Department of Pharmacology, K. Marcinkowski University of Medical Sciences in Poznan, Fredry 10, 61-701 Poznan, Poland
Received 5 June 2000; in revised form 29 December 2000; accepted 24 January 2001
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ABSTRACT |
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INTRODUCTION |
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One of the tests used for research on memory processes and learning processes in experimental animals is the social memory test (Thor and Holloway, 1982; Dantzer et al., 1987
; Perio et al., 1989
; Popik et al., 1992
; Benelli et al., 1995
; Griffin and Taylor, 1995
; Prast et al., 1996
; Kelly and Tran, 1997
; Argyriou et al., 1998
; Popik and van Ree, 1998
; Reid et al., 1999
; Kogan et al., 2000
). This test is based on the ability of animals to discriminate other animals by following chemosensory cues, which are the primary stimuli permitting such discrimination (Carr et al., 1976
; Thor and Holloway, 1982
). It can be assumed that this memory takes the form of short-term memory, strictly related to sensory memory (Dantzer et al., 1987
). It was also confirmed that this social behaviour (interest towards the young rat expressed by the adult rat) is not a type of behaviour conditioned by instincts, because rats behave in this way when they come into contact not only directly with a young rat but also with its urine (Sawyer et al., 1984
). Therefore, the introduction of the social memory test, being completely free of external enhancing stimuli, to the research on the memory of chronically EtOH-treated animals, should allow for better assessment of some cognitive processes in animals.
It is well known that one criterion for an animal model of alcohol dependence is the voluntary ingestion of ethanol (Lester and Freed, 1973). In normal populations of experimental animals, a group of EtOH preferring animals can be distinguished (Hammoumi et al., 1997
). In our previous research on different aspects of EtOH action, animals were first forced to consume ethanol and their EtOH preference was then defined by selecting preferring animals (Mikolajczak et al., 1999
). However, having adopted this method, we obtained a relatively small ratio (1012%) of preferring animals. Because it is known that disruption of the circadian cycle of experimental animals results in higher ratios of preferring animals (Geller, 1971
; Blum et al., 1989
; Lin and Hubbard, 1994
), we placed animals for 24 h in completely dark compartments, throughout the whole duration of the experiment (12 weeks). This yielded higher ratios of preferring animals (24%), compared to only 10% of rats kept in a normal circadian cycle (12 h/12 h) (P. Mikolajczak et al., unpublished data).
It is known that administration of EtOH to rats during pre- and postnatal periods results in impairment of social memory after the animals have reached adulthood (Kelly and Tran, 1997; Reid et al., 1999
). However, to our knowledge, there is no information on the effect of alcohol treatment on this type of memory in adult rats, so it seemed interesting to examine the effect of chronic EtOH (3 months) treatment on social recognition task performances in adult rats, selected on the basis of their preference for EtOH and kept on a 24-h dark cycle.
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MATERIALS AND METHODS |
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Additionally, for comparative purposes, throughout the whole period of chronic ethanol treatment, two EtOH-naive control groups of animals received only tap water: (3) with DCC (CD, n = 16); (4) with normal circadian cycle [kept on a reversed 12 h/12 h night/day cycle (lights on 19.007.00: CN, n = 15)].
There were no statistically significant differences in daily total fluid intake (ml ± SD) between all investigated animals [PRF, 35.0 ± 2.6; NPF, 33.5 ± 1.9; CD, 30.3 ± 1.5; CN, 32.8 ± 1.4; one-way analysis of variance (ANOVA): F(3,64) = 1.05, P > 0.1]. Throughout the process of chronic alcohol treatment all the animals had free access to standard laboratory food [Labofeed B (LSM); Feeds and Concentrates Production Plant, Poland, PN-ISO 9001:1996]. The average body weights (g ± SD) of animals (5-month-old) after the preference period were as follows: PRF, 418 ± 10; NPF, 425 ± 11; CD, 423 ± 11; CN, 449 ± 10. There were no statistical differences in the body mass of rats [one-way ANOVA F(3,64) = 1.44, P > 0.1].
Effect on spontaneous locomotor activity: the actimeter
Locomotor activity was conducted using the PAN licensed activity meter (Poland) by placing animals in the centre of the apparatus and recording their activity by electromechanical counters (Mikolajczak et al., 1999). The data were expressed as signals corresponding to spontaneous movements during 5 min. The experiments assessing the sedative activity were conducted after the preference study period between 09.00 and 15.00 in a dimly illuminated, soundproof room.
Social memory test
After the preference period and after assessment of locomotor activity, all groups of rats (PRF, NPF, CD, CN) were presented with social memory paradigms. Social memory paradigms based on olfactory recognition (Thor and Holloway, 1982; Sawyer et al., 1984
) which allowed the measurement of short-term memory conditions with short-term (STR paradigm) or long-term (LTR paradigm) recognition procedures were used in this study (Thor and Holloway, 1982
; Dantzer et al., 1987
; Griffin and Taylor, 1995
; Taylor et al., 1999
). Every adult rat was investigated through 3 consecutive days. Briefly, an adult rat was presented to a juvenile (~30 days old, 50 g) male rat (social stimuli) for 5 min and total social-investigatory behaviour (defined as being proximally orientated to juvenile rat (JR) or having direct contact while sniffing, following, nosing, grooming, pawing or generally inspecting any body surface of the juvenile by the adult) was measured with a hand-held cumulative timer to the nearest 0.1 s (T1). Next, after 30 min (STR paradigm) the same procedure with the same juvenile rat (known JR) was repeated (T2; day 1). The next day, for evaluation of non-specific effects of the STR paradigm, an unknown new juvenile (unknown JR) was exposed to the same adult rat during a second exposure (T2; day 2). On day 3, during T1 and T2, the same juvenile rat (known JR) was used as a social stimulus, but the inter-exposure interval was 120 min (LTR paradigm). Test values are expressed as the ratio of time spent on investigation during T2 divided by T1 (ratio of investigation duration: RID) (Prast et al., 1996
; Argyriou et al., 1998
). Any aggressive behaviour between animals (i.e. biting, kicking and fighting) was considered an immediate cause for terminating the experiment and excluding the data from the analysis.
All social investigations were conducted in home cages of adult rats between 09.00 and 15.00 in a dimly illuminated, soundproof room.
After every behavioural experiment, the EtOH-treated animals had free access to food, water and EtOH; in the case of control rats food and water were freely available.
Statistical analysis
The results obtained were expressed as the arithmetic means ± SEM. The statistical assessment of the EtOH effects kept in DCC were carried out using one-way ANOVA on locomotor activity or social investigations of the three different groups of rats (PRF, NPF and CD) followed by the least significance difference (LSD) test, when values of ANOVA reached P 0.05. ANOVA with replication was used for the assessment of specificity of the STR procedure by comparison of the results of PRF, NPF and CD groups after known JR vs unknown JR presentation as the repeated measure. The statistical analysis of DCC effect (CD vs CN) on locomotor activity or social memory was carried out by using one-way ANOVA.
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RESULTS |
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DISCUSSION |
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With respect to EtOH-drinking pattern and variations in body weight of the investigated rats, there were no statistically significant differences in daily total fluid intake and body weight among all investigated animals. Therefore, it can be concluded that the animals used in our study were not dehydrated and probably not undernourished. However, in the model of experimental alcoholism that we have adopted, we obtained two groups of rats differing in voluntary EtOH intake. We believe that the alcohol intake observed in our PRF group (7.3 ± 0.3 g/kg/day) is in agreement with the dose postulated to obtain dependence during chronic treatment in rats (~7 g/kg/day) (Hammoumi et al., 1997). Moreover, these PRF rats differ from NPF in some EtOH-induced behavioural paradigms such as in their period of EtOH-induced sleep-time (Mikolajczak et al., 1995
).
It has to be emphasized that the sedative component of action of EtOH can be omitted in this study. As far as the locomotor activities are concerned, there were no statistically significant differences between the analysed groups of rats (Fig. 1), which is in agreement with observations by others (McMillen et al., 1998
). It is also possible to conclude that, probably because of the continuous availability of EtOH during the experiments, there were few, if any, withdrawal symptoms influencing the rats' activity. Moreover, because it is known that EtOH-withdrawn rats show an impairment of their cognitive performances (Lukoyanov et al., 1999
), probably associated with excitotoxicity of increased glutamatergic transmission (Fadda and Rosetti, 1998), the presence of the withdrawal state in our EtOH-treated rats can also be excluded on account of their responses in our paradigms.
According to other researches (Arletti et al., 1997; Argyriou et al., 1998
; Popik and van Ree, 1998
), assessment of non-specific influences, such as impairment of alertness, was only performed by exposing an unknown JR rat to the adult rats in the case of the STR paradigm, when significantly diminished RIDs in EtOH-treated animals were found. Therefore, the elimination of any non-specific action in the LTR procedure was not necessary, because there were no statistical differences between all investigated groups.
The observation that the recognition time for the STR paradigm was shortened by chronic EtOH treatment shows that ethanol in some conditions leads to facilitation of short-term memory (Figs 2 and 3). This is in agreement with the observations that, in some EtOH-treatment protocols, long-term EtOH intake does not lead to cognitive impairment (Arendt et al., 1989
; Steigerwald and Miller, 1997
; Lukoyanov et al., 1999
). It seems that, under certain conditions (820 weeks of EtOH treatment in some studies), the performances of some learning and memory tasks may sometimes be transiently enhanced by chronic exposure to EtOH (Blokland et al., 1993
; Steigerwald and Miller, 1997
). It is known that, depending on dose and task requirements, EtOH can facilitate or impair cognitive functions and this dichotomy can be accounted for by ETOH's suppression of behavioural variability and processing of incidental stimuli (Devenport and Merriman, 1983
; McKinzie et al., 1994
). It seems that the effect of context and conditions of the stimuli used in different learning and memory tests may be responsible for obtaining either facilitation or impairment of some cognitive functions (Devenport and Merriman, 1983
). However, the assessment of learning and memory differences between rodent lines selected for high- and low-volitional intake of EtOH are still under investigation (Salimov, 1999
). It was postulated that selectively bred lines of rats for alcohol preference differ in many of their behavioural patterns (Overstreet et al., 1997
; McMillen et al., 1998
; Salimov, 1999
). For example, it was shown that positive (produced by appetitive training) or aversive (produced by aversive training) conditioning procedures alter the learning ability of preferring and non-preferring rats in an opposing manner using a signalled bar-pressing task (Blankenship et al., 1998
). However, in our study, there were no differences between PRF and NPF animals in social memory tests reported in the STR or LTR procedure. One of the explanations for the lack of differences may be due to the fact that, on applying the social memory test, neither aversive nor rewarding stimuli are used as cues for conditioning. It is probably true that this test, being completely void of external enhancing stimuli, utilizes the ability of the animals to discriminate other animals through chemosensory cues, which are the primary stimuli that permit such discrimination (Carr et al., 1976
; Thor and Holloway, 1982
). Therefore, the introduction of the social memory test to research on the memory of chronically EtOH-treated animals should allow for better assessment of some cognitive processes in animals. From the experiments that have been performed and which permitted the localization of brain structures involved in the social memory phenomenon (Letty et al., 1995
), it follows that the most significant role is attributed to the amygdala, and it seems reasonable to speculate that this part of the brain is not affected by EtOH in PRF and NPF rats.
On the basis of our data, it is difficult to explain whether and how the DCC is involved in the short-term memory in PRF and NPF animals. Numerous reports have revealed a relationship between chronic EtOH intake and dysregulation in the circadian patterns of several physiological systems (Sturtevant and Garber, 1988; Hyytia and Sinclair, 1990
; Madeira et al., 1997
; Baird et al., 1998
; Rajakrishnan et al., 1999
). As mentioned earlier, total darkness developed a propensity to drink EtOH (Geller, 1971
; Sinclair and Geller, 1972
; Lin and Hubbard, 1994
), and repeated photoperiod phase shifting led to increase of voluntary EtOH intake in animals (Gauvin et al., 1997
). Indirect involvement of alteration of circadian rhythm in learning and memory processes has been postulated (Moore and Sphe, 1993
); on the other hand, in view of the important role of the pineal gland in EtOH preference (Geller, 1971
; Sinclair and Geller, 1972
; Blum et al., 1989
), the circadian-sensitive neuronal elements (such as pineal gland and suprachiasmatic nucleus) may be involved in changes in cognitive function of EtOH-treated animals. However, there are no significant differences between RID values of CN and CD animals using the STR or LTR procedures; this means that the DCC does not alter short-term memory in EtOH-naive rats. Moreover, since PRF and NPF animals did not differ in the social memory test, the inter-relationships between EtOH preference, DCC and short-term memory in rats are therefore difficult to assess from this study, but the eventual contribution of DCC in the results of social memory in EtOH-treated rats cannot be excluded.
In conclusion, our results confirm the hypothesis that, under some conditions, probably when the toxic effects of EtOH are not as yet observable, EtOH may express a positive influence, especially on short-term memory of adult rats; this corresponds with some data for humans (Dufouil et al., 1997). From our data it is difficult to explain these observations directly. In this study, chronic administration of EtOH was performed on animals commonly regarded as adults (the 8th week of life) and this may be why the adopted procedure did not result in negative effects of EtOH on the STR paradigm in both groups of chronically EtOH-treated animals.
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FOOTNOTES |
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REFERENCES |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Argyriou, A., Prast, H. and Philippu, A. (1998) Melatonin facilitates short-term memory. European Journal of Pharmacology 349, 159162.[ISI][Medline]
Arletti, R., Benelli, A., Cavazzuti, E. and Bertolini, A. (1997) Galantide improves social memory in rats. Pharmacological Research 35, 317319.[ISI][Medline]
Baird, T. J., Briscoe, R. J., Vallett, M., Vanecek, S. A., Holloway, F. A. and Gauvin, D. V. (1998) Phase-response curve for ethanol: alterations in circadian rhythms of temperature and activity in rats. Pharmacology, Biochemistry and Behavior 61, 303315.[ISI][Medline]
Benelli, A., Bertolini, A., Poggioli, R., Menozzi, B., Basaglia, R. and Arletti, R. (1995) Polymodal doseresponse curve for oxytocin in the social recognition test. Neuropeptides 28, 251255.[ISI][Medline]
Blankenship, M. R., Finn, P. R. and Steinmetz, J. E. (1998) A characterization of approach and avoidance learning in alcohol-preferring and alcohol-nonpreferring rats. Alcoholism: Clinical and Experimental Research 22, 12271233.[ISI][Medline]
Blokland, A., Prickaerts, J. and Raaijmakers, W. (1993) Absence of impairments in spatial and temporal discrimination learning in Lewis rats after chronic ethanol consumption. Pharmacology, Biochemistry and Behavior 46, 2734.[ISI][Medline]
Blum, K., Briggs, A. H. and Trachtenberg, M. C. (1989) Ethanol ingestive behavior as a function of central neurotransmission. Experientia 45, 444452.[ISI][Medline]
Car, H., Borawska, M. H. and Wisniewski, K. (1994) Effects of vasopressin and analogue [d(CH2)1(5), Tyr (Me)2, Val4, 3Pro7] AVP on learning and memory in rats chronically treated with ethanol. Journal of Physiology and Pharmacology 45, 163171.[Medline]
Carr, W. J., Yee, L., Gable, D. and Marasco, E. (1976) Olfactory recognition of conspecifics by domestic Norway rats. Journal of Comparative Physiology and Psychology 90, 821828.[ISI][Medline]
Dantzer, R., Bluthe, R. M., Koob, G. F. and Le Moal, M. (1987) Modulation of social memory in male rats by neurohypophyseal peptides. Psychopharmacology 91, 363368.[ISI][Medline]
Devenport, L. D. and Merriman, B. J. (1983) Ethanol and behavioral variability in the radial-arm maze. Psychopharmacology 79, 2124.[ISI][Medline]
Dufouil, C., Ducimetiere, P. and Alperovitch, A. (1997) Sex differences in the association between alcohol consumption and cognitive performance. American Journal of Epidemiology 146, 405412.[Abstract]
Eckardt, M. J., Rohrbaugh, J. W., Stapleton, J. M., Davis, E. Z., Martin, P. R. and Weingartner, H. J. (1996) Attention-related brain potential and cognition in alcoholism-associated organic brain disorders. Biological Psychiatry 39, 143146.[Medline]
Fadda, F. and Rossetti, Z. L. (1998) Chronic ethanol consumption: from neuroadaptation to neurodegeneration. Progress in Neurobiology 56, 385431.[ISI][Medline]
Gauvin, D. V., Baird, T. J., Vanecek, S. A., Briscoe, R. J., Vallett, M. and Holloway, F. A. (1997) Effects of time-of-day and photoperiod phase shifts on voluntary ethanol consumption in rats. Alcoholism: Clinical and Experimental Research 21, 817825.[ISI][Medline]
Geller, I. (1971) Ethanol preference in the rat as a function of photoperiod. Science 173, 456459.[ISI][Medline]
Greene, P. L., Diaz-Granados, J. L. and Amsel, A. (1992) Blood ethanol concentration from early postnatal exposure: effects on memory-based learning and hippocampal neuroanatomy in infant and adult rats. Behavioral Neuroscience 106, 5161.[ISI][Medline]
Griffin, M. G. and Taylor, G. T. (1995) Norepinephrine modulation of social memory: evidence for a time-dependent functional recovery of behavior. Behavioral Neuroscience 109, 466473.[ISI][Medline]
Hammoumi, S., Naassila, M. and Daoust, M. (1997) Experimental findings in the study of the reduction of alcohol intake. European Neuropsychopharmacology 7, S337S340.[Medline]
Hekmatpanah, J. and Haghighat, N. (1994) Alcohol consumption by nursing rats and its effect on the cerebellum of the offspring. Alcohol and Alcoholism 29, 535547.[Abstract]
Hyytia, P. and Sinclair, J. D. (1990) Differential reinforcement and diurnal rhythms of lever pressing for ethanol in AA and Wistar rats. Alcoholism: Clinical and Experimental Research 14, 375379.[ISI][Medline]
Kelly, S. J. and Tran, T. D. (1997) Alcohol exposure during development alters social recognition and social communication in rats. Neurotoxicology and Teratology 19, 383389.[ISI][Medline]
Kogan, J. H., Frankland, P. W. and Silva, A. J. (2000) Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10, 4756.[ISI][Medline]
Krahl, S. E., Berman, R. F. and Hannigan, J. H. (1999) Electrophysiology of hippocampal CA1 neurons after prenatal ethanol exposure. Alcohol 17, 125131.[ISI][Medline]
Lester, D. and Freed, E. X. (1973) Criteria for an animal model of alcoholism. Pharmacology, Biochemistry and Behavior 1, 103107.[Medline]
Letty, S., Lerner-Natoli, M. and Rondouin, G. (1995) Differential impairments of spatial memory and social behavior in two models of limbic epilepsy. Epilepsia 36, 973982.[ISI][Medline]
Lin, N. and Hubbard, J. J. (1994) The increased ethanol preference in rats induced by choice, darkness or drugs is reduced by ritanserin. Brain Research Bulletin 33, 633638.[ISI][Medline]
Lukoyanov, N. V., Madeira, M. D. and Paula-Barbosa, M. M. (1999) Behavioral and neuroanatomical consequences of chronic ethanol intake and withdrawal. Physiology and Behavior 66, 337346.[ISI][Medline]
Madeira, M. D., Andrade, J. P., Kieberman, A. R., Sousa, N., Almeida, O. F. and Paula-Barbosa, M. M. (1997) Chronic alcohol consumption and withdrawal do not induce cell death in the suprachiasmatic nucleus, but lead to irreversible depression of peptide immunoreactivity and mRNA levels. Journal of Neuroscience 17, 13021319.
McKinzie, D., Lee, J., Bronfen, J. H., Spear, L. P. and Spear, N. E. (1994) Context and tone conditioning are selectively impaired by ethanol in the preweanling rat: effects of dose and time of administration. Behavioral and Neural Biology 62, 201209.[ISI][Medline]
McMillen, B. A., Means, L. W. and Matthews, J. D. (1998) Comparison of the alcohol-preferring P rat to the Wistar rat in behavioral tests of impulsivity and anxiety. Physiology and Behavior 63, 371375.[ISI][Medline]
Mikolajczak, P., Okulicz-Kozaryn, I. and Kaminska, E. (1995) Effects of acamprosate and baclofen on ethanol hypnotic action in chronically ethanol treated rats. Alcohol and Alcoholism 30, 550, C10.13.
Mikolajczak, P., Okulicz-Kozaryn, I., Szczawinska, K., Kaminska, E. and Kus, K. (1999) Zolpidem involvement on hypnotic effect of ethanol and passive avoidance tasks in chronically ethanol treated rats. Alcohol and Alcoholism 34, 511519.
Moore, R. Y. and Sphe, J. C. (1993) GABA is the principal neurotransmitter of the circadian systems. Neuroscience Letters 150, 112116.[ISI][Medline]
Nagahara, A. H. and Handa, R. J. (1997) Fetal alcohol exposure produces delay-dependent memory deficits in juvenile and adult rats. Alcoholism: Clinical and Experimental Research 21, 710715.[ISI][Medline]
Omoto, M., Seki, K., Imai, T. and Nomura, R. (1993) The effects of ethanol exposure on radial arm maze learning and behavior of offspring rats. Environmental Research 63, 109121.[ISI][Medline]
Overstreet, D. H., Halikas, J. A., Seredenin, S. B., Kampov-Polevoy, A., Viglinskaya, I. V., Kashevskaya, O., Badishtov, B. A., Knapp, D. J., Mormede, P., Kiianmaa, K., Li, T. K. and Rezvani, A. H. (1997) Behavioral similarities and differences among alcohol-preferring and -nonpreferring rats: confirmation by factor analysis and extension to additional groups. Alcoholism: Clinical and Experimental Research 21, 840848.[ISI][Medline]
Parsons, O. A. (1998) Neurocognitive deficits in alcoholics and social drinkers: a continuum? Alcoholism: Clinical and Experimental Research 22, 954961.[ISI][Medline]
Pauli, J., Wilce, P. and Bedi, K. S. (1995) Spatial learning ability of rats following acute exposure to alcohol during early postnatal life. Physiology and Behavior 58, 10131020.[ISI][Medline]
Perio, A., Terranova, J. P., Worms, P., Bluthe, R. M., Dantzer, R. and Biziere, K. (1989) Specific modulation of social memory in rats by cholinomimetic and nootropic drugs, by benzodiazepine inverse agonists, but not by psychostimulants. Psychopharmacology 97, 262268.[ISI][Medline]
Popik, P. and van Ree, J. M. (1998) Neurohypophyseal peptides and social recognition in rats. In Progress in Brain Research, vol. 119, Urban, I. J. A., Burbach, J. P. H. and De Wied, D. eds, pp. 415436. Elsevier, Amsterdam.
Popik, P., Vetulani, J. and van Ree, J. M. (1992) Low doses of oxytocin facilitate social recognition in rats. Psychopharmacology 106, 7174.[ISI][Medline]
Prast, H., Argyriou, A. and Philippu, A. (1996) Olfactory social memory in rats facilitated by histamine. Brain Research 734, 316318.[ISI][Medline]
Rajakrishnan, V., Subramanian, P., Viswanathan, P. and Menon, V. P. (1999) Effect of chronic ethanol ingestion on biochemical circadian rhythms in Wistar rats. Alcohol 18, 147152.[ISI][Medline]
Reid, C., Edwards, J., Wang, M., Manybeads, Y., Mike, L., Martinez, N., La Grange, L. and Reyes, E. (1999) Prevention by a silymarin/ phospholipid compound of ethanol-induced social memory deficits in rats. Planta Medica 65, 421424.[ISI][Medline]
Salimov, R. M. (1999) Different behavioral patterns related to alcohol use in rodents: a factor analysis. Alcohol 17, 157162.[ISI][Medline]
Sasaki, H., Matsuzaki, Y., Nakagawa, T., Arai, H., Yamama, M., Seikizawa, K., Ikarashi, Y. and Maruyama, Y. (1995) Cognitive function in rats with alcohol ingestion. Pharmacology, Biochemistry and Behavior 52, 845848.[ISI][Medline]
Sawyer, T., Hengehold, A. K. and Perez, W. A. (1984) Chemosensory and hormonal mediation of social memory in male rats. Behavioral Neuroscience 98, 908913.[ISI][Medline]
Sinclair, J. D. and Geller, I. (1972) Ethanol consumption by rats under different lighting conditions. Science 175, 11431144.[ISI][Medline]
Steigerwald, E. S. and Miller, M. W. (1997) Performance by adult rats in sensory-mediated radial arm maze tasks is not impaired and may be transiently enhanced by chronic exposure to ethanol. Alcoholism: Clinical and Experimental Research 21, 15531559.[ISI][Medline]
Sturtevant, R. P. and Garber, S. L. (1988) Circadian rhythm of blood ethanol clearance rates in rats: response to reversal of the L/D regimen and to continuous darkness and continuous illumination. Chronobiology International 5, 137148.[ISI][Medline]
Taylor, G., Farr, S., Griffin, M., Humphrey, W. and Weiss, J. (1999) Adult ontogeny of rat working memory of social interactions. Journal of Gerontology 54A, M145M151.[ISI]
Thor, D. H. and Holloway, W. R. (1982) Social memory of the male laboratory rat. Journal of Comparative Physiology and Psychology 96, 10001006.[ISI]
Tomlinson, D., Wilce, P. and Bedi, K. S. (1998) Spatial learning ability of rats following differing levels of exposure to alcohol during early postnatal life. Physiology and Behavior 63, 205 211.[ISI][Medline]