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Effects of pretraining paradoxical sleep deprivation upon two-way active avoidance
BEHAVIOURAL BRAIN RESEARCH ELSEVIER
Behavioural Brain Research 72 (1996) 181-183
Short communication
Effects of pretraining paradoxical sleep deprivation upon two-way active avoidance Agn~s Gruart-Masso 1, Roser Nadal-Alemany, Margalida Coll-Andreu, Isabel Portell-Cort~s, Margarita Marti-Nicolovius * Area de Psicobiologia, Departament de Psicologia de la Salut, Universitat Aut~noma de Barcelona, Apartat 46, 08193 Bellaterra, Barcelona, Spain Received 3 February 1995; revised 11 April 1995; accepted 12 April 1995
Abstract
In order to study whether paradoxical sleep (PS) is necessary to prepare subjects for the subsequent learning of a distributed two-way active avoidance cc~nditioning, 10 rats were subjected to 5 h of paradoxical sleep deprivation (PSD group) by means of the platform method immediately before each of 5 acquisition sessions (one daily), as well as before a long-term retention (LTR) session (14 days). Another group of rats (PSD control group; n=10) were placed on large platforms as a control for the side effects induced by PSD platforms. Rats in the dry control group (n = 10) did not receive any treatment. The number of avoidances of the PSD group was signiticantly lower on the 1st, 2nd and 3rd acquisition sessions compared to the PSD control group, and on the 2nd and 3rd sessions compared to the dry control group. PSD rats made significantly less intertrial crossings than dry controls on the 2nd and 3rd acquisition sessions, but no significant correlations were found between this variable and the number of avoidances. Therefore, o~Lrresults are not fully in contradiction with the hypothesis that PS previous to the training sessions might prepare the animal fer subsequent learning, although the influence of locomotor changes upon the performance of PSD subjects cannot be fully rejec,ted. Keywords: Pretraining rapid eye movement(REM) sleep deprivation;Two-wayactive avoidance; Learning and memory
A wide range of experimental data suggests that paradoxical sleep (PS) might be involved in learning and in memory consolidation processes [4,15]. Two basic questions have centered the interest of paradoxical sleep deprivation (PSD)experiments: (1) does PS prepare the subject for subsequent learning?; and (2) does PS facilitate the consolidation process? The latter question can be addressed in studies of post-training PSD. Studies using the pretrainJng approach are based on the hypothesis that PSD affects several factors involved in learning (i.e., neurotransmitters), so that PSD before training might impair learning dependent upon such factors. Two kinds of measures have been investigated: performance during initial exposure to the task (acquisition); and performance at some later time (retention) [123. 1Present address. Laboratorio de Neurosciencia,Facultad de Biologia, Avda Reina Mercedes, s/n, 41012 Sevilla, Spain. * Corresponding author. Fax: + 34 3 581 23 24. 0166-4328/96/$9.50© ElsevierScienceB.V. All rights reserved SSSDI 0166-4328(96)00082-8
Several studies on pretraining PSD in rats have shown detrimental effects upon the acquisition of one-way active avoidance, taste aversion, and passive avoidance [8,15], while no effects were found upon appetitive operant conditioning [ 5]. With regard to two-way active avoidance, only one work has shown detrimental effects after pretraining PSD in rats, and only when using the platform method, while no effects were found with the pendulum technique [17]. Other works have found no effects [13 or even a slight facilitatory effect upon the acquisition of shuttle-box avoidance [ 11,13 ]. With mice, deleterious effects of pretraining PSD upon two-way active avoidance have been reported only upon longterm retention, but not upon acquisition 1-14]. In summary, results regarding the influence of pretraining PSD upon shuttle-box avoidance are highly controversial. All the works studying the effects of pretraining PSD upon two-way active avoidance have been carried out on massed training (a single session consisting of a high number of trials), using a long PSD treatment adminis-
182
Agnks Gruart-Masso et al./Behavioural Brain Research 72 (1996) 181 183
tered in a single session (24-120 h), and without a previous adaptation of the animals neither to the platform method nor to the conditioning apparatus. Therefore, we designed an experiment aimed at evaluating whether PS previous to the acquisition and longterm retention (LTR) sessions of two-way active avoidance, when distributed training is used, is needed to prepare the subject for learning. To reduce the influence of the side effects induced by the PSD technique [2,3,6,9,10,16], short repeated 5-h sessions (one daily) of PSD by means of the platform method and previous sessions of adaptation to this technique have been used in the present work. Thirty naive male Wistar rats, with a mean age of 113 days (S.D.=4) and a mean weight of 441 g (S.D. = 11.9) at the beginning of the experiment, were used. In order to familiarize the subjects with the learning conditions each animal had 3 sessions (one daily) of adaptation to the shuttle-box apparatus (Campden Instruments, Ltd.), each consisting of 20 min of free ambulation. To habituate the animals to the platform method, they were also given 5 adaptation sessions (one daily), each consisting of being placed for 2 h on large platforms (16 cm diameter). Smaller platforms (7 cm diameter) were not used for adaptation to overcome the possibility that PSD during the adaptation phase might affect subsequent learning. The last 3 of those sessions were conducted on the same days as the shuttle box adaptation sessions. Forty-eight hours after the end of the adaptation sessions, subjects had 5 training sessions (10 trials each) in the two-way active avoidance apparatus, separated by 24-h intervals. The conditioned stimulus was a 80-dB tone lasting up to 3 s; the unconditioned stimulus consisted of an electrical footshock of 1 mA 30 s duration at most. A l-min intertrial interval was used. Both treatment and training sessions were conducted during the light time of the light-dark cycle. During the 5 h immediately previous to each acquisition session, animals were either placed on 7-cm platforms (PSD group; n= 10), on 16-cm platforms (PSD control group; n = 10) or were maintained in their home cage (dry control group; n = 10). The platform technique used in the present work has been described in detail elsewhere [7]. Fourteen days after the last training session, all subjects were given another 10-trial session to evaluate the level of LTR. To avoid the possibility that state-dependency would interfere with the performance of the subjects, the corresponding treatment was also administered prior to that session. As shown in Fig. 1, and confirmed by a MANOVA (polynomial c o n t r a s t : F1,27 = 13.87; P=0.001), the evolution of learning followed the expected upward tendency in all the groups. Comparison among groups for each session (MANOVA, 'simple' contrast) indicated that the number of avoidances of the PSD group was significantly lower compared to the PSD control group
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Fig. 1. Effects of pretraining PSD treatment upon the number of avoidances during acquisition and LTR (14 days) of a distributed shuttle box avoidance task. Results are expressed in means (+ S.E.M.).
on the first (F1,27= 6.24; P = 0.019), second (F1.27= 5.63; P=0.025), and third (Fl,zT=6.16; P=0.020) training sessions. On the other hand, the PSD group subjects made a statistically lower number of avoidances than the dry control group on both the second (F1.27 = 6.53; P=0.017) and third (};'1,27=5.75; P=0.024) sessions. The performance of animals in the PSD control group never differed in a statistical way from that of the dry control group. No statistical differences existed, either, between any of the groups during the LTR session. Furthermore, no differences between the mean avoidances on the last acquisition session and those of the LTR session were found within any of the groups. PSD subjects showed a lower number of intertrial crossings than the dry control ones on the 2nd and 3rd acquisition sessions (MANOVA, Contrast 'Simple': Fl,ZT=4.69; P=0.039 and /1,17=7.86; P=0.009, respectively). Nevertheless, the number of intertrial crossings did not show any statistical correlations with the number of avoidances on any session and for any group. In summary, 5 repeated sessions (one daily) of 5-h pretraining PSD treatment slowed down the acquisition of a distributed two-way active avoidance task, while having no effect either upon the final learning level achieved or upon LTR. These findings agree with those of a previous work where a detrimental effect upon a massed two-way active avoidance task was found after 72 h of PSD treatment with the platform method, either simple or multiple [ 17]. Nevertheless, our results do not agree with the lack of effects found both in the abovereported work when using the pendulum technique, and in another work using the platform method [ 1]. They
Agnds Gruart-Masso et al./Behavioural Brain Research 72 (1996) 181-183
do not either agree with other papers reporting facilitatory effects upon the acquisition of the same kind of task after 9 6 h [11] and 120h [13] of PSD treatment with the platform method. In contrast, the lack of effects of pretraining PSD upon L T R is in concordance with other experiments carried out in rats [ 13,17]. Nevertheless, the possibility remains that L T R might have been affected if a lower number of acquisition sessions had been used. The discrepancies between our results and those found in other experiments might be due to methodological differences, such as the uLse of different PSD techniques (namely, platform method vs pendulum technique), of different training schedules (massed vs distributed training), or of longer PSD treatment times (from 24 to 120 h in a single session vs 5-h repeated sessions in our work). Nevertheless, additional factors have also to be taken into account, since disruptive effects were also observed in a study using massed training (50 trials) and a long PSD session ,(72 h) [17]. Another factor to be considered is the degree of PSD obtained with the platforan method. This factor is influenced by the ratio between the animal weight and the PSD platform diameter 118]. Only in the previous work reporting a deterioration of performance [17], this ratio (330 g/6.2 cm) was rather similar to that in the PSD group of the present work (441 g/7 cm). In contrast, in the other studies [1,13], (:his ratio (150-200 g/7 cm) was similar to that in our PSD control platforms (441 g/16 cm). Therefore, this variable might be critical in explaining the discrepancies among the different works. Is the disruptive effect of acquisition observed in our experiment due to the deprivation of PS or is it attributable to the side effects induced by the platform method, such as stress or locomotor activity changes? A previous experiment in our laboratory showed that both PSD and PSD control platforms induce a moderate similar degree of stress when applied in the same temporal basis as in the present work [3]. Therefore, if stress had been a critical factor in our results, the PSD control animals would also have had to slhow a decrease in performance, which has not been the case. PSD animals showed a decrease in the number of intertrial crossings during the 2nd and 3rd acquisition sessions compared to the dry controls. It cannot be ruled out that in the present work, the locomotor activity changes might have influenced the performance of the subjects, although this influence does not seem to be critical, since: (1) no significant correlations were ever found between the nunaber of avoidances and the number of intertrial crossings in any group; and (2) no locomotor activity differences were found between the PSD and the PSD control groups, while their performance did significantly differ. In conclusion, a 5-h repeated pretraining PSD treatment slowed down the acquisition of a distributed shuttle box avoidance task, while having no influence
183
upon LTR. Although it cannot be ruled out that those results might be partially attributable to a decrease in locomotor activity, our results are not fully in contradiction with the hypothesis that PS previous to the training sessions might prepare the animal for subsequent learning.
Acknowledgment This research was supported by a CAICYT grant (643/84).
References [ 1] Albert, I., Cicala, G.A. and Siegel, J., The behavioral effects of REM sleep deprivation in rats, Psychophysiology, 6 (1970) 550-559. 12] Coenen, A.M.L. and Van Luijtelaar, J.L.M., Stress induced by three procedures of deprivation of paradoxical sleep, Physiol. Behav., 35 (1985) 501-504. 1-3] Coll-Andreu, M., Ayora-Mascarell,L., Trullas-Oliva,R. and Morgado-Bernal, I., Behavioral evaluation of the stress induced by the platform method for short-term paradoxical sleep deprivation in rats, Brain Res. Bull., 22 (1989) 825-828. [4] Dujardin, K., Guerrien, A. and Leconte,P., Sleep,brain activation and cognition, Physiol. Behav., 47 (1990) 1271-1278. [5] Hicks, R.A. and Paulus, M.J., Effectsof rapid eye movement sleep deprivation on the performanceof rats in a T-maze,Psychol. Rec., 23 (1973) 89-92. [6] Kovaizon, V.M. and Tsibulsky, V.L., REM sleep deprivation, stress and emotional behavior in rats, Behav. Brain Res., 14 (1984) 235-245. [7] Marti-Nicolovius,M., Portell-Cortrs, I. and Morgado Bernal, I., Improvement of shuttle-box avoidance following post-training treatment in paradoxical sleep deprivation platforms in rats, Physiol. Behav., 43 (1988) 93-98. 1"8] McGrath, M.J. and Cohen, D.B., REM sleep facilitation of adaptative waking behavior: a review of the literature, Psychol. Bull., 85 (1978) 24-57. 1"9] Murison, R., Ursin, R., Coover, G.D., Lien, W. and Ursin, H., Sleep deprivation procedure produces stomach lesions in rats, Physiol. Behav., 29 (1982) 693-694. 1,10] Ogilvie, R.D. and Broughton, R.J., Sleep deprivation and measures of emotionality in rats, Psychophysiology, 13 (1976) 249-260. [11] Oniani, T.N. and Lortkipanidze, N.D., Effectof paradoxical sleep deprivation on the learning and memory. In: T.N. Oniani (Ed.), Neurophysiology of Motivation, Memory and Sleep-Wakefulness Cycle, Metsniereba, Tbilisi, 1985, pp. 136-213.
[12] Pearlman, C.A., REM sleep and information processing: evidence from animal studies, Neurosci. Biobehav. Rev., 3 (1979) 57-68. 1"13] Plumer, S.I.,Matthews, L., Tucker, M. and Cook, T.M., The water tank technique: avoidance conditioning as a function of water level and pedestal size, Physiol. Behav., 12 (1974) 285-287. 1-14] Sagalrs, T. and Domino, E.F., Effects of stress and REM sleep deprivation on the patterns of avoidance learning and brain acetylcholine in the mouse,Psychopharmacologia, 29 (1973) 307-315. 1"15] Smith, C., Sleep states and learning: a review of the animal literature, Neurosci. Biobehav. Rev., 9 (1985) 157-168. [16] Van Hulzen,Z.J.M. and Coenen, A.M.L., Paradoxical sleep deprivation and locomotor activity in rats, Physiol. Behav., 27 (1982) 741-744. [17] Van Hulzen, Z.J.M. and Coenen, A.M.L., Effects of paradoxical sleep deprivation on two-way avoidance acquisition, Physiol. Behav., 29 (1982) 581-587.
Behavioural Brain Research 72 (1996) 181-183
Short communication
Effects of pretraining paradoxical sleep deprivation upon two-way active avoidance Agn~s Gruart-Masso 1, Roser Nadal-Alemany, Margalida Coll-Andreu, Isabel Portell-Cort~s, Margarita Marti-Nicolovius * Area de Psicobiologia, Departament de Psicologia de la Salut, Universitat Aut~noma de Barcelona, Apartat 46, 08193 Bellaterra, Barcelona, Spain Received 3 February 1995; revised 11 April 1995; accepted 12 April 1995
Abstract
In order to study whether paradoxical sleep (PS) is necessary to prepare subjects for the subsequent learning of a distributed two-way active avoidance cc~nditioning, 10 rats were subjected to 5 h of paradoxical sleep deprivation (PSD group) by means of the platform method immediately before each of 5 acquisition sessions (one daily), as well as before a long-term retention (LTR) session (14 days). Another group of rats (PSD control group; n=10) were placed on large platforms as a control for the side effects induced by PSD platforms. Rats in the dry control group (n = 10) did not receive any treatment. The number of avoidances of the PSD group was signiticantly lower on the 1st, 2nd and 3rd acquisition sessions compared to the PSD control group, and on the 2nd and 3rd sessions compared to the dry control group. PSD rats made significantly less intertrial crossings than dry controls on the 2nd and 3rd acquisition sessions, but no significant correlations were found between this variable and the number of avoidances. Therefore, o~Lrresults are not fully in contradiction with the hypothesis that PS previous to the training sessions might prepare the animal fer subsequent learning, although the influence of locomotor changes upon the performance of PSD subjects cannot be fully rejec,ted. Keywords: Pretraining rapid eye movement(REM) sleep deprivation;Two-wayactive avoidance; Learning and memory
A wide range of experimental data suggests that paradoxical sleep (PS) might be involved in learning and in memory consolidation processes [4,15]. Two basic questions have centered the interest of paradoxical sleep deprivation (PSD)experiments: (1) does PS prepare the subject for subsequent learning?; and (2) does PS facilitate the consolidation process? The latter question can be addressed in studies of post-training PSD. Studies using the pretrainJng approach are based on the hypothesis that PSD affects several factors involved in learning (i.e., neurotransmitters), so that PSD before training might impair learning dependent upon such factors. Two kinds of measures have been investigated: performance during initial exposure to the task (acquisition); and performance at some later time (retention) [123. 1Present address. Laboratorio de Neurosciencia,Facultad de Biologia, Avda Reina Mercedes, s/n, 41012 Sevilla, Spain. * Corresponding author. Fax: + 34 3 581 23 24. 0166-4328/96/$9.50© ElsevierScienceB.V. All rights reserved SSSDI 0166-4328(96)00082-8
Several studies on pretraining PSD in rats have shown detrimental effects upon the acquisition of one-way active avoidance, taste aversion, and passive avoidance [8,15], while no effects were found upon appetitive operant conditioning [ 5]. With regard to two-way active avoidance, only one work has shown detrimental effects after pretraining PSD in rats, and only when using the platform method, while no effects were found with the pendulum technique [17]. Other works have found no effects [13 or even a slight facilitatory effect upon the acquisition of shuttle-box avoidance [ 11,13 ]. With mice, deleterious effects of pretraining PSD upon two-way active avoidance have been reported only upon longterm retention, but not upon acquisition 1-14]. In summary, results regarding the influence of pretraining PSD upon shuttle-box avoidance are highly controversial. All the works studying the effects of pretraining PSD upon two-way active avoidance have been carried out on massed training (a single session consisting of a high number of trials), using a long PSD treatment adminis-
182
Agnks Gruart-Masso et al./Behavioural Brain Research 72 (1996) 181 183
tered in a single session (24-120 h), and without a previous adaptation of the animals neither to the platform method nor to the conditioning apparatus. Therefore, we designed an experiment aimed at evaluating whether PS previous to the acquisition and longterm retention (LTR) sessions of two-way active avoidance, when distributed training is used, is needed to prepare the subject for learning. To reduce the influence of the side effects induced by the PSD technique [2,3,6,9,10,16], short repeated 5-h sessions (one daily) of PSD by means of the platform method and previous sessions of adaptation to this technique have been used in the present work. Thirty naive male Wistar rats, with a mean age of 113 days (S.D.=4) and a mean weight of 441 g (S.D. = 11.9) at the beginning of the experiment, were used. In order to familiarize the subjects with the learning conditions each animal had 3 sessions (one daily) of adaptation to the shuttle-box apparatus (Campden Instruments, Ltd.), each consisting of 20 min of free ambulation. To habituate the animals to the platform method, they were also given 5 adaptation sessions (one daily), each consisting of being placed for 2 h on large platforms (16 cm diameter). Smaller platforms (7 cm diameter) were not used for adaptation to overcome the possibility that PSD during the adaptation phase might affect subsequent learning. The last 3 of those sessions were conducted on the same days as the shuttle box adaptation sessions. Forty-eight hours after the end of the adaptation sessions, subjects had 5 training sessions (10 trials each) in the two-way active avoidance apparatus, separated by 24-h intervals. The conditioned stimulus was a 80-dB tone lasting up to 3 s; the unconditioned stimulus consisted of an electrical footshock of 1 mA 30 s duration at most. A l-min intertrial interval was used. Both treatment and training sessions were conducted during the light time of the light-dark cycle. During the 5 h immediately previous to each acquisition session, animals were either placed on 7-cm platforms (PSD group; n= 10), on 16-cm platforms (PSD control group; n = 10) or were maintained in their home cage (dry control group; n = 10). The platform technique used in the present work has been described in detail elsewhere [7]. Fourteen days after the last training session, all subjects were given another 10-trial session to evaluate the level of LTR. To avoid the possibility that state-dependency would interfere with the performance of the subjects, the corresponding treatment was also administered prior to that session. As shown in Fig. 1, and confirmed by a MANOVA (polynomial c o n t r a s t : F1,27 = 13.87; P=0.001), the evolution of learning followed the expected upward tendency in all the groups. Comparison among groups for each session (MANOVA, 'simple' contrast) indicated that the number of avoidances of the PSD group was significantly lower compared to the PSD control group
ACQUSTON
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SESSIONS
Fig. 1. Effects of pretraining PSD treatment upon the number of avoidances during acquisition and LTR (14 days) of a distributed shuttle box avoidance task. Results are expressed in means (+ S.E.M.).
on the first (F1,27= 6.24; P = 0.019), second (F1.27= 5.63; P=0.025), and third (Fl,zT=6.16; P=0.020) training sessions. On the other hand, the PSD group subjects made a statistically lower number of avoidances than the dry control group on both the second (F1.27 = 6.53; P=0.017) and third (};'1,27=5.75; P=0.024) sessions. The performance of animals in the PSD control group never differed in a statistical way from that of the dry control group. No statistical differences existed, either, between any of the groups during the LTR session. Furthermore, no differences between the mean avoidances on the last acquisition session and those of the LTR session were found within any of the groups. PSD subjects showed a lower number of intertrial crossings than the dry control ones on the 2nd and 3rd acquisition sessions (MANOVA, Contrast 'Simple': Fl,ZT=4.69; P=0.039 and /1,17=7.86; P=0.009, respectively). Nevertheless, the number of intertrial crossings did not show any statistical correlations with the number of avoidances on any session and for any group. In summary, 5 repeated sessions (one daily) of 5-h pretraining PSD treatment slowed down the acquisition of a distributed two-way active avoidance task, while having no effect either upon the final learning level achieved or upon LTR. These findings agree with those of a previous work where a detrimental effect upon a massed two-way active avoidance task was found after 72 h of PSD treatment with the platform method, either simple or multiple [ 17]. Nevertheless, our results do not agree with the lack of effects found both in the abovereported work when using the pendulum technique, and in another work using the platform method [ 1]. They
Agnds Gruart-Masso et al./Behavioural Brain Research 72 (1996) 181-183
do not either agree with other papers reporting facilitatory effects upon the acquisition of the same kind of task after 9 6 h [11] and 120h [13] of PSD treatment with the platform method. In contrast, the lack of effects of pretraining PSD upon L T R is in concordance with other experiments carried out in rats [ 13,17]. Nevertheless, the possibility remains that L T R might have been affected if a lower number of acquisition sessions had been used. The discrepancies between our results and those found in other experiments might be due to methodological differences, such as the uLse of different PSD techniques (namely, platform method vs pendulum technique), of different training schedules (massed vs distributed training), or of longer PSD treatment times (from 24 to 120 h in a single session vs 5-h repeated sessions in our work). Nevertheless, additional factors have also to be taken into account, since disruptive effects were also observed in a study using massed training (50 trials) and a long PSD session ,(72 h) [17]. Another factor to be considered is the degree of PSD obtained with the platforan method. This factor is influenced by the ratio between the animal weight and the PSD platform diameter 118]. Only in the previous work reporting a deterioration of performance [17], this ratio (330 g/6.2 cm) was rather similar to that in the PSD group of the present work (441 g/7 cm). In contrast, in the other studies [1,13], (:his ratio (150-200 g/7 cm) was similar to that in our PSD control platforms (441 g/16 cm). Therefore, this variable might be critical in explaining the discrepancies among the different works. Is the disruptive effect of acquisition observed in our experiment due to the deprivation of PS or is it attributable to the side effects induced by the platform method, such as stress or locomotor activity changes? A previous experiment in our laboratory showed that both PSD and PSD control platforms induce a moderate similar degree of stress when applied in the same temporal basis as in the present work [3]. Therefore, if stress had been a critical factor in our results, the PSD control animals would also have had to slhow a decrease in performance, which has not been the case. PSD animals showed a decrease in the number of intertrial crossings during the 2nd and 3rd acquisition sessions compared to the dry controls. It cannot be ruled out that in the present work, the locomotor activity changes might have influenced the performance of the subjects, although this influence does not seem to be critical, since: (1) no significant correlations were ever found between the nunaber of avoidances and the number of intertrial crossings in any group; and (2) no locomotor activity differences were found between the PSD and the PSD control groups, while their performance did significantly differ. In conclusion, a 5-h repeated pretraining PSD treatment slowed down the acquisition of a distributed shuttle box avoidance task, while having no influence
183
upon LTR. Although it cannot be ruled out that those results might be partially attributable to a decrease in locomotor activity, our results are not fully in contradiction with the hypothesis that PS previous to the training sessions might prepare the animal for subsequent learning.
Acknowledgment This research was supported by a CAICYT grant (643/84).
References [ 1] Albert, I., Cicala, G.A. and Siegel, J., The behavioral effects of REM sleep deprivation in rats, Psychophysiology, 6 (1970) 550-559. 12] Coenen, A.M.L. and Van Luijtelaar, J.L.M., Stress induced by three procedures of deprivation of paradoxical sleep, Physiol. Behav., 35 (1985) 501-504. 1-3] Coll-Andreu, M., Ayora-Mascarell,L., Trullas-Oliva,R. and Morgado-Bernal, I., Behavioral evaluation of the stress induced by the platform method for short-term paradoxical sleep deprivation in rats, Brain Res. Bull., 22 (1989) 825-828. [4] Dujardin, K., Guerrien, A. and Leconte,P., Sleep,brain activation and cognition, Physiol. Behav., 47 (1990) 1271-1278. [5] Hicks, R.A. and Paulus, M.J., Effectsof rapid eye movement sleep deprivation on the performanceof rats in a T-maze,Psychol. Rec., 23 (1973) 89-92. [6] Kovaizon, V.M. and Tsibulsky, V.L., REM sleep deprivation, stress and emotional behavior in rats, Behav. Brain Res., 14 (1984) 235-245. [7] Marti-Nicolovius,M., Portell-Cortrs, I. and Morgado Bernal, I., Improvement of shuttle-box avoidance following post-training treatment in paradoxical sleep deprivation platforms in rats, Physiol. Behav., 43 (1988) 93-98. 1"8] McGrath, M.J. and Cohen, D.B., REM sleep facilitation of adaptative waking behavior: a review of the literature, Psychol. Bull., 85 (1978) 24-57. 1"9] Murison, R., Ursin, R., Coover, G.D., Lien, W. and Ursin, H., Sleep deprivation procedure produces stomach lesions in rats, Physiol. Behav., 29 (1982) 693-694. 1,10] Ogilvie, R.D. and Broughton, R.J., Sleep deprivation and measures of emotionality in rats, Psychophysiology, 13 (1976) 249-260. [11] Oniani, T.N. and Lortkipanidze, N.D., Effectof paradoxical sleep deprivation on the learning and memory. In: T.N. Oniani (Ed.), Neurophysiology of Motivation, Memory and Sleep-Wakefulness Cycle, Metsniereba, Tbilisi, 1985, pp. 136-213.
[12] Pearlman, C.A., REM sleep and information processing: evidence from animal studies, Neurosci. Biobehav. Rev., 3 (1979) 57-68. 1"13] Plumer, S.I.,Matthews, L., Tucker, M. and Cook, T.M., The water tank technique: avoidance conditioning as a function of water level and pedestal size, Physiol. Behav., 12 (1974) 285-287. 1-14] Sagalrs, T. and Domino, E.F., Effects of stress and REM sleep deprivation on the patterns of avoidance learning and brain acetylcholine in the mouse,Psychopharmacologia, 29 (1973) 307-315. 1"15] Smith, C., Sleep states and learning: a review of the animal literature, Neurosci. Biobehav. Rev., 9 (1985) 157-168. [16] Van Hulzen,Z.J.M. and Coenen, A.M.L., Paradoxical sleep deprivation and locomotor activity in rats, Physiol. Behav., 27 (1982) 741-744. [17] Van Hulzen, Z.J.M. and Coenen, A.M.L., Effects of paradoxical sleep deprivation on two-way avoidance acquisition, Physiol. Behav., 29 (1982) 581-587.