Journal of Behavioral and Brain Science, 2011, 1, 172-180
doi:10.4236/jbbs.2011.13023 Published Online August 2011 (http://www.SciRP.org/journal/jbbs)
Copyright © 2011 SciRes. JBBS
Sex Influence on the Formation of Alcohol Preference
and Behavior in Rats during the Long-Term
Caffeine and Ethanol Intake
Eugenia Kutcher1,2, Alexey Egorov1,2, Elena Filatova1, Kristina Kulagina1, Nadezhda Chernikova1
1Behavior Neurophysiology and Pathology Laboratory, IM Sechenov Institu te of Evolutionary Physiology
and Bioc he mistry, Russian Academy of Sciences, St. Petersburg, Russia
2Department of Psychi at ry an d Ad di ct i ons, Medical Faculty, St. Petersburg State University,
St. Petersburg, Russia
E-mail: draegorov@mail.ru
Received
March 23, 2011; revised April 11, 2011; accepted May 4, 2011
Abstract
Last years the intake of energy drinks (drinks containing caffeine and alcohol) both in young men and women
has been increased. However the investigators do not pay attention to the analysis of gender differences. The
goal of the study was the investigation of ethanol and caffeine influence on the alcohol preference formation
and behavior in male and female rats under the conditions of long-term experiment. It has been found that six
month intake of caffeine, ethanol and their combination has led to the increase of alcohol preference both in
male and female rats. Alcohol preference was formed earlier in rats consumed combination of caffeine with
ethanol, later on in rats consumed ethanol. In animals consumed caffeine the strong alcohol preference did
not form up to the end of the experiment. Alcohol preference was higher in female rats consuming caffeine
with ethanol and pure ethanol solution compared to male rats. Behavioral activity significantly increased in
females consumed caffeine and caffeine with ethanol, compared to animals received ethanol and controls.
Similar tendency was observed in male rats. The anxiety level was significantly higher in females rats in all
experimental groups compared to controls, while males did not demonstrate increased anxiety.
Keywords: Ethanol, Caffeine, Two-Bottle Test, Behavioral Activity, Anxiety
1. Introduction
According to epidemiological data, up to 80% consumed
alcoholic beverages in Russia is beer and light alcoholic
beverages. It happens not due to replacement of strong
liquors, but because of alcohol consumption increase per
capita [1]. Beer and light alcoholic beverages, including
energy drinks, are very popular among young generation,
both in Russian males and females [2]. In the US the
ingestion of energy drinks in combination with alcohol is
becoming increasingly popular [3,4], with 24% of a large
stratified sample of college students reporting such con-
sumption within the past 30 days [3].
There is an association between the heavy use of caf-
feine and the heavy use of alcohol [5,6]. The effects of
energy drinks which contain both ethanol and caffeine
are not good investigated especially after long term in-
take. One study showed that ingestion of a caffeinated
energy drink (Red Bull) with vodka reduced participants
perception of impairment of motor coordination in com-
parison to vodka alone, but did not significantly reduce
objective measures of alcohol-induced impairment of
motor coordination, reaction time, or breath alcohol con-
centration [7]. Thus, when mixing energy drinks and
alcohol, users may not feel the symptoms of alcohol in-
toxication. This may increase the potential for alcohol-
related injury [8]. In addition, mixing energy drinks with
alcohol was associated with increased heavy episodic
drinking and episodes of weekly drunkenness [3] and
closely associated with a problem behavior syndrome [9].
In recent publication Arria with colleagues [10] insist
that weekly or daily energy drink consumption is strongly
associated with alcohol dependence Besides, energy drink
consumption significantly predicted subsequent non-
medical prescription stimulant use [11].
Data on the combined effects of caffeine and ethanol
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173
in acute animal experiments are controversial [12,13]. It
was shown in mice that a single dose caffeine adminis-
tration only masks alcoholic intoxication, but did not
compensate the ethanol induced cognitive impairments
[14], as it has been previously observed [15,16]. In was
demonstrated that the administration of energy drink
alone has increased the locomotor activity of mice in
relation to a control group. Low doses of ethanol alone or
in combination with energy drink did not affect their
locomotor activity. However, the reduction of activity
observed after high doses of ethanol was antagonized by
energy drink [17].
However, few and controversial empirical studies to
date have examined the demographics of energy drink
consumption, particularly with respect to gender differ-
ences in the prevalence or correlates of consumption. It
was supposed that young males are the main consumers
of beverages containing caffeine and alcohol [18]. In a
survey of 1253 college students, energy drink users were
disproportionately male and consumed alcohol more fre-
quently than non-energy drink users [11]. Temple with
colleagues [19] have suggested that boys are more
sensitive to the effects of caffeine than girls. Meanwhile,
another publication reported about higher rates of con-
sumption in female students than in male students [20].
Epidemiological date have shown the increase in beer
and soft drink consumption in adolescents and young fe-
males as well [1]. Besides, clinical investigations have
demonstrated both young males and female prepon-
derance to light beverages [21,22]. We did not find out
animal experimental studies on combined ethanol and ca-
ffeine intake with respect to gender peculiarities.
The aim of the study was the investigation of ethanol
and caffeine influence on alcohol preference formation
and behavior in male and female rats under the condi-
tions of long-term experiment.
2. Materials and Methods
The study was was conducted on 60 adult Wiatar rats: 30
males and 30 females. The animals were kept on a
standard diet. Rats were divided into four groups. Within
6 months of the experiment the first group had access
only to a solution containing 10% ethanol and 0.4 g/l of
caffeine, the second group—only 10% alcohol solution,
and the third—to a solution containing 0.4 g/l caffeine,
the fourth (control)—only to water.
Alcohol preference was measured using a standard
two bottle test before the experiment and each subsequent
month during the whole experiment after a 24 hours dep-
rivation. This was made by placing the animals into a
single cage and offering them two waterers: one con-
tained water, and the other 10% ethanol solution. The
quantity of liquid taken from different waterers was es-
timated during a 15 minutes time period.
Behavior parameters were estimated before and every
month of the experiment using “Open field”. The “Open
field” test allows seeing animals with high or low loco-
motion and emotional levels. The setting is a square,
divided into smaller squares area 0.5 × 0.5 m bounded by
non-transparent 0.8 m borders around the periphery.
Number of crossed squares, vertical points, urination and
defecation, latent period of leaving the first square, and
grooming were registered during a 5 minute period.
After 6 months of the experiment the anxiety and be-
havioral activity were investigated in the “Suok test”.
“Suok test” is an alley divided into segments 5 cm wide
and placed at a height of 50 cm upon the floor [23]. A
series of parameters which reflected motor and investi-
gative activities, as well as anxiety was estimated during
a 5-minute time period. These parameters also included:
the number of crossed segments, the vertical activity,
peep down, orientations, the latent period of exit from
the starting square and the number of feet from slipping,
falling, urinations and defecations. Reduction indicators
of motor and behavioral activity (crossings, the vertical
activity, peep down, orientations), and an increase in the
number of slips, falls, urinations and defecations are re-
porting increasing levels of anxiety in animals.
The order of the tests was 1) two-bottle test was con-
ducted before and each month of the experiment; 2) Next
day after the “two-bottle” test the “open field” test was
conducted before and each month of the experiment; 3)
“Suok-test” in the end of the experiment. The light inten-
sity was 60 Watt from the lamp 1.5 meter above the open
field set or “Suok-test” set. The persons doing the testing
were blind to experimental conditions, i.e. they did not
know what kind of liquor was consumed by the rat. All
rats were marked by another collaborator. The female
estrous cycle stage was not taken into consideration.
Statistical analysis was performed using ANOVA
Fisher LSD test. The experiments were carried out in
accordance with the requirements of the Commission on
Bioethics and in compliance with international standards
GLP («Good Laboratory Practice»).
3. Results
Before and after the first month of the experiment all
male rats have shown the low level of ethanol consump-
tion in two-bottle test, compared to control (Figure 1). In
the third, fourth and fifth months the ethanol preference
has increased in all animals excepting the controls, al-
though these differences were only a tendency. After
sixth month of the experiment the same tendency was
observed: the caffeine + ethanol rats consumed more
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174
ethanol in two-bottle test than before the experiment and
compared to animals of the other groups.
In female rats the ethanol consumption in two-bottle
test was also low before the experiment (Figure 2). A
month later, the ethanol preference has increased in all
rats except controls. The ethanol consumption in the
“two-bottle” test was significantly higher in all experi-
mental groups compared to the control group after the
second month (ethanol + caffeine p < 0.057, ethanol p <
0.058, caffeine p < 0.016) and after the third month of
the experiment (ethanol + caffeine p < 0.0006, ethanol p
< 0.0013, caffeine p < 0.0039). After the fifth month
ethanol preference was significantly increased in etha-
nol+caffeine and ethanol groups compared with animals
consuming caffeine (p < 0.015, p < 0.052) and controls
(p < 0.00015, p < 0.0006). After 6 months, the ethanol +
caffeine female rats have demonstrated significantly
higher ethanol preference in two-bottle test (p < 0.077
Figure 1. Consumption of ethanol solution in the “two-bottle” test in male rats. The ordinate axis shows the percentage of
consumed ethanol from the total amount of liquid consume d in the test (data are expressed as the arithmetic mean value and
the standard error of the mean). Along the horizontal axis—months of the experiment.
Figure 2. Consumption of ethanol solution in the “two-bottle” test in female rats. All indications as in Figure 1.
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compared with ethanol, p < 0.0012 compared with caf-
feine, p < 0.000016 compared with water). The lower
preference was in ethanol rats, than in caffeine, than in
controls.
Thus, from the second to fourth months of the experi-
ment the ethanol consumption was increased in rats of
both sexes in the two-bottle test, excepting the control
animals. The greatest ethanol preference was observed in
the groups drinking caffeine with ethanol.
It is of interest, that the highest difference was observed
in male and female rats, consuming ethanol with caffeine
(p < 0.000050). The female rats, drinking ethanol, have
preferred alcohol in two-bottle test more than male rats,
too (p < 0.034). The caffeine and control male and fe-
male animals didn’t differ statistically (Figure 3).
ANOVA results are presented in Table 1.
In the open field test male rats showed higher beha-
vioral activity before the experiment (Figure 4). The
behavioral activity included the number of crossed squares
and the vertical activity. In subsequent months, this ac-
tivity decreased, which is likely due to habituation of
animals to test conditions and a reduction of explora-
tory activity. The rats consumed caffeine with ethanol
were significantly more active than other rats on the third
and sixth months of experience.
Female rats also demonstrated the highest behavioral
activity in the open field during the first measure before
the experiment (Figure 5). Then, behavioral activity has
Table 1. ANOVA results of factor (“substance”, “time” and “sex”) influence on ethanol consumption in the two-bottle test.
Factors SS Degr. of MS F p
substance 61115.4 3 20371.8 17.0901 0.000000
time 24780.8 6 4130.1 3.4648 0.002440
sex 13815.2 1 13815.2 11.5897 0.000740
subst*time 29691.4 18 1649.5 1.3838 0.136176
subst*sex 9538.9 3 3179.6 2.6674 0.047626
time*sex 9188.8 6 1531.5 1.2848 0.263432
subst*time*sex 21944.9 18 1219.2 1.0228 0.432945
Error 416016.0 349 1192.0
Figure 3. Consumption of ethanol in the “tw o-bottle” test by male and female rats. The ordinate axis show s the percentage of
consumed ethanol from the total amount of liquid consume d in the test (data are expressed as the arithmetic mean value and
the standard error of the mean). The abscissa—groups of rats consuming different substances. Left bar—male rats, right bar
—female rats.
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Figure 4. Total behavioral activity in the “open field” test in male rats. Along the horizontal axis—months of the experiment;
the ordinate—the total behavioral activity (number of crossed squares and vertical activity), in points.
Figure 5. Total behavioral activity in the “open field” test in female rats. All indications as in Figure 3.
decreased in all groups. On the third and fourth months
of the experiment behavioral activity was significantly
higher in rats taking caffeine, than in other groups. By
the fifth month of the experiment the activity signifi-
cantly increased in rats consuming alcohol and caffeine.
It was significantly higher than in other groups (receiv-
ing ethanol p < 0.002, caffeine – p < 0.052, control – p <
0.0002). After 6 months of the experiment, the behave-
ioral activity was similar in animals receiving ethanol
with caffeine, caffeine and control animals and was sig-
nificantly lower in rats drinking ethanol (p < 0.05 as
compared to receiving ethanol with caffeine).
Thus, both male and female consumed caffeine with al-
cohol showed a significantly higher behavioral activity in
the open field during different experimental months: the
males in the third and sixth, while females only in the
fifth month of the experiment. Females, taking caffeine,
showed higher behavioral activity in the middle of the
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experiment, in contrast to males.
ANOVA results are presented in Table 2.
After 6 months of the experiment, male rats received ca-
ffeine with ethanol demonstrated higher behavioral ac-
tivity in “Suok test” than animals receiving ethanol (p <
0.08) (Figure 6). Behavioral activity in this test was
measured by the number of crossed segments, vertical
postures, orientations and peeking. The data obtained in
“Suok test” are similar to those in the open field. Any-
way the conditions of “Suok test” are more stressful than
in the open field.
In female rats consumed caffeine behavioral activity in
the “Suok test” was significantly higher (p < 0.0030
compared to receiving ethanol + caffeine, p < 0.0050 –
ethanol and p < 0.00006 – control).
The level of anxiety, including the slips, falls, urina-
tions and defecations, did not differ in all male groups
(Figure 7). Anxiety level was significantly higher com-
pared to controls in female rats, receiving ethanol + caf-
feine (p < 0.022) and ethanol (p < 0.013).
4. Discussion and Conclusions
The results of two-bottle test suggest that both psychoac-
tive substances: caffeine, ethanol and their combination
leads to the increase of ethanol preference in two months
from the start of the experiment. It is known that single
dose caffeine affects the preference of ethanol intake:
according to some authors’ it increased [13], while ac-
cording to the others caffeine reduced ethanol consump-
tion [12]. During combined chronic intake of both sub-
stances one can observe not only the mutual effect of
Table 2. ANOVA results of factor (“substance”, “time” and “sex”) influence on behavioral activity in the “open field” test.
Factors SS Degr. of MS F p
substance 6592.8 3 2197.6 3.3718 0.018719
time 62980.2 6 10496.7 16.1053 0.000000
sex 47958.2 1 47958.2 73.5830 0.000000
subst*time 13893.6 18 771.9 1.1843 0.271572
subst*sex 2551.7 3 850.6 1.3050 0.272641
time*sex 6892.7 6 1148.8 1.7626 0.106019
subst*time*sex 10600.1 18 588.9 0.9035 0.574591
Error 220945.3 339 651.8
Figure 6. Behavioral activity in the “Suok test” after 6 months of the experiment in male and female rats. Left bar—male rats,
right bar—female rats. The ordinate—behavioral acts, in points.
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Figure 7. Anxiety in the “Suok test” after 6 months of the experiment in male and female rats. All indications as in Figure 6.
ethanol and caffeine, but the effect changes of each sub-
stances because of their interaction. It is important that
alcohol preference was higher in female rats drinking
caffeine with ethanol and ethanol compared to males.
This fact demonstrates higher development of alcohol
preponderance in females consuming stimulant-ethanol
mixture and pure ethanol solution.
It is known that the effects of caffeine are associated
with the adenosine receptor blocking which induces
changes in other neurotransmitter systems: dopamine,
serotonin, noradrenalin and acetylcholine [24]. It was ob-
served that the acute alcohol introduction changes the
activity of all monoaminergic systems [25]. It was shown
that serotonin and noradrenalin systems play a modulat-
ing role in the development of tolerance to ethanol [26].
Increased dopamine stimulates ethanol consumption,
while increased serotonin reduces it [27]. It is supposed
that caffeine, ethanol or their combination effects medi-
ated via monoaminoergic system lead to the increase of
alcohol consumption in experimental animals compared
to water control rats. In all animals received caffeine and
ethanol combination, the alcohol preference increased
earlier than in animals consuming pure 10% ethanol. The
rats received only caffeine does not exhibit a persistent
preference for alcohol. Perhaps, in the case of combined
caffein and ethanol consumption the more rapid increase
in tolerance occurred, and as a consequence the increase
of alcohol preference. Earlier the sensitivity to nicotine
and cocaine as a result of prior caffeine intake has been
described in experimental animals [28].
The obtained increase of behavioral activity in caf-
feine and ethanol + caffeine rats agrees with Ferreira
with colleagues, [17] data that.the administration of en-
ergy drink alone has increased the locomotor activity of
mice and facts that reduction of activity observed after
high doses of ethanol was antagonized by energy drink.
In behavioral experiments (open field and Suok tests)
both gender similarities and differences were revealed.
Obviously that animal behavior in both tests is related
not only to the motor and research activity, but to emo-
tional state as well. Female rats consuming caffeine +
ethanol and caffeine were significantly more active com-
pared to the other female groups. All male groups did not
reveal this difference. It may be explained by higher
anxiety level among caffeinated females. Pervious inves-
tigations have considered that anxiety level does posi-
tively correlate with alcohol intake [29,30] It is known
that female alcoholism is often correlated with affective
disorders [31], which is associated with sero- tonin defi-
ciency [32,33].
Thus, it can be concluded that:
A long-time intake of caffeine, ethanol and their com-
bination has led to the increase of alcohol preference
both in male and female rats;
Alcohol preference was higher in female rats consum-
ing caffeine with ethanol and pure ethanol solution
compared to male rats;
Alcohol preference was formed earlier in rats con-
sumed combination of caffeine with ethanol, later on
in rats consumed ethanol. In animals consumed caf-
feine the strong alcohol preference did not form up to
the end of the experiment;
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Behavioral activity significantly increased in female
consumed caffeine and caffeine with ethanol, com-
pared to animals received ethanol and controls. Simi-
lar tendency was observed in male rats;
The anxiety level was significantly higher in females
rats in all experimental groups compared to controls,
while males did not demonstrate increased anxiety.
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