Neuroscience 205 (2012) 73–80
A SIMPLE METHOD FOR DETECTION OF FOOD FORAGING
BEHAVIOR IN THE RAT: INVOLVEMENT OF NMDA AND DOPAMINE
RECEPTORS IN THE BEHAVIOR
F. LI,a1 W. Y. CAO,a1 M. B. LI,a Y. XU,a J. W. ZHANG,a
J. Y. ZHANG,a X. G. LUO,a R. P. DAI,b X. F. ZHOUc AND
C. Q. LIa*
a
Department of Anatomy and Neurobiology, XiangYa School of Med-
icine, Central South University, Tongzipo Road 172, Changsha
410013, Hunan, China
b
Department of Anesthesia, the second XiangYa Hospital of Central
South University, Ren-Min Road 86, Changsha, Hunan, China
c
Department of Human Physiology and Center for Neuroscience,
Flinders University, GPO Box 2100, Adelaide SA5001, Australia
Abstract—Food foraging behavior involves food removing,
hoarding, and competitive preying upon other animals. It is
also associated with high cognitive functions such as invest-
ing effort into decision making, but no established laboratory
model is available to detect the behaviors. In the present
study, we have developed a novel laboratory rodent model to
detect competitive, non-competitive, and no-hurdle foraging
conditions that can mimic the corresponding environment in
nature. We found that normal rats consistently foraged the
food from a food container to the field and spread food into
piles in the open field. There was no difference between male
and female rats in the amount of foraged food in the compet-
itive, non-competitive, and no-hurdle food foraging tests. The
amount of foraged food was consistent each day for five
consecutive days with a slight increase in following days.
There was no significant difference in the amount of food
foraged in the presence or absence of bedding materials. A
dramatic decrease of foraged food was found in the rats after
administration of haloperidol (dopamine D2 receptor antago-
nist) in the competitive, non-competitive, and no-hurdle food
foraging tests. Treatment with MK-801 (non-competitive
N-methy-D-aspartate receptor antagonist) reduced the for-
aged food in the competitive food foraging test, but did not
affect the foraged food in the non-competitive and no-hurdle
food foraging tests. Our study provides a simple but consis-
tent analogue of natural food foraging behavior. Our study
also suggests that dopaminergic and glutaminergic systems
are differentially involved in the food foraging behaviors.
© 2012 IBRO. Published by Elsevier Ltd. All rights reserved.
Key words: food foraging behavior, MK-801, haloperidol, rat.
Food foraging behavior is a species-specific behavior that
involves searching for food as well as transporting, hoard-
ing, and competitively snatching food away from other
animals. Hoarding, which is especially prevalent among
rodents, is an important adaptive strategy in times of food
1
These authors contributed equally to this work.
*Corresponding author. Tel: ⫹86-731-82650421; fax: ⫹86-731-82650426.
E-mail address: lichangqi2003@163.com (C. Q. Li).
Abbreviations: DA, dopamine; Hal, Haloperidol; NMDA, N-methy-D-
aspartate.
0306-4522/12 $36.00 © 2012 IBRO. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuroscience.2011.12.057
73
shortage, inclement weather, predation dangers, and re-
production, as it allows animals to control over food entries
(Sherry, 1990). Indeed, hoarding anticipates future need
and allows animals to remain in its sheltered nest while
feeding. However, in a natural environment it might be
disadvantageous for animals to pursue a larger food item if
the benefits do not outweigh the costs (Deacon, 2006).
Many studies suggest that foraging behavior involves
higher cognitive functions such as effort-based decision
making. Organisms making optimal decision require the
evaluation of both the costs and benefits of potential
choices (Day et al., 2010). A question that needs further
study is how the nature or amount of training on the cost-
benefit contingencies preoperatively affects choices. In
most of operant-based tasks, pretraining is usually used to
ensure stable and consistent performance. Until now, tech-
niques available for investigating food acquisition in verte-
brates are technically challenging. When studying sponta-
neous alternate in food foraging, the artificial nature of
manipulation of handling the rats to the starting position is
an obvious problem (Whishaw et al., 1995). Previous
models simply involve measuring the amount of hoarded
food transported from an external source into the home
cage (Lacroix et al., 1998; Walton et al., 2009), and this
is unsatisfactory because the rats in their studies are
trained before the test, a confounding factor that distorts
the perspective of the true nature of the animal behavior.
Mott et al. employ a T-maze task (Mott et al., 2009),
whereas Farrar et al. have used a concurrent fixed ratio
5 (FR5)/chow-feeding procedure (Farrar et al., 2007) to
assess effort-related choice behaviors. A small labora-
tory animal model of food foraging without prior training
or manipulation is necessary to mimic the natural animal
behavior. To this end, we have established a novel
laboratory model including competitive, non-competi-
tive, and no-hurdle food foraging paradigms. The es-
sence of the model in the competitive and non-compet-
itive food foraging paradigms is that food is offered in a
wire mesh container (the cage lid) on a 16-cm-high
cage, with or without a same gender residing rat, which
forces test rats to make an effort energetically or psy-
chologically to overcome the hurdle and compete with
residing rats to forage food.
Recently, there has been a surge of interest in the
complexity of animal cognition such as future planning and
decision making. There has been a growing interest in the
neurobiological basis underlying decision making, with em-
phasis placed on the different neuromodulators mediating
these types of executive functions. The behavioral and
74 F. Li et al. / Neuroscience 205 (2012) 73–80
neural effects of effort-related decision making are strongly
modulated by the availability of dopamine. Mesolimbic do-
pamine (DA) is a main component of the exertion of effort
in food-seeking behavior and effort-related decision mak-
ing (Salamone, 2009). DA depletion in the nucleus accum-
bens results in a reduced willingness to expend effort to
obtain rewards representing a strong reduced “wanting” in
animals. In food-seeking behaviors, rats with impaired DA
transmission instead select the way that require less effort
(Farrar et al., 2007; Mott et al., 2009; Worden et al., 2009).
Haloperidol (Hal) is an antidopaminergic drug (selective
D2 receptor antagonist) frequently used to treat psychosis
(Seeman, 2006). Other transmitters are also involved in
effort-related processes. For example, the N-methy-D-as-
partate (NMDA) receptor antagonist ketamine plays a key
role in the decision making when monkeys perform a visual
search task (Shen et al., 2010). In the present study, we
administered MK-801 (a highly selective noncompetitive
NMDA receptor antagonist) or haloperidol 30 min before
the food foraging test was performed by rats to validate our
model.
EXPERIMENTAL PROCEDURES
Animals
The study was carried out on male and female Sprague–Dawley
rats (200 –250 g) obtained from Central South University Animal
Services (Changsha, China). All experimental rats were housed
one per cage in the wire-topped plastic home base with removable
wire cover (30 cm⫻18 cm⫻16 cm) and ad libitum access to water.
The experimental protocol was approved by the Animal Care and
Use Committee of Central South University and conformed to the
National Institutes of Health Guide for the Care and Use of Lab-
oratory Animals. All efforts were made to minimize the number of
rats used and their suffering. For each treatment group in this
series of experiments, 8 –13 animals were used.
Behavioral test
The test was performed under a sound-attenuating environment in
an open field, which was constructed with black wood with dimen-
sions of 150 cm⫻150 cm⫻50 cm (Fig. 1). All behavioral tests were
Fig. 1. Photographs display the competitive food foraging paradigm from 7:00 PM to 7:00 AM the next day under 12-h fasting conditions. A small
wire-topped plastic home cage (30 cm⫻18 cm⫻16 cm) with 250 g standard rodent food pellets on the wire mesh was placed in the open field. (A) A
photograph of the open field with a control rat before the test. (B) A photograph of the open field with the control rat shown in (A) after the test. The
control rats spread food into piles in the field.
recorded with a video camera mounted directly above the testing
apparatus. For the time course, all rats were weighed and handled
accordingly and then left undisturbed in their home cages for the
duration of the experiment.
Food foraging test. The test was performed after 12 h of
food deprivation in an open field (Fig. 1). Rats have free access to
water during testing in the open field. On the days of testing, the
test male and female rats were removed from their home cages in
which the rats had been residing for at least 1 week and placed on
the open field, and the rats were allowed to become accustomed
to the open field before testing. After habituating for 2 h in the field,
one of following sessions was then conducted. The test rat was
allowed to navigate to the cage and foraged food freely from 7:00
PM to 7:00 AM of the next day. The amount of food moved to the
open field and the amount left in the food containers were sepa-
rately calculated at 7:00 AM the following day. Different rats were
used for different procedures so that no animal experienced more
than one session, and the rats were randomly assigned to proce-
dures as described below.
Competitive food foraging test. For testing competitive
food foraging activity, one rat was placed in a small plastic
home cage (30 cm⫻18 cm⫻16 cm) with a metal wire cover
(Fig. 1) with 250 g of standard food pellets on the wire mesh,
and a test rat which had been deprived of food for 12 h was
placed in the open field. The rat residing in the small home cage
and the test rat came from different litters and did not have any
interactions with each other before the test. The test rat was
allowed to navigate to the cage and foraged food freely from
7:00 PM–7:00 AM the next day.
Non-competitive food foraging test. For testing the non-
competitive food foraging activity, the test rat was placed in the
open field and allowed to navigate to the cage without any residing
rat in the cage, and the rat foraged food freely from 7:00 PM–7:00
AM next day. The other parts of procedures were conducted in the
same manner as in the test session of the competitive food
foraging paradigm.
No-hurdle food foraging test. We also designed a no-hurdle
foraging test. During the no-hurdle foraging test, 250 g of standard
food pellets were placed in transparent bright Plexiglas tray (30
cm⫻18 cm⫻2 cm; Changsha Zhonghui Plexiglass product Tech-
nology Corp, LTD, Changsha, China) instead of a small wire-
topped plastic home cage, and the tray was placed within the open
field close to one side of the wall. The other parts of the procedure
were conducted in the same manner as in the test sessions of the
competitive and non-competitive food foraging paradigms.
 F. Li et al. / Neuroscience 205 (2012) 73–80 75

In these experiments, the amount of food carried to the open RESULTS

field was considered the amount of food foraged per night.
A simple method to evaluate food foraging behavior
The effects of several variables on the competitive in rats
food foraging behavior
We found that naive rats without training or manipulation
Male rat was used to evaluate the effects of variables on the foraged food pellets from the food container to the field and
competitive food foraging behavior. All the experiments were car-
spread food into piles in the open field in three procedures
ried out under 12-h fasting conditions except the experiment that
compared food foraging behavior under fasting and non-fasting (Fig. 1B). Few rats scattered food everywhere in the open
conditions. field. The amounts of food foraged by male rats in the com-
petitive, non-competitive, and no-hurdle food foraging tests
The effect of fasting versus non-fasting on the food foraging
behavior. One group of testing rats were deprived of food for were 151.54⫾23.07 g, 174.77⫾18.97 g, and 156.43⫾20.39
12 h (fasting during 7:00 AM–7:00 PM) but given free access to g, respectively. The amount of food foraged by female rats in
water before the experiment. Other groups of testing rats were the competitive, non-competitive, and no-hurdle food forag-
given free access to food during the experiment. The competitive ing tests were 157.75⫾27.40 g, 180.38⫾16.62 g, and
food foraging test was conducted as described in section Com-
182.48⫾21.11 g, respectively. Two-way ANOVA indicated
petitive food foraging test.
no effects of test type (F(2,48)⫽0.583, P⫽0.562) and animal
The effect of a clean floor versus floor with bedding materials gender (F(1,48)⫽0.516, P⫽0.477) or their interaction (F(2,48)⫽
on the competitive food foraging behavior. The effect of clean 0.146, P⫽0.865) (n⫽8 per group) (Fig. 2).
floor versus floor with bedding materials on the competitive food
foraging behavior was investigated. Bedding material was spread
over the entire field at 5:00 PM. The competitive food foraging test The effect of fasting on the competitive food
was conducted as described in section Competitive food foraging foraging behavior
test.
The activities in animals with fasting were increased in the
The procedures were conducted for five consecutive days in competitive food foraging behavior test compared with
a rat. After the completion of the competitive food foraging test
non-fasting rats (160.56⫾30.23 g vs. 53.11⫾15.0 g). Stu-
at 7:00 AM each day, the rats were put back to their home cages
until the next session at 7:00 PM of the same day (fasting from 7:00 dent’s test indicated that the activities were significantly
AM to 7:00 PM, testing from 7:00 PM to 7:00 AM the next day), and increased after fasting in relative to no fasting (t⫽⫺5.701,
the tests were repeated for five consecutive days. P⬍0.0001, n⫽13) (Fig. 3A).
Effects of a higher degree of difficulty on the competitive and
non-competitive food foraging tests in rats. As showed in Fig. The effect of bedding in the floor of open field on
4A, B, the food container (16 cm in height) was placed upon a 50 competitive food foraging behavior
cm⫻35 cm⫻20 cm (length⫻width⫻height) plastic cage. It means
that the test rat which is in the open field had to climb total of We compared the amounts of food foraged by rats in the
36-cm-high barrier to get the food. The competitive and non- field with and without bedding. As shown in Fig. 3B, there
competitive food foraging test was conducted as described in was no significant difference in the two groups with or
section Competitive food foraging test and in section Non-com-
without bedding (162.38⫾31.03 g vs.155.64⫾45.37 g)
petitive food foraging test, respectively.
(t⫽⫺0.270, P⫽0.790, n⫽12).
The effects of pharmacological manipulations on the
food foraging test
One group of male rats were injected subcutaneously in a volume
of 1.0 ml/kg body weight with Hal(0.1mg/kg s.c.; Sigma Chemical,
St. Louis, MO, USA; it was dissolved in 10% glacial acetic acid,
brought to volume with saline, and the pH was adjusted to 6.5 with
NaOH). The dose of haloperidol used in the present study was
based upon previously performed research (Bardgett et al., 2009;
Farrar et al., 2007). A second group of rats were injected with
MK-801 (0.2 mg/kg s.c., Sigma) which was dissolved in sterile
saline and injected based on previous report with some modifica-
tion (Mishima et al., 2002). Control rats received vehicle (saline)
injections by the same route. Competitive, non-competitive, and
no-hurdle food foraging behavior were studied 30 min after injec-
tion of haloperidol or MK-801 or vehicle.

Statistical analysis
The results are presented as mean⫾SEM. Statistical differences
were determined using one way or two-way ANOVA followed by
post hoc Dunnett testing or Tukey post hoc multiple comparison
test where appropriate. Unpaired two-tailed Student’s t-test was
used if only two groups were applied. P⬍0.05 was considered
statistically significant.
Fig. 2. The amount of foraged food was calculated in three kinds of
food foraging tests under 12-h fasting conditions. Two-way ANOVA
indicated no effects of both test type (F(2,48)⫽0.583, P⫽0.562) and
animal gender (F(1,48)⫽0.516, P⫽0.477) and their interactions (F(2,48)⫽
0.146, P⫽0.865) (n⫽8 per group).
76 F. Li et al. / Neuroscience 205 (2012) 73–80

Fig. 3. Effects of variables on competitive food foraging behavior. (A) The effect of fasting on competitive food foraging behavior. Student’s test
indicated that foraging activity was significantly increased after fasting (t⫽⫺5.701, P⬍0.0001, n⫽13). (B) The effect of floor condition (with or without
bedding) on competitive food foraging behavior. Student’s test indicated that there was no significant difference in the amount of foraged food with
or without bedding materials on the floor (t⫽⫺0.270, P⫽0.790, n⫽12). (C) The amount of foraged are consistent but slightly increased when the same
procedure was repeated for five consecutive day on competitive food foraging behavior (fasting during 7:00 AM–7:00 PM; test during 7:00 PM–7:00 AM).
There was no significant difference in foraged food in the different time points with one-way ANOVA (F(4,48)⫽1.739, P⫽0.164, n⫽8).

The effect of repeating the same procedure for five
consecutive days on the competitive food foraging
behavior
The amount of foraged food was very consistent when
the same procedure was repeated for five consecutive
days (fasting during 7:00 AM–7:00 PM; testing during 7:00
PM–7:00 AM). Although there was a slight increase in the
amount of food foraged with increased number of tests,
there was no significant difference with one-way ANOVA
(F(4,48)⫽1.739, P⫽0.164, n⫽8) (Fig. 3C).
The effect of degree of difficulty on the competitive
and non-competitive food foraging tests in rats
We found that naive rats foraged mostly food pellets from
the food container to the field into piles in the open field
after adding the difficulty in the non-competitive food for-
aging tests (Fig. 4A), but only a little food pellets was
spread into the open field after adding the difficulty in the
competitive food foraging tests (Fig. 4B). Quantitative anal-
ysis revealed that after adding the difficulty, the foraged
food per night was slightly decreased in non-competitive
food foraging test (170.85⫾26.8 g vs. 152.05⫾22.6 g,
t⫽1.424, P⫽0.176, n⫽8). In the competitive food foraging
tests, the foraged food per night was significantly de-
creased after adding the level of difficulty (153.81⫾22.8 g
vs. 97.03⫾16.21 g, t⫽4.373, P⫽0.001, n⫽8) (Fig. 4C). In
addition, when the difficulty was added the amount of
foraged food in the competitive food foraging test was less
than in the non-competitive food foraging test(F(3,31)⫽
11.983, P⬍0.001, n⫽8) (Fig. 4C).
The effect of the DA receptor antagonist haloperidol
and the NMDA receptor antagonist MK-801 injection on
the three kinds of food foraging behavior
Control rats with vehicle injection and experimental rats
with Hal injection or MK-801 injection were tested for the
three kinds of food foraging test procedures. The amount
of foraged food of vehicle rats in competitive, non-compet-
itive, and no-hurdle food foraging tests was 165.92⫾24.73 g,
174.72⫾18.67 g, and 156.61⫾20.02, respectively. After
pretreatment with haloperidol, the amount of foraged food
in competitive, non-competitive, and no-hurdle food forag-
ing tests was 96.43⫾21.14 g, 74.41⫾14.63 g, and 58.55⫾
16.24 g, respectively, being significantly decreased (P⬍0.01,
n⫽8) compared with that of vehicle groups (Fig. 5). Pretreat-
ment of MK-801 significantly decreased the amount of for-
aged food in competitive food foraging tests in comparison
with the vehicle treatment (71.32⫾7.1 g vs. 165.92⫾24.73
g, P⬍0.01, n⫽8). There were no significant differences
between the MK-801 treatment group and the vehicle
 F. Li et al. / Neuroscience 205 (2012) 73–80 77

Fig. 4. Effects of different degrees of difficulty on the competitive and non-competitive food foraging tests in rats under 12-h fasting conditions.
Photographs display the non-competitive and competitive food foraging paradigm from 7:00 PM to 7:00 AM the next day after adding the difficulty.
(A) A photograph of the open field with a test rat in the non-competitive food foraging tests after one night foraging freely. The photograph
showed that all of food pellets from the food container were spread into piles in the open field. (B) A photograph of the open field with a test
rat in the competitive food foraging tests after one night foraging freely. The photograph showed that only a small food pellets were spread into
the open field, considerable food pellets were remained in the food container. (C) Effects of different levels of difficulty on the competitive and
non-competitive food foraging tests in rats. A dramatic decrease was found in the foraged food (g/12 h) of rats after adding the degree of difficulty
in the competitive food foraging behavior. There was no significant difference of foraged food in the non-competitive food foraging tests between
the conventional and higher degree of difficulty. The amount of foraged food was fewer in the competitive food foraging test when the difficulty
was added than in the non-competitive food foraging test in the two levels of difficulty. ** P⬍0.01 represents statistically significant differences
compared with conventional degree of difficulty group in the competitive food foraging behavior. ## P⬍0.01 represents statistically significant
differences compared with non-competitive food foraging tests groups (n⫽8 per group). For interpretation of the references to color in this figure
legend, the reader is referred to the Web version of this article.

treatment group in non-competitive and no-hurdle food
foraging tests (P⬎0.10) (Fig. 5). The amount of food eaten
per night in vehicle, haloperidol, and MK-801 treatment
rats were 18.63⫾3.9 g, 23.11⫾8.1 g, and 17.47⫾6.0 g,
respectively, one-way ANOVA indicated that haloperidol
and MK-801 treatment did not induced any effect on eaten
activity (F(2,29)⫽2.278, P⬎0.05, n⫽10).
DISCUSSION
The food foraging paradigm has played a major role in
the conceptual framework of behavioral science. An
increasing body of evidence indicates that food foraging
activity is associated with decision making and effort
investing (Rushworth et al., 2004; Walton et al., 2009).
In fact, it is an important model of a highly integrative
method for exploring numerous questions through dif-
ferent disciplines (Pravosudov and Smulders, 2010).
Many studies explore the influence of a variety of factors
on the foraging behavior: risk sensitivity, presence of
competitors, and predation risk, and so forth (Arcis and
Desor, 2003). However, these studies have used ani-
mals that are required manipulated or trained, which
may distort the interpretation of data or generate condi-
tioning effects. To study the foraging behaviors, it is
necessary to establish a method that can imitate and
reflect the nature of the food foraging behavior so that a
78 F. Li et al. / Neuroscience 205 (2012) 73–80
Fig. 5. Effects of haloperidol or MK-801 on three kinds of food forag-
ing tests in rats under 12 h fasting conditions. A significant decrease
was found in foraged food (g/12 h) of rats after administration of
haloperidol in the three kinds of food foraging behavior. A reduced
foraged food (g/12 h) in rats after administration of MK-801 was only
found in the competitive food foraging behavior. ** P⬍0.01, ## P⬍0.01
(n⫽8 per group). Vel: vehicle, Hal: haloperidol.
quantitative method can be directly used to examine
what neural mechanisms are implicated in the behavior.
The present study aimed to establish the method and
characterize it with different paradigms.
Firstly, we successfully created a simple and practical
laboratory model that can quantitatively detect the natural
food foraging behavior without any artificial intervention or
training. In our experiment, we tested competitive, non-
competitive, or no-hurdle food foraging conditions where
different animals were used respectively. These para-
digms represent three different situations: invest a larger
psychological effort plus a physical effort to gain reward,
invest a physical effort to obtain food, or exert no signifi-
cant physical effort to get food. The method works well and
allows animals to forage food freely within the field. In
nature, animals constantly face the risk of encountering
predators. They usually need to compete with other ani-
mals and overcome hurdles when foraging food. There-
fore, we designed the competitive food foraging activity
and non-competitive food foraging activity tests in which
animals must conquer the hurdle of a 16-cm-high plastic
cage to get the food. We also designed the no-hurdle food
foraging tests that allows an animal free access to food
held in a bright tray with 2-cm high without physical hur-
dles. During the competitive food foraging test, the rat
which was resident in the small home cage would shriek
and threat the invader (test) rat that wanted to forage food
on the wire mesh. In the presence of a hungry conspecific,
the resident rat is at risk on losing its food. Even without
bodily touching and fighting, this response implied a com-
petition or conflict. We designed the food foraging test
during the night without any human interruption to mimic
the natural food hunting behavior of rats. This is a big
advantage as our method avoids many confounds of arti-
ficial laboratory training and humanly handling. The over-
training of a task leads to behavior autonomy and develops
a habit without voluntary control by the mouse (Killcross
and Coutureau, 2003). Human handling can generate con-
ditioning effect, which may complicate neurobiological
mechanisms. As the foraging behavior is associated with
the process of decision making and effort investing (Rush-
worth et al., 2004; Walton et al., 2009), this model may be
important in exploring the neurobiological mechanisms of
high integrative brain functions.
In addition, we have studied that the effects of several
variables on competitive food foraging behavior using the
established animal model. Notably, we found that the
amount of foraged food in fasted animals was significantly
increased. It is a fact that the motivation for foraging and
hoarding more food tends to be activated when the rats are
experiencing a certain extent of hunger. The increase in
the foraged food after fasting indicates the state of satiety
is important for foraging behavior. In the present study
using the open field, which was a black floor constructed of
wood, we found that there was no significant difference in
the amount of foraged food with or without bedding mate-
rials on the floor. We had thought that foraging behavior
would be affected if the open field was covered with bed-
ding material. Some studies demonstrated that environ-
ment structure can affect the foraging behavior. For exam-
ple, increased illumination can reduce gerbil’s foraging
activity in areas without cover (Arcis and Desor, 2003).
More interestingly, when a rat was tested using same
procedure for five consecutive days, the amount of foraged
food is very consistent with only slight increase in the
competitive food foraging tests. This result suggests that
our method is very robust and reproducible. The data also
suggest that the prior experience does not significantly
affect subsequent foraging behavior. This result also sug-
gests that our method can be used to investigate interven-
ing factors or neurobiological mechanisms in the same rats
with internal controls by repetitive testing.
There was no difference in the amount of foraged food
among three kinds of food foraging tests, which means that
under certain level of difficulty animals would like to carry
all the food outsides to its territory. To determine whether
the foraging behavior was affected after exceeding con-
ventional level of difficulty, we designed another test to
increase the level of difficulty during which they had to put
more effort to climb a 36-cm-high hurdle in the competitive
and non-competitive conditions. After adding the level of
difficulty, we found that foraged food was significantly de-
creased in the competitive food foraging tests. However,
the higher degree of difficulty reduced food foraging activ-
ity, but it did not reach significance in the non-competitive
food foraging tests. These data suggest that the variables
such as the physical hurdle and the presence of a com-
petitor may interact with each other. When facing a com-
petitor and a high level of difficulty rats foraged less food.
In the absence of a competitor, this level of the difficulty did
not affect the activity. This result suggests that rats had to
invest a larger psychological effort plus a more physical
effort to gain reward.
Extensive studies have demonstrated that cost/benefit
decisions regarding relative effort are mediated by distrib-
uted dopaminergic and glutaminergic neural circuits (Flo-
resco et al., 2008). We hypothesize that the dopaminergic
and glutaminergic systems might be involved in the forag-
 F. Li et al. / Neuroscience 205 (2012) 73–80
ing behaviors. We undertook to test the role of neurotrans-
mitter receptors (NMDA or DA receptor) in food foraging
behavior with the established model by assessing the abil-
ity of their antagonists in this behavior. Dopamine released
in the nucleus accumbens is thought to contribute to the
decision to exert effort to seek reward (Nicola, 2010). The
amount of consumed food was not significantly different
after injection of haloperidol, a dopamine D2 receptor an-
tagonist, indicating that the D2 receptor has no significant
effect on food consumption in our model, which is consis-
tent with previous studies (McFarland and Ettenberg.,
1998) that suggest that dopamine transmission may not be
necessary for the demonstration of normal food-seeking
behavior. However, we found a clear impact of dopaminer-
gic modulation of the foraging behavior. The injection of
haloperidol caused an obvious reduction in food foraged
activity during the competitive, non-competitive, and no-
hurdle foraging behavior test compared with the control
group, suggesting that the D2 receptor is involved in food
foraging behavior. Many studies indicated that the disrup-
tion of dopaminergic transmission decreases effort-based
decision making (Floresco et al., 2008). Bardgett et al.’s
results showed that rats were more likely to choose the
smaller reward arm after haloperidol treatment (Bardgett et
al., 2009), suggesting that D2 receptor is involved in deci-
sion making. We found that the foraging behavior of three
different paradigms tested in the present studies was in-
hibited after haloperidol treatment. It suggests that there
may be subtle difference in neurobiological mechanisms
between decision making and foraging behavior. In our
model, the animals would not only make effort to obtain
food but also overcome hurdles for ongoing transfer of the
food into the field, which may associate with the reinforce-
ment process of a goal-directed behavior. Soto et al.’s
study demonstrated that food’s reinforcing effectiveness
was lowest in dopamine D2 receptor knockout mice indi-
cated by the behavioral economic analysis of decreases in
consumption with increases in price (Soto et al., 2011).
It should be emphasized that we cannot completely
rule out the possibility of the effect of haloperidol on loco-
motor activities, which may affect the foraging behavior.
However, we choose the low dose of haloperidol injection
(0.1 mg/kg) that does not affect the locomotor functions as
tested in the previous studies (Salamone et al., 2009).
Salamone et al. found that only higher doses of haloperidol
(0.4 mg/kg) produced motor impairments that interfere with
feeding behavior (Salamone et al., 1990). The duration of
the foraging test may reduce the possibility that the forag-
ing reduction was due to haloperidol-induced locomotor
dysfunction, as the catalepsy effect induced by the halo-
peridol treatment (4 mg/kg, i.p.) was attenuated after 3-h
injection (Adams et al., 1997). In our experiment, the du-
ration of 12 h provides enough time for the food foraging
behavior. Nonetheless, our results indicate that the de-
crease in the altered amount of foraged food after halo-
peridol treatment is most likely due to the specific effects of
the drugs on foraging behavior.
However, after MK-801 injection (0.2mg/kg s.c.), the
foraging activity in rats was only reduced in the competitive
79
food foraging behavior test indicating that the role of MK-
801 on foraging behavior was a specific effect. It is rea-
sonable to argue that the observed decrease in the amount
of foraged food could have been due to blockade of NMDA
receptor, which resulted in the disruption of competitive
activity. Our study suggests that NMDA receptor may be
involved in the regulating the social competitive activity.
We found that the quantity of consumed food was not
significantly different between the injection group and con-
trol group, indicating that NMDA had no effect on appetitive
behavior.
Our report describes an experimental method that al-
lows an animal to freely forage food in the field with or
without a physical or psychological barrier to overcome,
allowing an investigation of behaviors that can mimic food
foraging-related behaviors in nature. Based on the well-
validated animal paradigm, this study assessed the effects
of several variables on the established competitive food
foraging test. Most importantly, we elucidated the role
played by two neurotransmitter systems in the behavior
using our established models. In doing so, we provided
unambiguous and strong evidence to support the notion
that a dramatic decrease of foraged food was found in the
rats after administration of haloperidol in the competitive,
non-competitive, and no-hurdle food foraging tests. Treat-
ment with MK-801 reduced the foraged food in the com-
petitive food foraging test, but did not affect the foraged
food in the non-competitive and no-hurdle food foraging
tests. Our data support the notion that competitive food
foraging activity may be associated with the function of
both dopamine and excitatory amino acids. We believe
that this method could be of great utility in studies striving
to determine which brain regions are involved in cues of
food foraging behavior associated with reinforcement pro-
cess and effort-related decision making.
In light of the complexity of reinforcement process and
effort-related decision making, the intrinsic mechanism of this
state should be further studied. Using the simple and robust
model described, this study opens future avenues for analy-
sis of this complex animal behavior by manipulation of factors
such as levels of neurochemical substrates. Such advances
will be crucial for refining and developing future models of
human psychopathology. Future work will aim to elucidate
whether other neurotransmitters, such as 5-hydroxytrypta-
mine or opioids, are biologically relevant in foraging behavior,
as well as the involvement of specific brain regions.
Acknowledgments—This study was supported by National Natural
Science Foundation of China (30971533 to C.Q.L.).
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