avoidance responses corresponding to the difference between the score obtained during the first five test trials and the last five training trials, obtained for each experimental condition (within-group comparisons: **p < .025).
RETENTION PERFORMANCE ENHANCED BY PSD
Retention: Within-group comparisons showed no modification of the avoidance performance between training and testing for the NPSD control animals or for PSD24, PSD48, or PSD72 groups. However, the animals placed on PSD immediately following training (Group PSDO) exhibited a significant improvement in avoidance performance (F(1, 14) = 8.65, p < .025) (see Fig. la). Between-group comparisons performed on the savings in avoidance indicated no significant effect of the post-training treatments, including the comparison concerning Group NPSD and Group PSDO (F(1, 28) = 1.19, ns). However, an analysis of variance performed on the avoidance performance throughout retraining indicated that relative to Group NPSD, a facilitative effect of the immediate sleep deprivation (Group PSDO) was obtained (F(1, 28) = 4.77, p < .05) as well as the repetition (F(4, 112) = 3.83, p < .025) but not an interaction between both factors (F(4, 112) = .57) (see Fig. lb). There was no difference either within or between groups when the number of errors was analyzed. Discussion This experiment, which was designed to investigate the effects of PSD applied during a period that corresponds to the establishment of the longterm spontaneous improvement of the retention performance (LTSI) (Gisquet-Verrier & Alexinsky, 1988), gave unexpected results. First of all, contrary to previous experiments (Smith and Kelly, 1988), none of the delayed PSD groups exhibited disrupted retention performance. More unexpected was the fact that an immediate PSD of 24 h induced a facilitative effect, instead of the much more commonly observed disruptive effect on retention performance (Fishbein and Gutwein, 1978; McGrath and Cohen, 1978; Pearlman, 1979; Smith, 1985). We must emphasize that this effect was obtained on the avoidance performance but not on the discrimination performance. It did, however, persist for the whole retention test. Since animals were not habituated to the PSD situation, one possible explanation may be that the PSD imposed immediately after training induced an increase in arousal processes that in turn enhanced fixation of the memory trace. This treatment could conceivably be similar to a post-training stimulation of the mesencephalic reticular formation (Bloch, 1970) or even to a post-training exteroceptive stimulation (Emmerson & DeVietti, 1982). The results could also be due to a stressful effect of the PSD. It has already been noted that a moderately stressful situation can enhance retention in an avoidance task (Levine, 1966; Sagales and Domino, 1973). Another possible explanation might be that in the present experiment, in contrast to most of the PSD studies, the retention test took place long after the initial training (3 to 6 days later). Then, the later testing time
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could possibly be responsible for this unexpected facilitative effect of the immediate PSD. Under such conditions, the results could then be due to the rebound of paradoxical sleep which for the most part normally occurred during the first 24 h following the PSD (Dement, Henry, Cohen, & Ferguson, 1967). If this is true, one might expect that a PS rebound occurring 24 to 48 h following initial training could reinforce the consolidation/memory processes and then later enhance the retention performance. Yet, another explanation could be that the PSD delayed the maturation of the memory trace and that a retention test occurring 6 days later (Group PSDO) took place during the LTSI phase. These alternate explanations are examined in experiments 2 and 3. EXPERIMENT 2
The present experiment was done to investigate the possibility that the facilitative effect of immediate PSD could be due to an increase in arousal processes that, in turn, may enhance consolidation/memory processes and then improve the retention performance. Such an arousal could be due either to PSD in itself and associated factors or to the experimental conditions that accompanied PSD such as isolation, confinement, movement restraint, and frustration. In order to verify the possibility that the enhancement of retention performance could be due to these latter factors, animals placed under the same conditions as PSD animals but on larger platforms were compared to both nondeprived and PS-deprived animals.
Subjects and Method Forty-seven male Sprague-Dawley rats served as subjects in the present experiment. Two rats were eliminated because of their poor training performance. The 45 remaining animals were assigned to one of the three experimental groups (n = 15): Group NPSD (the control group), which was not subjected to PSD, Group PSDO consisting of animals placed for 24 h in the PSD situation immediately following training as in experiment 1, and Group Pseudo-PSDO (PsPSDO) which was identical to Group PSDO except that the animals were placed on larger platforms permitting PS episodes. As in experiment 1, all the animals were tested for retention 7 days following the training phase.
Results Initial training: As in the preceding experiment, analyses of variance performed on the training performance indicated a significant increase over the three blocks of five training trials whatever the performance measure (17 < .005 to p < .001) and no difference between groups (Fig. 2a).
RETENTION PERFORMANCE ENHANCED BY PSD FACILITATION • .
PSDO PsPSDO / i
NPSD PsPSD PSDO DISRUPTION
blocks of I
1 2 3
Fic. 2. (a) Mean number of avoidance responses obtained during training and retraining (7 days later) for non-PSD animals (NPSD), for animals placed in the PSD situation immediately following training (PSDO), and for animals placed in the PSD situation on large platforms (PsPSDO). (b) Mean score (-+ SEM) of savings in avoidance responses for each experimental condition (within-group comparisons: **p < .025).
Retraining: Within-group comparison indicated a significant improvement of the avoidance performance between the end of training and the beginning of testing for Group PSDO (F(1, 14) = 6.46, p = .022) and no significant difference for the two remaining groups (NPSD, F(1, 14) = 1; and PsPSD, F(1, 14) = 2.91) (see Fig. 2a). Between-group comparisons showed that Group PSDO exhibited more savings in avoidance than Group NPSD (F(1, 28) = 3.65, p = .063). None of the other comparisons reached significance (Fig. 2b). No difference between and within groups was found when the number of errors was considered. Conclusion The present results confirm those obtained in experiment 1 showing that an immediate 24-h PSD enhanced the retention performance 7 days following partial training in an avoidance task. Furthermore, the results indicate that this improvement in performance cannot be attributed to the experimental conditions associated with PSD since animals placed under similar conditions but on larger platforms did not exhibit similar enhancement in performance. However, these results do not allow us to preclude an arousal interpretation produced by PSD per se.
GISQUET-VERRIER AND SMITH EXPERIMENT 3
The first experiments demonstrated a facilitative effect of an immediate 24-h PSD on the retention performance, 7 days following initial training. In order to clarify these results, the aim of the present experiment was to determine which of the three factors (1) PSD, (2) rebound of PS, or (3) delay between deprivation and testing was implicated in this unexpected facilitative effect. For that purpose, trained animals were tested either immediately following the PSD, as was the case in most of the studies demonstrating a disruptive effect of the PSD on the retention performance (Smith, 1985), or 24 h later, i.e., after the PS rebound.
Subjects and Method Subjects were 72 male Sprague-Dawley rats. All animals received pretraining and training according to the previously mentioned general procedure. Eight animals were discarded because of their poor training performance. Half of the 64 remaining animals were exposed to an immediate 24-h PSD (PSDO), whereas the other half remained in their home cage (NPSD). Testing occurred for half of the animals 24 h (T24) following initial training (i.e., immediately after the PSD for the PSD animals) ,or 48 h (T48) for the other half (i.e., 24 h following the end of the PSD). Animals were then assigned to one of four experimental groups (n = 16): NPSD-T24, PSDO-T24, NPSD-T48, and PSDO-T48 according to a 2 (PS-deprived or nondeprived) × 2 (TTI = 24 or 48 h) factorial design.
Results Initial training: Analyses of the training performance indicated results similar to those obtained in the previous experiments: a significant increase in performance over the three blocks of five training trials (p < .03 to p < .001) and no difference between groups. Retraining: Figure 3 represents the results obtained for the avoidance measure. Within-group comparisons indicated an improvement in performance between the end of training and the beginning of retraining for Group NPSD-T24 (F(1, 15) = 4.31, p = .053), Group PSDO-T24 (F(1, 15) = 22.99, p < .001), and Group PSDO-T48 (F(1, 15) = 8.57, p <
.01). An overall analysis of variance performed 0n savings in avoidance indicated a significant facilitative effect of the paradoxical sleep deprivation (F(1, 60) = 9.00, p = .009), no effect of the TTI (F(1, 60) = 2.41), and no interaction between post-training treatments and length of the TTI (F(1, 60) = .097). Paired comparisons showed that the non-PSD animals exhibited significantly less savings in avoidance than the corresponding PSD animals (NPSD-T24 and PSDO-T24, F(1, 30) = 3.80, p = .057; NPSD-T48 and
R E T E N T I O N P E R F O R M A N C E E N H A N C E D BY PSD 
blocks of 1
FIG. 3. (a) Mean number of avoidance responses obtained during training and retraining occurring either 24 or 48 h following initial training for non-PSD animals (Groups N P S D T24 and NPSD-T48) and for animals placed in PSD immediately following training (Groups PSDO-T24 and PSDO-T48). (b) Mean score (---SEM) of savings in avoidance responses for each experimental condition (within-group comparisons: *.05 < p < .10 and *** p < .01).
PSDO-T48, F(1, 30) = 5.22, p = .028). On the other hand, there was no difference between the two non-PSD control groups or between the two PSDO groups (F < 1 in each case). A 2 x 2 x 5 analysis of variance (post-training treatment x TTI x repetition of retraining block trials) indicated a significant main effect of post-training conditions (PS deprivation or not) (F(1, 60) = 5.69, p = .019) and of the repetition (F(4, 60) = 6.25, p < .001). Table 1 indicates the percentage of animals which emitted an avoidance response during the last block of training trials and the first block of testing trials. X z analyses indicated that while there was no difference between the four groups at the end of training (e(3) = .39), large dif-
Percentage of Animals during the Last Block of Training and the First B l oc k of Testing
% = 13 % = 38
% = 19 % = 81
% = 13 % = 19
% = 13 % = 75
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ferences were obtained at the beginning of testing (e(3) = 17.29, p < .001) with significantly more PS-deprived animals avoiding than the corresponding nondeprived animals (TTI 24 h, e(1) = 6.34, p < .02; TTI 48 h, e(1) = 10.16, p < .01). Statistical analyses performed on the discriminative score (number of errors) indicate that none of the comparisons led to a significant effect. Conclusion This experiment demonstrates that a 24-h PSD delivered immediately after a partial brightness discrimination avoidance training induced a clear facilitative effect on the retention performance of rats tested either immediately or 24 h thereafter. The results indicate that there is not only an increase in the number of avoidance responses but also an increase in the number of animals giving an avoidance response. These results indicate the facilitative effect of PSD on the avoidance performance does not depend on a PS rebound.
GENERAL DISCUSSION The results obtained in this series of experiments demonstrate that a 24-h PSD starting immediately after a training episode can induce a facilitative effect on retention of an avoidance task. Results from experiment 2 demonstrate that this unexpected effect is not due to properties of stress induced by PSD-associated factors, since animals placed under similar general conditions but on larger platforms do not exhibit similar facilitation. The facilitative effect of PSD is evident when testing takes place immediately after the end of the PSD, demonstrating that the enhancement of performance is not related to the postdeprivation rebound PS. To be effective, PSD must be linked in time with the acquisition phase. No effect was obtained following a 24-h or more delayed PSD. The enhancement of the avoidance performance induced by PSD persists over several days, being observed 24 h and even, although somewhat attenuated, 6 days following the end of the treatment. In every case, the facilitative effect of post-training PSD has been demonstrated on the avoidance component of the performance and never on the discrimination performance. It has been repeatedly noted in studies using similar training tasks that, whereas avoidance performance was affected by various treatments, no effect was obtained with respect to the ability of the rats to correctly recall the safe stimulus. It can be emphasized that such a differential effect is due to the fact that the choice response is overlearned relative to the avoidance response and, hence, less susceptible to any intervening factor (see Gisquet-Verrier & Alexinsky, 1988). These results, demonstrating a clear facilitative effect of post-training PSD, could be analyzed as being due to the fact that PSD actually
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improves memory. As a general theoretical idea, such a position seems too extreme. The substantial PS/learning literature (Bloch, 1970; Fishbein & Gutwein, 1978; Pearlman, 1979; Smith, 1985) suggests that PS is necessary in many learning situations, not necessary in a few, and apparently detrimental in the odd situation. Hence these unexpected data, contrary to the bulk of the literature, may instead result from special features in our experimental design. One possible unique condition is the length of the PSD. An examination of the literature, however, indicates that although many studies show a detrimental effect on learning with much shorter PSD periods, there are also many which show a similar effect after a 24-h or longer post-training PSD (Fishbein, 1971; Leconte and Bloch, 1970; Smith, 1985). Thus, the length of PSD would not seem to be adequate to explain the present results. One factor which was somewhat different from the majority of studies was the low level of training that was carried out (15 consecutive trials during training). This procedure led to very partial learning performance. It has been well established that PSD is ineffective when applied following minimal learning (Kitahama, Valatx, & Jouvet, 1981) or following overlearning (Sloan, 1972). However, although amount of training could explain an absence rather than a disruptive effect of PSD, it is inadequate to explain a facilitative rather than a disruptive effect of PSD on learning. Another variable is the nature of the task. Pearlman (1979) has noted that the success of post-training PSD experiments was highly correlated with task difficulty. According to Seligman's (1970) distinction between prepared and unprepared learning, the Y-maze shock-avoidance task used in the present experiment has to be classified as an unprepared learning task, and hence should be susceptible to PSD, at least for one of the considered measures. As a matter of fact, PSD has already been observed to disrupt learning with this type of task in both appetitive and aversive situations (Kitahama et al., 1981; Pearlman & Becker, 1973). Task difficulty could account for lack of effect on retention, but is unable to account for a facilitative effect. There is one study in the literature that reports an enhancement of avoidance performance following post-training PSD (Kitahama, Valatx, & Jouvet, 1976). There are several similarities between the present study and this study. In both cases animals were submitted to a partial acquisition (15 consecutive training trials) of a brightness discrimination avoidance task in a Y-maze. The PSD benefited the avoidance component but not the discrimination component of the task. This effect was obtained with 10 h of PSD on C57B1 mice. Since the opposite effect was observed, in the same study, with C57Br animals, it seems possible that the strain of animal used in these studies might be an important variable. Although PSD animals in both experiments
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performed better than the corresponding non-PSD animals, the avoidance scores remained quite low (Kitahama et al., 1976). Behaviorally, the C57B 1 strain was inferior in learning ability to the C57Br strain. Similarly, the Sprague-Dawley rat has been shown to be a poor performer when it comes to avoidance relative to rats from other strains, such as black rats (Schaeffer, 1959), Long-Evans (Nakamura & Anderson, 1962), or Wistar (Kuribara, Ohashi, & Tadokoro, 1976). Barrett, Leith, and Ray (1973) indicated that Fischer F344 or CDF were greatly superior to the Sprague-Dawleys in acquiring the avoidance response using a brightness discrimination in a Y-maze, although both strains learned the discrimination component of the task. It seems well established that strain differences in acquiring an avoidance response is based upon the activity response to shock stress and not to a difference in general learning ability. In support of that view, it has been shown that the strain-specific response differences to the shock can be manipulated by the administration of drugs. For instance, combined injections of scopolamine and amphetamine, both known to attenuate induced behavioral suppression, have been shown to increase the avoidance performance of Sprague-Dawley rats to a level similar to that reached by the other strains (Barrett et al., 1973). It could be hypothesized that the avoidance score used in this series of experiments, which included avoidance responses as well as attempts to avoid, is particularly susceptible to a decrease in behavioral suppression. This suppression is shown to be strong in Sprague-Dawley rats placed in an avoidance situation. However, under similar conditions, a facilitative effect of PSD has also been obtained in overtrained animals when avoidance responses alone were considered (Gisquet-Verrier & Smith, 1988). Further, it would be expected that similar treatments would lead to opposite results when applied to different strains of rats, depending on their initial internal state. The study performed by Kuribara et al. (1976), demonstrating that pretest injections of Diazepam differentially affect the avoidance performance of rats as a function of their strain, supports this assumption. More precisely, the authors showed a decrease in avoidance response in good avoidance performers (Wistar and Holtzman rats) whereas the avoidance response of normally poor avoidance performers (Sprague-Dawley rats) was improved. It would seem that in most cases PSD induces an 'impairment of the avoidance performance. However, when applied to our Sprague-Dawley rats, PSD instead induces an improvement in performance, perhaps because of a differential behavioral response to a similar treatment, due to strain differences. An examination of the learning-sleep literature shows that the Sprague-Dawley was used somewhat less than either the Wistar or the LongEvans rats and the number of experiments reporting positive results
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following PSD was higher for these two latter strains. However, a substantial number of studies using this strain and avoidance tasks have provided results implicating PS in the learning process (Smith, 1985; Smith and Kelly, 1988; Smith and Lapp, 1986). However, it should be noted that the avoidance behavior demonstrated by rats of the same strain but coming from different vendors can be considerably different. Nakamura and Anderson (1962) indicated differences in the percentage of avoidance responses, such as 76% versus 47%, in two groups of L o n g Evans rats provided by two different suppliers. Such a factor could account for the discrepancies obtained between " F r e n c h " and "Canadian" Sprague-Dawley rats. An important point concerns the mechanism by which an immediate PSD can induce an improved performance evidenced not only immediately following PSD but also 6 days later, when most of the internal consequences of a 24-h PSD could be expected to have dissipated. In experiment 2 of the present study, it was clearly established that PSD-associated factors, such as isolation, confinement, movement restraint, and frustration, do not determine the facilitative effect of PSD, since animals placed under the same conditions but on larger platforms did not exhibit a similar improvement in performance. It should also be noted that Kitahama et al. (1976) obtained a facilitative effect of PSD on C57B1 mice with instrumental PSD as well as with pharmacologically induced PSD. This result confirms our data in showing that PSD itself, and not associated factors, is implicated in these unexpected facilitative effects. Thus the possibility remains that in our animals, known to demonstrate a large behavioral suppression, PSD itself causes an increase in arousal that enhances information processing in the same way as a post-trial reticular stimulation (Bloch, 1970) or a post-training exteroceptive stimulation (Emmerson & DeVietti, 1982). A similar explanation has recently been proposed by Marti-Nicolovius, Portel-Cortes, and Morgado-Bernal (1988) to explain the improvement of performance obtained during acquisition in control animals placed on large platforms. The fact that a facilitative effect of PSD, obtained in the present study, persists throughout long-term intervals, provides more support for a retrograde effect of PSD. Alternately, it can be proposed that PSD affects the internal state of the animals in such a way that they become more able to perform an avoidance response. For example, it has been reported that PSD results in diminished fear in the Sprague-Dawley rat (Hicks and Moore, 1979). Animals deprived of either 48 or 96 h of PS showed reduced scores on emotionality (less defecation and urination, increased exploration) in an open field situation compared to non-PSD controls. In the present studies, it might be possible, in experiment 3, to explain the superior avoidance behavior of the PSDO-T24 group in terms of reduced fear. It seems
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somewhat less likely, although still possible, that the effects of the PSD were still partially present one day after the end of the deprivation (PSDO-T48) and could account for the superior number of avoidances compared to controls. However, it seems very unlikely that it could account for the enhancement effects observed in experiments 1 and 2, since retesting occurred 7 days after the PSD. The literature presents clear evidence that PSD induces dysfunctioning in neurotransmitter systems. On the other hand, similar alterations of the internal state have been shown to enhance avoidance responses. Stern and Morgane (1974) suggested that paradoxical sleep maintains the functioning of the catecholamine system in the central nervous system. They demonstrated that administration of drugs which enhanced catecholamine activity can reverse some behavioral deficits which occurred with PSD. More recently, Monti (1982, 1983) indicated that depletion of noradrenaline (NA) and dopamine (DA) results in a reduction of PS. Cooper, Breese, Howard, and Grant (1972) reported that modest levels of reduction in NA and to a lesser extent DA in the Sprague-Dawley rat resulted in superior ability to learn the two-way shuttle shock-avoidance task compared to controls. This could possibly explain the facilitative effect of PSD on retention performance. However, the change in NA in rats following PSD produced by the conventional platform technique does not appear to be large. While Tsuchiya, Tom, and Kobashi (1969) found a reduction in NA following PSD, several other groups reported no change in NA levels after varying numbers of days of PSD (Pujol, Jouvet, & Glowinski, 1968; Stern, Miller, Cox, & Maickel, 1971). Another transmitter apparently more responsive to change with PSD is acetylcholine (Ach). Skinner, Overstreet, & Orbach (1976) demonstrated that injections of physostigmine (an anticholinesterase agent) delivered after training prevented the memory-disruptive effects of PSD. Further, two studies reported reduced amounts of ACh in rat telencephalon after 96 h of PSD (Bowers, Hartmann, & Freedman, 1966; Tsuchiya et al., 1969). Tsuchiya et al. (1969) also reported an increase in ACh in the telencephalon after 24 h of PSD. ACh transmitter levels are also believed to vary with time following shock escape training in a Y-maze. Artificially increasing or decreasing ACh levels following training in rats was found to be either beneficial or detrimental depending upon when it was induced (Deutsch, 1983). These authors concluded that the optimum level of ACh necessary to maintain memory varied for many days following the end of training. It is possible that immediate PSD induces, in our Sprague-Dawley rats, a particular internal state which reduces the behavioral suppression, particularly strong in Sprague-Dawley rats. This in turn enhances their ability to adequately perform an avoidance response. Such an internal state would be present at the time of testing when PSD ended just before
RETENTION PERFORMANCE ENHANCED BY PSD
the retention test or would be evoked by replacing the animals in the training situation in the case of a delayed retention test. The present findings demonstrate that, at least in some particular circumstances, retention performance can be enhanced by PSD. Whatever the cause of such facilitation, this result sheds some light upon the generality of the relation between PS and memory. Such a relationship must now be considered to be more complex than it has to this point. To summarize, the results of the present experiment indicate that under certain conditions a 24-h PSD can enhance retention performance and a more complex relation between PS and memory exists than previously believed. Important variables undoubtedly include strain and type of learning task, number of training trials, hours of PSD, and training test intervals. In our opinion, the unexpected facilitative effects of an immediate 24-h PSD, obtained in the present study, are probably due to an interaction between these variables and two main factors, the genetic characteristics of the animals used in this study and the internal state of these animals which may react differently than other strains to the same PSD treatment. Whether PSD induces decreased behavioral suppression by increasing arousal, which enhances information processing, or modifies the internal state of the animals in such a way that they are better able to perform the avoidance response cannot be determined from the present data.
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Fishbein, W., & Gutwein, B. M. (1978). Paradoxical sleep and memory storage processes. Behavioral Biology, 19, 425-464. Gisquet-Verrier, P., & Alexinsky, T. (1988). Time-dependent fluctuations of retention performance in an aversively motivated task. Animal Learning & Behavior, 16, 5866. Gisquet-Verrier, P., & Smith, C. (1988). Paradoxical sleep deprivation enhances retention performance in a Y-maze avoidance task in rats. Communication presented in the Annual Meeting of European Brain and Behaviour Society, Zurich. Hicks, R. A., & Moore, J. D. (1979). REM sleep deprivation diminishes fear in rats. Physiology & Behavior, 22, 689-692. Kitahama, K., Valatx, J.-L., & Jouvet, M. (1976). Apprentissage d'un labyrinthe en Y chez deux souches de souris. Effets de la privation instrumentale et pharmacologique du sommeil. Brain Research, 108, 75-86. Kitahama, K., Valatx, J.-L., & Jouvet, M. (1981). Paradoxical sleep deprivation and performance of an active avoidance task: impairement in C57Br mice and no effect in C57B1/6 mice. Physiology & Behavior, 27, 41-50. Kuribara, H., Ohashi, K., & Tadokoro, S. (1976). Rat strain differences in the acquisition of conditioned avoidance responses and in the effects of Diazepam. Japanese Journal of Pharmacology, 26, 725-735. Leconte, P., & Bloch, V. (1970). D6ficit de la retention d'un conditionnment apr6s privation de sommeil paradoxal chez le rat. Comptes rendus hebdomadaires des S~ances. Academie des Sciences, Paris, 271, 226-229. Levine, S. (1966). UCS intensity and avoidance learning. Journal of Experimental Psychology, 71, 163-164. Marti-Niclovius, M., Portell-Cortes, I., & Morgado-Bernal, I. (1988). Improvement of shuttle-box avoidance following post-training treatment in paradoxical sleep deprivation in rats. Physiology & Behavior, 43, 93-98. McGrath, M. J., & Cohen, D. B. (1978). REM sleep facilitation of adaptive waking behavior: A review of the literature. Psychological Bulletin, 85, 24-57. Monti, J. M. (1982). Catecholamines and the sleep-wake cycle. I. EEG and behavioral arousal. Life Sciences, 30, 1145-1157. Monti, J. M. (1983). Catecholamines and the sleep-wake cycle. II. REM sleep. Life Sciences, 32, 1401-1415. Nakamura, C. Y., & Anderson, N. H. (1962). Avoidance behavior differences within and between strains of rats. Journal of Comparative & Physiological Psychology, 55, 740747. Pearlman, C. (1979). REM sleep and information processing: Evidence from animal studies. Neuroscience and Biobehavioral Reviews, 3, 57-68. Pearlman, C., & Becker, M. (1973). Brief posttrial REM sleep deprivation impairs discrimination learning in rats. Physiological Psychology, 1, 373-376. Pujol, J. F., Jouvet, M., & Glowinski, J. (1968). Increased turnover of cerebral norepinephrine during rebound of paradoxical sleep in the rat. Science, 159, 112-114. Sagales, T., & Domino, E. F. (1973). Effects of stress and REM sleep deprivation on the patterns of avoidance learning and brain acetylcholine in the mouse. Psychopharmacologia, 29, 307-315. Schaeffer, V. H. (1959). Differences between strains of rats in avoidance conditioning without an explicit warning stimulus. Journal of Comparative & Physiological Psychology, 52, 120-122. Seligman, M. E. P. (1970). On the generality of the laws of learning. Psychological Review, 77, 406-418. Skinner, D. M., Overstreet, D. H., & Orbach, J. (1976). Reversal of the memory-disruptive effects of REM sleep deprivation by physostigmine. Behavioral Biology, 18, 189-198.
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Sloan, M. A. (1972). The effects of rapid eye movement (REM) sleep on maze learning and aggression in the albino rat. Journal of Psychiatric Research, 9, 101-111. Smith, C. (1985). Sleep states and learning: A review of the animal literature. Neuroscience & Biobehavioral Reviews, 9, 157-168. Smith, C., & Kelly, G. (1988). Paradoxical sleep deprivation applied two days after the end of training retards learning. Physiology & Behavior, 43, 213-216. Smith, C., & Lapp, L. (1986). Prolonged increases in both PS and number of REMs following a shuttle avoidance task. Physiology & Behavior, 36, 1053-1057. Stern, W. C., Miller, F. P., Cox, R. H., & Maickel, R. P. (1971). Brain norepinephrine and serotonin levels following REM sleep deprivation in the rat. Psychopharmacologia, 22, 50-55. Stern, W. C., & Morgane, P. J. (1974). Theoretical view of REM sleep function: Maintenance of catecholamine systems in the central nervous system. Behavioral Biology, 11, 1-32. Tsuchiya, K., Toru, M., & Kobashi, T. (1969). Sleep deprivation: Changes of monoamines and acetylcholine in rat brain. Life Sciences, 8, 867-873.