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Behavioral evaluation of the stress induced by the platform method for short-term paradoxical sleep deprivation in rats
Brain Research Bulletin,
0361-9230/89
Vol. 22, pp. 825-828. 0 Maxwell Pergamon Macmillan plc, 1989. Printed in the U.S.A
$3.00 + .OO
Behavioral Evaluation of the Stress Induced by the Platform Method for Short-Term Paradoxical Sleep Deprivation in Rats MARGALIDA COLL-ANDREU,” LIDIA AYORA-MASCARELL,” RAMON TRULLAS-OLIVAT AND IGNACIO MORGADO-BERNAL”’ *Area de Psicobioiogia, Universitat Autonoma de Barcelona, Ap. 46. 08193 Bellaterra, Barcelona, Spain ~~bor~to~ of Bioor~ffnic chemist, NI~~K, Nat~o~l institutes of Health, Beihesd~, MD 20892 Received 26 July 1988
COLL-ANDREU, hi., L. AYO~-MASCA~LL, R. TRULLAS-OLIVA AND I. MOR~ADO-BERNAL. Behaviornt evultcarion of the stress induced by the plarform method for short-term paradoxical sleep deprivation in rats. BRAIN RBS BULL 22(5) 825-828, 1989.-To evaluate whether the results of short-term PSD (Paradoxical Sleep Deprivation) using the platform method can be influenced by stress, changes in body weight and in behavioral indices (food and water intake and ambulation and defecation in an open field) were measured in rats after each of four S-hour sessions of confinement to small or large platforms. The animals of the two platform groups when compared to animals kept in home cages showed a similar decrease in body weight which was significant only after the first day of treatment, while no changes in the other measures were observed. It is concluded that 1) the effects of stress induced by short-term confinement to platforms do not seem to be a remarkable confounding factor in short-term PSD studies and 2) large platforms can be used both as an adequate stress control for small platforms and as a means of adapting the animals to the method. Paradoxical
sleep deprivation
Platform method
stress
THE platform method, or watertank, is a technique used for paradoxical sleep deprivation (PSD) in animals, It was designed by Jouvet et al. in 1964 (6) and has been widely used owing to its advantages: it is effective, economic and does not require any invasive manipulation of the anatomical and neurophysiological systems of the animals. However, it has been reported that the platform method subjects the animals to different stressful conditions (5,24). As a control for those side effects, Morden et al. (14) recommended the use of a larger platform. It is expected that animals placed on that platform are subjected to the same adverse conditions than those on the small platform, while sleep deprivation is low. Particularly, the platform method has been extensively used in ex~~ments concerned with the study of critical periods of ~st~ainingmemo~consolidation(l,3,4,7, 10, 11, 13, 16-22). One of those experiments (13), which was recently carried out in our laboratory, studied the effect of short-term (5 hr) posttraining platform method treatment upon distributed shuttle-box avoidance in rats. In contrast to what was expected, the treatment on a large platform (16 cm) improved learning over the successive training
‘Requests for reprints should be addressed
sessions. A similar but not significant improvement was also observed in the animals treated on a small platform (7 cm). Because those results could be mainly a consequence of the stress (and/or related arousal) induced by the treatment on platforms, we decided to investigate whether stress differences exist between small and large platform treatments which could explain the differences observed in shuttle-box improvement between large and small platform groups. Therefore, we designed an experiment in order to evaluate the stress induced by short-term confinement to small and large platforms. For that purpose, we measured body weight and behavioral indices (food and water intake and ambulation and defecation scores in the open field) in the experimental animals. METHOD
Subjects The subjects were 30 male Wistar rats, with an age ranging from 100 to 150 days old, and a mean weight of 412 g. (SD = 38.57) at the start of the experiment. Prior to the experiment
to Ignacio Morgado-Bemal.
825
X26
COLL-ANDREU
-
n
PSD
q
PSD
control
0
DRY
control
E7’AL_.
possible differences in sleepiness and fatigue with the other groups could be compensated). The rest of the procedures were the same as those carried out during adaptation. PSD control (n = l(I). Animals in this group were placed on large platforms for the same time and conditions as the ones in group I, The rest of the procedures were also identical. Dry control 1n= IO). Rats in this group remained in their home cages. All the procedures were the same as in the adaptation phase. RESULTS
5
BL-1
1-2 COMPARED
2-3
3-4
SESSIONS
FIG. 1. Percent of weight loss (meant S.E.M.) between consecutive sessions from baseline to the fourth day of treatment for the three groups. Statistical differences were found in the loss of body weight between dry control group and the two platform groups after the first session of treatment on flowerpots, F(2.27) = 8.02, p=O.O012. The differences were due to the fact that both platform groups lost more weight than dry controls. No significant differences were found on any of the other days. *p
animals were housed singly and allowed free access to food and water. They were always kept under conditions of controlled temperature (20-25°C) and humidity (40-708) and were subjected to an artificial light/darkness cycle of 12112 hr (lights on at 8 a.m. ). Apparatus Platforms. The platforms were inverted flowerpots placed in watettanks, with undersides projecting 1 cm above the surface of the water. The watertanks were covered with wire mesh lids to prevent the animals from escaping. Small platforms had a diameter of 7 cm, long platforms of 16 cm. Open field (OF). The OF consisted of a cylindrical wooden white surface, 33.5 cm high, and a round wooden platform divided into 19 sections approximately the same area. Illumination was provided by a 40 W red bulb hanging 1.2 meters above the floor of the OF. Feeders. Feeders for the measurement of the consumption of powdered food were made following the indications given by Leshem (12). Procedure Adaptation to the experimental conditions and baselines (7 days). This stage was necessary in order to adapt the subjects to
the special conditions which they were to undergo afterwards. Throughout this stage animals were subjected to the following daily treatments: at 4 p.m. they were handled and weighed, and then they were allowed free access to food and water for 3 hours (from 4:30 to 7:30 p.m.). At the onset of the dark period, rats were tested in the OF for 4 min. Finally, rats were taken back to their cages, in which they remained, deprived of food and water, until the following day at 4 p.m. The mean of the measures taken during days 5, 6 and 7 of this phase were considered as baseline values. Treatment on flowerpots (4 days). At the end of the adaptation period animals were randomly allocated to one of the three following groups: PSD (n = IO). Subjects in this group were placed on a small platform from 10 a.m. to 3 p.m. every day. After being removed from the platform, they were left in their cages for an hour (so that
Body Weight (See Fig. I). Over the four treatment sessions, rats in small and large platform groups lost, respectively, 4.39% and 3.15% of their baseline weight. Analyses of variance (ONEWAY-SPSSX) for the body weight changes between consecutive sessions (in %) showed significant differences among groups after the first day of treatment, F(2.27)=8.02, p=O.O012. Contrasts by the Duncan procedure showed that subjects in both PS and PSD control groups lost, on that day, significantly more weight than dry controls. Body weight changes did not significantly differ between any of the groups on the rest of the days. Food and Water Intake
As shown in Fig. 2, which depicts the evolution of all the behavioral measures during the treatment, food intake in both platform groups exhibited a slight decrease during the first day of the treatment period and an increase on days 2 and 3. In spite of that, analyses of covariance (MANOVA-SPSSX) taking baseline values as the covariate did not show statistical differences between groups on any treatment session. Similarly, analyses of covariance for the water intake did not show statistical differences, either, between any of the groups on any of the sessions. Open Field Behavior
A tendency to an increase of ambulation scores and a decrease of defecations throughout the sessions was observed in the three groups (see Fig. Z), but statistical analyses (analyses of covariante; MANOVA-SPSSX) failed to detect significant differences between the three groups, neither in the number of squares crossed nor in the number of defecations. DISCUSSION
The results obtained in our experiment show that short-term treatment to the platform method can be stressful, as indicated by the significant decrease of the animal body weight after the first treatment session. This decrease was apparently not dependent on a decrease of ingestion, for no substantial drop of either food or water intake was observed. The treatment had no effect on the OF measures recorded, either. Those findings cannot be compared to previous ones because, while long-term treatment on both small and large platforms has been reported to induce several behavioral and physiological stress responses (2, 8, 9, 15, 23), prior data on the stress induced by short-term treatment are lacking. From the data obtained in our experiment we can, therefore, suggest that when animals are subjected to short-term (hours) repeated treatment on platforms their overt behavior does not show critical disturbances which might constitute a confounding factor when studying the effects observed after the deprivation of paradoxical sleep achieved with this method and which could affect the performance on retention tests. On the other hand, the fact that
THE PLATFORM METHOD AND STRESS
2
4
3
SESSIONS
SESSIONS
8
PSD
Cl PSD
0
1
SESSIONS
2
3
control
DRY control
4
SESSIONS
FIG, 2. Evolution throughout baseline and the four treatment sessions of all the behavioral measures recorded in Experiment I (food and water intake, ambulation and defecation scores in an open field) in the three groups. All the variables are represented as percent of baseline values fmean+S.E.M.). No statistical differences between groups were found on any of the sessions. Dotted lines represent baseline values (100%).
between the two platform groups were not ever found indicates that the levels of stress are always similar in the two groups and, therefore, large piatforms can be considered adequate controls for the stress induced by small platforms. Finally, the fact that the body weight decrease was only significant after the first treatment sessions seems to indicate that, when applied intermittently over several sessions, animals adapt to the significant
differences
platform-induced stress. Differences by both platforms (small and large) main responsible for the differences observed in our previous experiment
in the levels of stress induced do not seem, therefore, the in shuttle-box improvement reported above (13).
ACKNOWLEDGEMENT This research was supported by a CAICYT grant (643184).
REFERENCES 1. Bloch, V.; Hennevin, E.; Leconte, P. Interaction between post-trial reticular stimulation and subsequent paradoxical sleep in memory consolidation processes. In: Drucker-Cohn, R. R.; McCaugh, J. L.. eds. Neurobiology of sleep and memory. London: Academic Press; 1977255-272. 2. Coenen, A. M. L.; Van Luijtelaar, E. L. J. M. Stress induced by three procedures of deprivation of paradoxical sleep. Physiol. Behav. 35501-504; 1985. 3. Danguir, J.; Nicolaidis, S. Impairments of learned aversion acquisition following paradoxical sleep deprivation in the rat. Physiol. Behav. 17:489-492; 1976. 4. Hars, B.; Hennevin, E. Reminder abolishes impairment of learning induced by paradoxical sleep retardation. Physiol. Behav. 30:831836; 1983. 5. Home, J. A.: McGrath, M. J. The consolidation hypotbesis for REM sleep function. Stress and other confounding factors: A review. Biol. Psychol. 18: 165-I 84; t 984. 6. Jouvet, D.; Vimont, P.; Delorme, F.; Jouvet, M. Etude de la privation selective de la phase paradoxal de sommeil chez le chat. C. R. SCanc. Sot. Biol. 158:756-759; 1964. 7. Kitahama. K.; Valatx, J. L.; Jouvet, M. Apprentissage d’un labyrinthe en Y chez deus souches de souris. Effects de la p~vation instrumentale et pharmacologique du sommeil. Brain Res. 108:75-86; 1976. 8. Kovalzon, V. M.; Tsibulsky, V. L. REM sleep deprivation without
9. 10.
11.
12. 13.
14.
15.
16.
stress in rats. In: Popoviciu, L.; Asgian, B.; Badiu, G., eds. Sleep 1978. Fourth European Congress on Sleep Research. Base]: S. Karger; 1980:41 l-414. Kovalzon, V. M.; Tsibulsky, V. L. REM sleep deprivation, stress and emotional behavior in rats. Behav. Brain Res. 14235-345; 1984. Leconte, P.; Hennevin, E. Caracteristiques temporelles de I’augmentation de sommeil paradoxal consecutif a I’apprentissage chez le rat. Physiol. Behav. 11:677-686; 1973. Leconte, P.; Hennevin, E.; Bloch, P. Duration of paradoxical sleep necessary for the acquisition of conditioned avoidance in the rat. Physiol. Behav. 13:675681; 1974. Leshem, M. A convenient feeder for the measurement of consumption of powdered food by rats. Physiol. Behav. 27:391-392; 1981. Marti-Nicolovius, M.; Portell-Cartes, I.; Morgado-Bemal. 1. Improvement of shuttle-box avoidance fotlowing post-training treatment in paradoxical sleep dep~vation platforms in rats. Physiol. Behav. 43:93-98: 1988. Morden, B.; Mitchel, G.: Dement, W. SeIective REM sleep deprivation and compensation phenomena in the rat. Brain Res. 5:339-349; 1967. Murison, R.; Ursin, R.; Coover, G. D.; Lien, W.; Ursin, H. Sleep deprivation procedure produces stomach lesions in ra&s. Physiol, Behav. 29:693-694; 1982. Pearlman, C. A. REM sleep deprivation impairs latent extinction in rats. Physiol. Behav. 11:233-237; 1973.
x2x
17. Pearlman. C. A.; Becker, M. Brief post-trial REM sleep deprivation impairs discrimination learning in rats. Physiol. Psychol. 1373-376: 1973. 18. Pearlman, C. A.; Greenberg, R. Post-trial REM sleep: a critical period for consolidation of shuttle-box avoidance. Anim. Learn. Behav. 1:49-51; 1973. 19. Rideout, B. E. Non-REM sleep as a source of learning deficits induced by REM sleep deprivation. Physiol. Behav. 22:1043-1047: 1979. 20. Shiromani, P.; Gutwein, B. M.; Fishbein, W. Development of learning and memory in mice after brief paradoxical sleep deprivation.
COLL-ANDREC
El’ AL.
Physiol. Behav. 22:971-979: 1979. 21. Smith, C.: Butler, S. Paradoxical sleep at selective times tollowing training is necessary for learning. Physiol. Behav. 29:469--173: 1982. 22. Smith, C.: Lapp. L. Prolonged increases in both PS and number ot REMs following a shuttle avoidance task. Physiol. Beha\ 36. 1053-1058; 1986. 23. Van Luijtelaar. E. L. J. M.; Coenen. A. M. L. Differential behavioral effects of two instrumental paradoxical sleep deprivation techniques in rats. Biol. Psychol. 15:85-93; 1982. 24. Vogel. W. A review of REM sleep deprivation. Arch. Grn. Psychiatry 32:749-761; 1975.
0361-9230/89
Vol. 22, pp. 825-828. 0 Maxwell Pergamon Macmillan plc, 1989. Printed in the U.S.A
$3.00 + .OO
Behavioral Evaluation of the Stress Induced by the Platform Method for Short-Term Paradoxical Sleep Deprivation in Rats MARGALIDA COLL-ANDREU,” LIDIA AYORA-MASCARELL,” RAMON TRULLAS-OLIVAT AND IGNACIO MORGADO-BERNAL”’ *Area de Psicobioiogia, Universitat Autonoma de Barcelona, Ap. 46. 08193 Bellaterra, Barcelona, Spain ~~bor~to~ of Bioor~ffnic chemist, NI~~K, Nat~o~l institutes of Health, Beihesd~, MD 20892 Received 26 July 1988
COLL-ANDREU, hi., L. AYO~-MASCA~LL, R. TRULLAS-OLIVA AND I. MOR~ADO-BERNAL. Behaviornt evultcarion of the stress induced by the plarform method for short-term paradoxical sleep deprivation in rats. BRAIN RBS BULL 22(5) 825-828, 1989.-To evaluate whether the results of short-term PSD (Paradoxical Sleep Deprivation) using the platform method can be influenced by stress, changes in body weight and in behavioral indices (food and water intake and ambulation and defecation in an open field) were measured in rats after each of four S-hour sessions of confinement to small or large platforms. The animals of the two platform groups when compared to animals kept in home cages showed a similar decrease in body weight which was significant only after the first day of treatment, while no changes in the other measures were observed. It is concluded that 1) the effects of stress induced by short-term confinement to platforms do not seem to be a remarkable confounding factor in short-term PSD studies and 2) large platforms can be used both as an adequate stress control for small platforms and as a means of adapting the animals to the method. Paradoxical
sleep deprivation
Platform method
stress
THE platform method, or watertank, is a technique used for paradoxical sleep deprivation (PSD) in animals, It was designed by Jouvet et al. in 1964 (6) and has been widely used owing to its advantages: it is effective, economic and does not require any invasive manipulation of the anatomical and neurophysiological systems of the animals. However, it has been reported that the platform method subjects the animals to different stressful conditions (5,24). As a control for those side effects, Morden et al. (14) recommended the use of a larger platform. It is expected that animals placed on that platform are subjected to the same adverse conditions than those on the small platform, while sleep deprivation is low. Particularly, the platform method has been extensively used in ex~~ments concerned with the study of critical periods of ~st~ainingmemo~consolidation(l,3,4,7, 10, 11, 13, 16-22). One of those experiments (13), which was recently carried out in our laboratory, studied the effect of short-term (5 hr) posttraining platform method treatment upon distributed shuttle-box avoidance in rats. In contrast to what was expected, the treatment on a large platform (16 cm) improved learning over the successive training
‘Requests for reprints should be addressed
sessions. A similar but not significant improvement was also observed in the animals treated on a small platform (7 cm). Because those results could be mainly a consequence of the stress (and/or related arousal) induced by the treatment on platforms, we decided to investigate whether stress differences exist between small and large platform treatments which could explain the differences observed in shuttle-box improvement between large and small platform groups. Therefore, we designed an experiment in order to evaluate the stress induced by short-term confinement to small and large platforms. For that purpose, we measured body weight and behavioral indices (food and water intake and ambulation and defecation scores in the open field) in the experimental animals. METHOD
Subjects The subjects were 30 male Wistar rats, with an age ranging from 100 to 150 days old, and a mean weight of 412 g. (SD = 38.57) at the start of the experiment. Prior to the experiment
to Ignacio Morgado-Bemal.
825
X26
COLL-ANDREU
-
n
PSD
q
PSD
control
0
DRY
control
E7’AL_.
possible differences in sleepiness and fatigue with the other groups could be compensated). The rest of the procedures were the same as those carried out during adaptation. PSD control (n = l(I). Animals in this group were placed on large platforms for the same time and conditions as the ones in group I, The rest of the procedures were also identical. Dry control 1n= IO). Rats in this group remained in their home cages. All the procedures were the same as in the adaptation phase. RESULTS
5
BL-1
1-2 COMPARED
2-3
3-4
SESSIONS
FIG. 1. Percent of weight loss (meant S.E.M.) between consecutive sessions from baseline to the fourth day of treatment for the three groups. Statistical differences were found in the loss of body weight between dry control group and the two platform groups after the first session of treatment on flowerpots, F(2.27) = 8.02, p=O.O012. The differences were due to the fact that both platform groups lost more weight than dry controls. No significant differences were found on any of the other days. *p
animals were housed singly and allowed free access to food and water. They were always kept under conditions of controlled temperature (20-25°C) and humidity (40-708) and were subjected to an artificial light/darkness cycle of 12112 hr (lights on at 8 a.m. ). Apparatus Platforms. The platforms were inverted flowerpots placed in watettanks, with undersides projecting 1 cm above the surface of the water. The watertanks were covered with wire mesh lids to prevent the animals from escaping. Small platforms had a diameter of 7 cm, long platforms of 16 cm. Open field (OF). The OF consisted of a cylindrical wooden white surface, 33.5 cm high, and a round wooden platform divided into 19 sections approximately the same area. Illumination was provided by a 40 W red bulb hanging 1.2 meters above the floor of the OF. Feeders. Feeders for the measurement of the consumption of powdered food were made following the indications given by Leshem (12). Procedure Adaptation to the experimental conditions and baselines (7 days). This stage was necessary in order to adapt the subjects to
the special conditions which they were to undergo afterwards. Throughout this stage animals were subjected to the following daily treatments: at 4 p.m. they were handled and weighed, and then they were allowed free access to food and water for 3 hours (from 4:30 to 7:30 p.m.). At the onset of the dark period, rats were tested in the OF for 4 min. Finally, rats were taken back to their cages, in which they remained, deprived of food and water, until the following day at 4 p.m. The mean of the measures taken during days 5, 6 and 7 of this phase were considered as baseline values. Treatment on flowerpots (4 days). At the end of the adaptation period animals were randomly allocated to one of the three following groups: PSD (n = IO). Subjects in this group were placed on a small platform from 10 a.m. to 3 p.m. every day. After being removed from the platform, they were left in their cages for an hour (so that
Body Weight (See Fig. I). Over the four treatment sessions, rats in small and large platform groups lost, respectively, 4.39% and 3.15% of their baseline weight. Analyses of variance (ONEWAY-SPSSX) for the body weight changes between consecutive sessions (in %) showed significant differences among groups after the first day of treatment, F(2.27)=8.02, p=O.O012. Contrasts by the Duncan procedure showed that subjects in both PS and PSD control groups lost, on that day, significantly more weight than dry controls. Body weight changes did not significantly differ between any of the groups on the rest of the days. Food and Water Intake
As shown in Fig. 2, which depicts the evolution of all the behavioral measures during the treatment, food intake in both platform groups exhibited a slight decrease during the first day of the treatment period and an increase on days 2 and 3. In spite of that, analyses of covariance (MANOVA-SPSSX) taking baseline values as the covariate did not show statistical differences between groups on any treatment session. Similarly, analyses of covariance for the water intake did not show statistical differences, either, between any of the groups on any of the sessions. Open Field Behavior
A tendency to an increase of ambulation scores and a decrease of defecations throughout the sessions was observed in the three groups (see Fig. Z), but statistical analyses (analyses of covariante; MANOVA-SPSSX) failed to detect significant differences between the three groups, neither in the number of squares crossed nor in the number of defecations. DISCUSSION
The results obtained in our experiment show that short-term treatment to the platform method can be stressful, as indicated by the significant decrease of the animal body weight after the first treatment session. This decrease was apparently not dependent on a decrease of ingestion, for no substantial drop of either food or water intake was observed. The treatment had no effect on the OF measures recorded, either. Those findings cannot be compared to previous ones because, while long-term treatment on both small and large platforms has been reported to induce several behavioral and physiological stress responses (2, 8, 9, 15, 23), prior data on the stress induced by short-term treatment are lacking. From the data obtained in our experiment we can, therefore, suggest that when animals are subjected to short-term (hours) repeated treatment on platforms their overt behavior does not show critical disturbances which might constitute a confounding factor when studying the effects observed after the deprivation of paradoxical sleep achieved with this method and which could affect the performance on retention tests. On the other hand, the fact that
THE PLATFORM METHOD AND STRESS
2
4
3
SESSIONS
SESSIONS
8
PSD
Cl PSD
0
1
SESSIONS
2
3
control
DRY control
4
SESSIONS
FIG, 2. Evolution throughout baseline and the four treatment sessions of all the behavioral measures recorded in Experiment I (food and water intake, ambulation and defecation scores in an open field) in the three groups. All the variables are represented as percent of baseline values fmean+S.E.M.). No statistical differences between groups were found on any of the sessions. Dotted lines represent baseline values (100%).
between the two platform groups were not ever found indicates that the levels of stress are always similar in the two groups and, therefore, large piatforms can be considered adequate controls for the stress induced by small platforms. Finally, the fact that the body weight decrease was only significant after the first treatment sessions seems to indicate that, when applied intermittently over several sessions, animals adapt to the significant
differences
platform-induced stress. Differences by both platforms (small and large) main responsible for the differences observed in our previous experiment
in the levels of stress induced do not seem, therefore, the in shuttle-box improvement reported above (13).
ACKNOWLEDGEMENT This research was supported by a CAICYT grant (643184).
REFERENCES 1. Bloch, V.; Hennevin, E.; Leconte, P. Interaction between post-trial reticular stimulation and subsequent paradoxical sleep in memory consolidation processes. In: Drucker-Cohn, R. R.; McCaugh, J. L.. eds. Neurobiology of sleep and memory. London: Academic Press; 1977255-272. 2. Coenen, A. M. L.; Van Luijtelaar, E. L. J. M. Stress induced by three procedures of deprivation of paradoxical sleep. Physiol. Behav. 35501-504; 1985. 3. Danguir, J.; Nicolaidis, S. Impairments of learned aversion acquisition following paradoxical sleep deprivation in the rat. Physiol. Behav. 17:489-492; 1976. 4. Hars, B.; Hennevin, E. Reminder abolishes impairment of learning induced by paradoxical sleep retardation. Physiol. Behav. 30:831836; 1983. 5. Home, J. A.: McGrath, M. J. The consolidation hypotbesis for REM sleep function. Stress and other confounding factors: A review. Biol. Psychol. 18: 165-I 84; t 984. 6. Jouvet, D.; Vimont, P.; Delorme, F.; Jouvet, M. Etude de la privation selective de la phase paradoxal de sommeil chez le chat. C. R. SCanc. Sot. Biol. 158:756-759; 1964. 7. Kitahama. K.; Valatx, J. L.; Jouvet, M. Apprentissage d’un labyrinthe en Y chez deus souches de souris. Effects de la p~vation instrumentale et pharmacologique du sommeil. Brain Res. 108:75-86; 1976. 8. Kovalzon, V. M.; Tsibulsky, V. L. REM sleep deprivation without
9. 10.
11.
12. 13.
14.
15.
16.
stress in rats. In: Popoviciu, L.; Asgian, B.; Badiu, G., eds. Sleep 1978. Fourth European Congress on Sleep Research. Base]: S. Karger; 1980:41 l-414. Kovalzon, V. M.; Tsibulsky, V. L. REM sleep deprivation, stress and emotional behavior in rats. Behav. Brain Res. 14235-345; 1984. Leconte, P.; Hennevin, E. Caracteristiques temporelles de I’augmentation de sommeil paradoxal consecutif a I’apprentissage chez le rat. Physiol. Behav. 11:677-686; 1973. Leconte, P.; Hennevin, E.; Bloch, P. Duration of paradoxical sleep necessary for the acquisition of conditioned avoidance in the rat. Physiol. Behav. 13:675681; 1974. Leshem, M. A convenient feeder for the measurement of consumption of powdered food by rats. Physiol. Behav. 27:391-392; 1981. Marti-Nicolovius, M.; Portell-Cartes, I.; Morgado-Bemal. 1. Improvement of shuttle-box avoidance fotlowing post-training treatment in paradoxical sleep dep~vation platforms in rats. Physiol. Behav. 43:93-98: 1988. Morden, B.; Mitchel, G.: Dement, W. SeIective REM sleep deprivation and compensation phenomena in the rat. Brain Res. 5:339-349; 1967. Murison, R.; Ursin, R.; Coover, G. D.; Lien, W.; Ursin, H. Sleep deprivation procedure produces stomach lesions in ra&s. Physiol, Behav. 29:693-694; 1982. Pearlman, C. A. REM sleep deprivation impairs latent extinction in rats. Physiol. Behav. 11:233-237; 1973.
x2x
17. Pearlman. C. A.; Becker, M. Brief post-trial REM sleep deprivation impairs discrimination learning in rats. Physiol. Psychol. 1373-376: 1973. 18. Pearlman, C. A.; Greenberg, R. Post-trial REM sleep: a critical period for consolidation of shuttle-box avoidance. Anim. Learn. Behav. 1:49-51; 1973. 19. Rideout, B. E. Non-REM sleep as a source of learning deficits induced by REM sleep deprivation. Physiol. Behav. 22:1043-1047: 1979. 20. Shiromani, P.; Gutwein, B. M.; Fishbein, W. Development of learning and memory in mice after brief paradoxical sleep deprivation.
COLL-ANDREC
El’ AL.
Physiol. Behav. 22:971-979: 1979. 21. Smith, C.: Butler, S. Paradoxical sleep at selective times tollowing training is necessary for learning. Physiol. Behav. 29:469--173: 1982. 22. Smith, C.: Lapp. L. Prolonged increases in both PS and number ot REMs following a shuttle avoidance task. Physiol. Beha\ 36. 1053-1058; 1986. 23. Van Luijtelaar. E. L. J. M.; Coenen. A. M. L. Differential behavioral effects of two instrumental paradoxical sleep deprivation techniques in rats. Biol. Psychol. 15:85-93; 1982. 24. Vogel. W. A review of REM sleep deprivation. Arch. Grn. Psychiatry 32:749-761; 1975.