EFFECT OF ETHANOL ON MORPHINE STATE-DEPENDENT LEARNING IN THE MOUSE: INVOLVEMENT OF GABAERGIC, OPIOIDERGIC AND CHOLINERGIC SYSTEMS

A. Vakili1,2, K. Tayebi1,2, M. R. Jafari3, M. R. Zarrindast1,* and B. Djahanguiri1

1 Department of Pharmacology, School of Medicine, Tehran University of Medical Sciences, Tehran, 2 School of Medicine, Tehran University of Medical Sciences, Tehran and 3 Department of Pharmacology, School of Medicine, Zanjan University of Medical Sciences, Zanjan, Iran

* Author to whom correspondence should be addressed at: Department of Pharmacology, School of Medicine, Tehran University of Medical Sciences, P.O. Box 13145–784, Tehran, Iran. Tel.: +98 21 611 2801; Fax: +98 21 640 2569; E-mail: zarinmr{at}ams.ac.ir

(Received 19 February 2004; first review notified 2 April 2004; in revised form 6 May 2004; accepted 21 June 2004)


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Aims: We have studied the effect of acute administration of ethanol when it replaced morphine in step-down passive avoidance task on the test day and the effects of antagonists of GABAergic, opioidergic and cholinergic systems on ethanol actions. Methods: Morphine (5 mg/kg, s.c.) was administered as pre-training and 24 h later as pre-test drug, and the latencies were measured in mice. Ethanol (0.125, 0.25, 1 and 2 g/kg, i.p.) was administered instead of pre-test morphine. Antagonists of GABAergic (bicuculline 0.5, 1 and 2 mg/kg, i.p.), opioidergic (naloxone 0.06, 0.25 and 1 mg/kg, i.p.) and cholinergic (atropine 0.625 and 1.25 mg/kg, i.p. and mecamylamine 0.5, 1 and 2 mg/kg, i.p.) systems were co-administered with ethanol (0.25 g/kg, i.p.) on the test day. Locomotor activity was measured as well. Results: Pre-training morphine impaired the memory on the test day which was restored when the same dose of morphine was used as pre-test drug. All four doses of ethanol replaced pre-test morphine and enhanced the memory. This effect was prevented by all of the above antagonists. No significant changes were seen in the locomotor activity of the animals treated with ethanol or antagonists compared to the proper controls. Conclusions: GABAergic, endogenous opioidergic and cholinergic systems are involved in the memory recall improvement by ethanol when it replaced morphine on the test day. A review of the literature suggests other possibilities such as the release of intermediate neurotransmitters.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The measurement of step-down latency in passive avoidance has been used to study learning and memory in laboratory animals (Kameyama et al., 1986Go). The pre-training administration of morphine impaired the memory. When 24 h later the same dose of morphine was administered before testing, the memory was restored (Izquierdo and Dias, 1983Go; Bruins Slot and Colpaert, 1999Go). This is known as morphine state-dependency (morphine St-D). Several drugs have been demonstrated, in our laboratory, to replace the pre-testing effect of morphine on the restoration of memory (Khavandgar et al., 2002Go, 2003; Homayoun et al., 2003Go; Zarrindast et al., 2004Go). We report, to our knowledge for the first time, the effects of the administration of low doses of ethanol on morphine St-D in mice on the test day.

Ethanol has been shown to affect many processes involved with central nervous system functions including memory. However, when administered as a single dose, the effects of ethanol on memory depend on several factors e.g. the animal, the dose and duration of ethanol administration and the performed test. Taking together the above variables, ethanol has been reported to impair (Holloway, 1972Go; Bammer and Chesher, 1982Go; Castellano and Pavone, 1988Go; Sasaki et al., 1995Go) or to enhance memory (Mikolajczak et al., 2001Go; Prediger and Takahashi, 2003Go). Several hypotheses have been proposed to explain the acute effects of ethanol on memory in the laboratory animals. Henn et al. (1998)Go have suggested that the effect of ethanol on memory may be due to an involvement of the GABAergic system. Moreover, there is evidence suggesting that the reinforcing effects of ethanol on the memory are mediated by the endogenous opioid system (Kalant, 1977Go; Prediger and Takahashi, 2003Go) or the cholinergic system (Stancampiano et al., 2004Go).

Our preliminary results show that ethanol administration on the pretest day enhanced the memory recall in the step-down avoidance task. To explore the possible involvement of the GABAergic, endogenous opioidergic and cholinergic systems on the observed effects of ethanol, the animals were pretreated with bicuculline (GABAA antagonist), naloxone (opioid antagonist), atropine (muscarinic cholinergic antagonist) and mecamylamine (nicotinic cholinergic antagonist), respectively. The locomotor activity of the animals was studied as well.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Animals
Male albino NMRI mice weighing 20–30 g were used. The animals were kept in an animal house with a 12-h light/12-h dark cycle and controlled temperature (22 ± 2°C). They were given food and water ad libitum. They were housed in groups of 10 in Plexiglas animal cages. Each animal was used once. All procedures were carried out in accordance with institutional guidelines for animal care and use.

Apparatus
The passive avoidance apparatus consisted of a wooden box (30 x 30 x 40 cm high) with a steel-rod floor (29 parallel rods, 0.3 cm in diameter set 1 cm apart). A wooden platform (4 x 4 x 4 cm) was set in the center of the grid floor. Intermittent electric shocks (1 Hz, 0.5 s and 50 V DC) were delivered to the grid floor by an insulated stimulator. Locomotor activity was measured with an activity meter, Animex, type S (LKB Farrad). The locomotor activity meter had a Plexiglas box (40 x 25 x 15 cm high).

Passive avoidance testing
Each mouse was gently placed on the wooden platform. When the mouse stepped down from the platform and placed its paws on the grid floor, intermittent electric shocks (1 Hz, 0.5 s and 50 V DC) were delivered for 15 s (Hiramatsu and Kameyama, 1995Go). This training procedure was carried out between 10:00 a.m. and 3:00 p.m.

Memory testing was performed 24 h later, in which each mouse was placed on the platform again and the step-down latency measured, in the absence of electric foot shocks, with a step-watch as passive avoidance behaviour. An upper cut-off of 300 s was set. The retention test was also carried out between 10:00 a.m. and 3:00 p.m. Saline, morphine and ethanol were injected 30 min before training or testing. This interval was set at 15 min for bicuculline, atropine and mecamylamine, and 5 min for naloxone.

Locomotion study
For locomotor activity study, each animal was placed in a plastic cage for 30 min to acclimatize to the environment before testing. Immediately after drug injection, animals were returned to the cage for measuring the locomotion. Counts were made for a period of 30 min.

Drug treatment
Ten animals were used to examine the effect of each dose of the tested drug. In experiments in which the animals received two or three saline or vehicle injections, the doses were adjusted in a way for each animal to receive a volume of at most 10 ml/kg.

In experiment 1, 10 animals received saline before training and testing. Other animals received 5 mg/kg morphine as pre-training treatment. These animals were treated 24 h later as pre-test treatment with saline, three different doses of morphine (0.5, 1 and 5 mg/kg), four different doses of ethanol (0.125, 0.25, 1 and 2 g/kg) or a combination of morphine (0.5 mg/kg) + ethanol (0.125 g/kg). We have also studied the effect of the above mentioned doses of morphine or ethanol on pre-training saline-treated mice.

In experiment 2, animals received morphine (5 mg/kg) as pre-training treatment. These animals received as pre-test treatment three different doses of bicuculline (0.5, 1 and 2 mg/kg), three different doses of naloxone (0.06, 0.25 and 1 mg/kg), two different doses of atropine (0.625 and 1.25 mg/kg) or three different doses of mecamylamine (0.5, 1 and 2 mg/kg). The same animals received ethanol at a dose of 0.25 g/kg or saline. In Fig. 2, data of the effects of pre-test treatment with saline, morphine (5 mg/kg) and ethanol (0.25 g/kg) from Fig. 1, are illustrated for comparison of the effects of bicuculline, naloxone, atropine and mecamylamine on the improvement of memory by ethanol.



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Fig. 2. The effect of pre-test administration of three different doses of bicuculline, three different doses of naloxone, two different doses of atropine and three different doses of mecamylamine co-administered with ethanol following pre-training administration of morphine on step-down latency compared to pre-test administration of ethanol alone. Each value represents the median and quartiles of 10 animals. *Significantly different (P < 0.05) from pre-test ethanol treated animals.

 


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Fig. 1. The effect of pre-test administration of different doses of morphine, ethanol and morphine + ethanol following pre-training morphine on the step-down latencies compared to pre-training morphine and pre-test saline group. Ten animals received saline 30 min before training and 30 min before testing. Other animals were trained 30 min after morphine administration and 24 h later were tested 30 min after saline (morphine–saline treated animals), three different doses of morphine, four different doses of ethanol and morphine + ethanol. Each value represents the median and quartiles of 10 animals. *, **Significantly different (P < 0.05) from morphine–saline treated animals.

 
Drugs
Morphine sulfate was purchased from Temad (Iran). Ethanol (absolute) was purchased from Merck Co. (Germany). Bicuculline and mecamylamine were purchased from Sigma (England). Naloxone hydrochloride was a gift from Tolid-daru (Iran). Atropine sulphate was a gift from Sina-Daru (Iran). Drugs were dissolved in 0.9% saline. Drugs were administrated intraperitoneally (i.p.) or subcutaneously (s.c.) in a volume of at most 10 ml/kg.

Data analysis
The retention latencies were expressed as the median and interquartile range. Because of the large individual variations, the data were analyzed by using Kruskal–Wallis non-parametric one-way analysis of variance (ANOVA) followed by 2-tailed Mann–Whitney's U-test followed by Bonferoni's correction for the paired comparisons. For locomotor activity the counts were expressed as the mean ± standard errors. The data were analyzed by analysis of variance (ANOVA) followed by Tukey post hoc. In all statistical evaluations P < 0.05 was considered as the criterion for statistical significance.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Effect of the drugs on the memory of mice
Results are summarized in Figs 1 and 2.

The injection of morphine at a dose of 5 mg/kg (s.c.) on the training day impaired memory retention. When the drug (0.5, 1 and 5 mg/kg) was injected 30 min before testing, the impaired memory was reversed: P = 0.052, 0.0036 and 0.004 for 0.5, 1 and 5 mg/kg morphine respectively, compared with the saline injected group (Morphine State-Dependency). The best effect was observed with 5 mg/kg of morphine.

Ethanol produced no change in training-day saline-treated animals (data not shown), but reversed the memory impairing effect of morphine (P = 0.015, 0.008, 0.0003 and 0.009 for 0.125, 0.25, 1 and 2 g/kg ethanol respectively). The co-administration of 0.125 g/kg ethanol with 0.5 mg/kg morphine did not increase the memory recall compared with that of the same dose of morphine (P = 0.531).

Bicuculline, naloxone, atropine and mecamylamine did not change the memory retention in saline or morphine treated animals (data not shown).

The administration of bicuculline after ethanol (0.25 g/kg) prevented the memory recall by ethanol (P = 0.238, 0.042 and 0.392 for 0.5, 1 and 2 mg/kg bicuculline, respectively). The effect of bicuculline was significant only at 1 mg/kg.

Naloxone prevented the ethanol-induced memory retrieval (P = 0.103, 0.012 and 0.024 for 0.06, 0.25 and 1 mg/kg, respectively). The effect of naloxone was significant at the doses of 0.25 and 1 mg/kg.

When atropine was injected after ethanol (0.25 g/kg), it prevented significantly the memory recall by ethanol (P = 0.038 and 0.036 for 0.625 and 1.25 mg/kg, respectively).

When mecamylamine was injected after ethanol (0.25 g/kg) it prevented the memory recall by ethanol (P = 0.024, 0.02 and 0.144 for 0.5, 1 and 2 mg/kg, respectively). The effect of mecamylamine was significant at the doses of 0.5 and 1 mg/kg.

Effect of the drugs on the locomotor activity of mice
Ethanol with the doses used in the present experiment showed no effect on locomotor activity either by itself or in combination with morphine.

The same results were obtained with different doses of bicuculline. When the drug was used at a dose of 0.5 mg/kg in combination with ethanol (0.25 g/kg), it significantly increased the locomotor activity (P = 0.032).

Naloxone, atropine and mecamylamine, at the doses used in the present experiment showed no effect on the locomotor activity either alone or in combination with a fixed dose of morphine (0.5 mg/kg) or ethanol (0.25 g/kg).


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Several drugs have been reported to improve memory recall when replacing the administration of morphine on the test day in step-down passive avoidance task (see Introduction).

Acute ethanol administration has been reported to have state-dependent effects on conditioned avoidance responding (Crow, 1966Go; Overton, 1966Go). Moreover, the independent effects of ethanol on memory in man and laboratory animals have also been studied in detail (Fadda and Rossetti, 1998Go; Ryabinin, 1998Go).

There were two findings in the present report. First, the acute administration of different doses of ethanol (0.125, 0.25, 1 and 2 g/kg) improved morphine-induced memory impairment in a step-down passive avoidance task when they replaced morphine on the test day. Second, drugs which antagonized GABAergic, endogenous opioidergic or cholinergic systems (but not all doses of each antagonist) prevented the improving action of ethanol on memory (see Results).

Reports on the effects of ethanol administration on memory processes in laboratory animals are contradictory. Ethanol administration has been widely reported to impair memory in man and laboratory animals (Acheson et al., 2001Go). Passive avoidance procedures have also shown a decrease in memory retention following the administration of ethanol (Holloway, 1972Go; Bammer and Chesher, 1982Go; Castellano and Pavone, 1988Go; Sasaki et al., 1995Go). Contrary to the above findings Mikolajczak et al. (2001)Go and Prediger and Takahashi (2003)Go have demonstrated that under some experimental conditions ethanol facilitates short-term memory in laboratory animals. Recently Stancampiano et al. (2004)Go have demonstrated that ethanol could have a biphasic action on the cholinergic system to cause deficit or to exert facilitator effects on memory. The same authors suggested that increased cholinergic transmission may contribute to the improving effects of ethanol on memory.

In the present study bicuculline, a GABAA receptor antagonist, prevented the improving effect of ethanol on memory recall. Several behavioural effects of ethanol are enhanced by GABAA receptor agonist and attenuated by antagonists or inverse agonists (Lister et al., 1991). Despite the plethora of data linking ethanol action to GABAA receptors, in vivo studies examining a direct interaction between these two are inconclusive (Morrow et al., 2001Go). Although initially the effects of ethanol on memory were considered to be hippocampus-independent, recent studies have shown that the hippocampus is involved in passive avoidance learning (for review, see Ryabinin, 1998Go).

There is considerable evidence that the reinforcing effects of ethanol on memory are mediated by the endogenous opioid system and that some of the behavioural and pharmacological effects of ethanol are similar to those produced by opioids (Kalant, 1977Go; Prediger and Takahashi, 2003Go). The fact that opioid antagonist reversed the effects of ethanol on the CNS also suggested an involvement of endogenous opioid peptides in the mechanism of action of this substance (Gianoulakis, 1993Go). Taken together, it is unlikely that ethanol has a dramatic effect on opioid receptor binding. Our results showed that naloxone prevented the improving effect of ethanol on memory recall. According to Prunell et al. (1987)Go both the CNS stimulant and depressant effects of ethanol in rats have been antagonized by naloxone. However, other investigators suggested that the effects of naloxone are probably due to a non-specific analeptic action rather than blockade of opioid receptors (Saddler et al., 1985Go).

The activity of the cholinergic septo-hippocampal pathway plays a major role in the memory processes and is a possible target for the acute effect of ethanol (Cocco et al., 2002Go). Impairment of the hippocampal cholinergic system has only so far been observed after long term ethanol administration (Henn et al., 1998Go). Higher ethanol doses decrease cortical cholinergic functions and lower doses stimulate hippocampal ACh release (Henn et al., 1998Go). This is in agreement with the results of the present experiment in which both atropine and mecamylamine prevented the improving effect of ethanol on memory recall.

Apart from the involvement of GABAergic, endogenous opioidergic and cholinergic systems in the mechanism of action of ethanol on memory improvement, Davis and Walsh (1970)Go have suggested that ethanol metabolism in the body may result in the formation of morphine-like alkaloids (tetrahydropapaveroline) which may replace the effect of morphine on the test day to improve memory recall.

Moreover, Hoffman et al. (1990)Go have reviewed the part played by NMDA receptors on certain acute behavioural effects of ethanol and have concluded that these receptors may be involved in the effects of ethanol on memory. Nakagawa and Iwasaki (1996)Go have investigated the part played by NMDA receptors in state-dependent learning (SDL) induced by ethanol in rats. They have concluded that NMDA receptor complex may not be involved in ethanol SDL. Napiorkowska-Pawlak et al. (2000)Go have shown that dizacilpine (MK-801), a non competitive NMDA receptor antagonist, failed to change the amnesiac effect of ethanol in a passive avoidance task in mice. The above data do not support the hypothesis concerning the involvement of NMDA receptors in the effects of ethanol on memory.

The doses of ethanol used in the present study did not show any sedative effect, which was assessed by measuring locomotor activity. In fact, with the exception of one group of animals which were treated with bicuculline (0.5 mg/kg) + ethanol (0.25 g/kg), there were no significant changes in the locomotor activity of other groups of animals compared to the proper controls. The above results suggest that the locomotor activity and memory recall of the step-down passive avoidance task are not inter-related. This hypothesis is in agreement with the results reported by other investigators. Sanberg and Fibiger (1979)Go have demonstrated that oral administration of taurine resulted in the impairment in retention of a step-down passive avoidance task in rats without changes on spontaneous locomotor activity. McNamara et al. (1995)Go have reported that treatment with (+/–)3,4-methylenedioxymethamphetamine (MDMA) increased locomotor activity without a significant change in step-down passive avoidance behaviour in rats. Vianna et al. (2000)Go have studied the involvement of protein kinase C isoforms on memory retrieval and found it unrelated to locomotor activity or anxiety level of rats. Barros et al. (2002)Go have studied the effects of bupropion and sertraline on memory retrieval and found it unrelated to locomotor activity as well. Experiments with ethanol also failed to show a direct relationship between locomotor activity and memory in laboratory animals (McMillen et al., 1998Go; Prediger and Takahashi, 2003Go).

In conclusion, single injection of different doses of ethanol, when they replaced morphine on the test day, improved the impaired memory in step-down passive avoidance task. In the present study, blockade of GABAergic, endogenous opioidergic and cholinergic systems prevented this effect of ethanol, which is suggestive of the involvement of the above systems in the effects of ethanol on memory.

A review of the literature suggests other possibilities such as modulation of the release of intermediate neurotransmitters by ethanol. Studies concerning the effect of ethanol as pre-training treatment on memory, the use of different timing between ethanol administration and the test and the effects of chronic ethanol administration seem to be of interest.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Acheson, S. K., Ross, E. L. and Swartzwelder, H. S. (2001) Age-independent and dose-response effects of ethanol on spatial memory in rats. Alcohol 23, 167–175.[CrossRef][ISI][Medline]

Bammer, G. and Chesher, G. B. (1982) An analysis of some effects of ethanol on performance in a passive avoidance task. Psychopharmacology (Berlin) 77, 66–73.[ISI][Medline]

Barros, D. M., Izquierdo, L. A., Medina, J. H. and Izquierdo, I. (2002) Bupropion and sertraline enhance retrieval of recent and remote long-term memory in rats. Behavioural Pharmacology 13, 215–220.[ISI][Medline]

Bruins Slot, L. A. and Colpaert, F. C. (1999) Opiate state of memory: receptor mechanisms. Journal of Neuroscience 19, 10520–10529.[Abstract/Free Full Text]

Castellano, C. and Pavone, F. (1988) Effects of ethanol on passive avoidance behaviour in the mouse: involvement of GABAergic mechanisms. Pharmacology Biochemistry and Behaviour 29, 321–324.[CrossRef][ISI][Medline]

Cocco, S., Diaz, G., Stancampiano, R., Diana, A., Carta, M., Curreli, R., Sarais, L. and Fadda, F. (2002) Vitamin A deficiency produces spatial learning and memory impairment in rats. Neuroscience 115, 475–482.[CrossRef][ISI][Medline]

Crow, L. T. (1966) Effects of alcohol on conditioned avoidance responding. Physiology and Behaviour 1, 89–91.[CrossRef][ISI]

Davis, V. E. and Walsh, M. J. (1970) Alcohol addiction and tetrahydropapaveroline. Science 169, 1105–1106.[ISI][Medline]

Fadda, F. and Rossetti, Z. L. (1998) Chronic ethanol consumption: from neuroadaptation to neurodegeneration. Progress in Neurobiology 56, 385–431.[CrossRef][ISI][Medline]

Gianoulakis, C. (1993) Endogenous opioids and excessive alcohol consumption. Journal of Psychiatry and Neuroscience 18, 148–156.[ISI][Medline]

Henn, C., Klein, J. and Löffelholz, K. (1998) Stimulatory influence of ethanol on the septohippocampal cholinergic pathway. A role for GABA receptors? Journal of Physiology (Paris) 92, 439–440.[CrossRef]

Hiramatsu, M. and Kameyama, T. (1995) Effects of dynorphine A-(1–13) on carbon monoxide-induced delayed amnesia in mice studied in step-down type passive avoidance task. European Journal of Pharmacology 282, 185–191.[CrossRef][ISI][Medline]

Hoffman, P. L., Rabe, C. S., Grant, K. A., Valverius, P., Hudspith, M. and Tabakoff, B. (1990) Ethanol and the NMDA receptor. Alcohol 7, 229–231.[CrossRef][ISI][Medline]

Holloway, F. A. (1972) State-dependent effects of ethanol on active and passive avoidance learning. Psychopharmacologia 25, 238–261.

Homayoun, H., Khavandgar, S. and Zarrindast, M. R. (2003) Morphine state-dependent learning: interactions with alpha2-adrenoceptors and acute stress. Behavioural Pharmacology 14, 41–48.[ISI][Medline]

Izquierdo, I. and Dias, R. D. (1983) Effect of ACTH, epinephrine, beta-endorphine, naloxone, and of the combination of naloxone or beta-endorphine with ACTH or epinephrine on memory consolidation. Psychoneuroendocrinology 8, 81–87.[CrossRef][ISI][Medline]

Kalant, H. (1977) Comparative aspects of tolerance to, and dependence on, alcohol, barbiturates and opiates. Advances in Experimental Medicine and Biology 85B, 169–186.[Medline]

Kameyama, T., Nabeshima, T. and Kozawa, T. (1986) Step-down-type passive avoidance- and escape-learning method. Suitability for experimental amnesia models. Journal of Pharmacological Methods 16, 39–52.[CrossRef][ISI][Medline]

Khavandgar, S., Homayoun, H., Torkaman-Boutorabi, A. and Zarrindast, M. R. (2002) The effects of adenosine receptor agonists and antagonists on morphine state-dependent memory of passive avoidance. Neurobiology of Learning and Memory 78, 390–405.[CrossRef][ISI][Medline]

Khavandgar, S., Homayoun, H. and Zarrindast, M. R. (2003) The effect of L-NAME and L-arginine on impairment of memory formation and state-dependent learning induced by morphine in mice. Psychopharmacology (Berlin) 167, 291–296.[ISI][Medline]

Lister, R. G. and Linnoila, M. (1991) Alcohol, the chloride ionophore and endogenous ligands for benzodiazepine receptors. Neuropharmacology 30, 1435–1440.[ISI][Medline]

McMillen, B. A., Means, L. W. and Matthews, J. N. (1998) Comparison of the alcohol-preferring P rat to the Wistar rat in behavioural tests of impulsivity and anxiety. Physiology of Behaviour 63, 371–375.[CrossRef]

McNamara, M. G., Kelly, J. P. and Leonard, B. E. (1995) Some behavioural and neurochemical aspects of subacute (+/–)3.4-methylenedioxyamphetamine administration in rats. Pharmacology Biochemistry and Behaviour 52, 479–484.[CrossRef][ISI][Medline]

Mikolajczak, P., Okulicz-Kozaryn, I., Nowaczyk, M. and Kaminska, E. (2001) Ethanol facilitation of short-term memory in adult rats with a disturbed circadian cycle. Alcohol and Alcoholism 36, 292–297.[Abstract/Free Full Text]

Morrow, A. L., Van Doren, M. J., Penland, S. N. and Matthews, D. B. (2001) The role of GABAergic neuroactive steroids in ethanol action, tolerance and dependence. Brain Research Review 37, 98–109.[ISI][Medline]

Nakagawa, Y. and Iwasaki, T. (1996) Ethanol-induced state-dependent learning is mediated by 5-hydroxytryptamine3 receptors but not by N-methyl-D-aspartate receptor complex. Brain Research 706, 227–232.[CrossRef][ISI][Medline]

Napiorkowska-Pawlak, D., Malinowska, B., Pawlak, R., Buczko, W. and Gothert, M. (2000) Attenuation of the acute amnestic effect of ethanol by ifenprodil: comparison with ondansetron and dizocilpine. Fundamentals Clinical Pharmacology 14, 125–131.

Overton, D. A. (1966) State-dependent learning produced by depressant and atropine-like drugs. Psychopharmacologia 10, 6–31.

Prediger, R. D. and Takahashi, R. N. (2003) Ethanol improves short-term social memory in rats. Involvement of opioid and muscarinic receptors. European Journal of Pharmacology 462, 115–123.[CrossRef][ISI][Medline]

Prunell, M., Boada, J., Feria, M. and Benitez, M. A. (1987) Antagonism of the stimulant and depressant effects of ethanol in rats by naloxone. Psychopharmacology (Berlin) 92, 215–218.[ISI][Medline]

Ryabinin, A. E. (1998) Role of hippocampus in alcohol-induced memory impairment: implications from behavioural and immediate early gene studies. Psychopharmacology (Berlin) 139, 34–43.[CrossRef][ISI][Medline]

Saddler, J. M., James, M. F. and Harington, A. P. (1985) Naloxone does not reverse ethanol analgesia in man. Clinical and Experimental Pharmacology and Physiology 12, 359–364.[ISI][Medline]

Sanberg, P. R. and Fibiger, H. C. (1979) Impaired acquisition and retention of a passive avoidance response after chronic ingestion of taurine. Psychopharmacology (Berlin) 62, 97–99.[ISI][Medline]

Sasaki, H., Matsuzaki, Y., Nakagawa, T., Arai. H., Yamama, M., Sekizawa, K., Ikarashi, Y. and Maruyama, Y. (1995) Cognitive function in rats with alcohol ingestion. Pharmacology Biochemistry and Behaviour 52, 845–848.[CrossRef][ISI][Medline]

Stancampiano, R., Carta, M., Cocco, S., Curreli, R., Rossetti, Z. L. and Fadda, F. (2004) Biphasic effects of ethanol on acetylcholine release in the rat prefrontal cortex. Brain Research 997, 128–132.[CrossRef][ISI][Medline]

Vianna, M. R., Barros, D. M., Silva, T., Choi, H., Madche, C., Rodrigues, C., Medina, J. H. and Izquierdo, I. (2000) Pharmacological demonstration of the differential involvement of protein kinase C isoforms in short- and long-term memory formation and retrieval of one-trial avoidance in rats. Psychopharmacology (Berlin) 150, 77–84.[CrossRef][ISI][Medline]

Zarrindast, M. R., Jafari, M. R., Ahmadi, S. and Djahanguiri, B. (2004) Influence of central administration ATP-dependent K+ channel on morphine state-dependent memory of passive avoidance. European Journal of Pharmacology 487, 143–148.[CrossRef][ISI][Medline]





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