Observational learning in C57BL 6j mice

Behavioural Brain Research 174 (2006) 125–131

Research report

Observational learning in C57BL/6j mice
Pascal Carlier a,∗ , Marc Jamon b,1
a

Equipe CNRS G´enomique Fonctionnelle Comportements et Pathologies, CNRS—GFCP/P3M/Aix-Marseille Universit´es,
31 Chemin Joseph Aiguier, 13402 Marseille Cedex 20, France
b Equipe CNRS G´
enomique Fonctionnelle Comportements et Pathologies, CNRS—GFCP/P3M/Aix-Marseille Universit´es,
31 Chemin Joseph Aiguier, 13402 Marseille Cedex 20, France
Received 8 June 2006; received in revised form 11 July 2006; accepted 13 July 2006
Available online 30 August 2006

Abstract
The ability of mice to solve a complex task by observational learning was investigated with C57BL/6j mice. Four female demonstrators
were trained to reliably perform a sequence that consisted in pushing a piece of food into a tube attached to the side of a puzzle box, and
recovering it by opening a drawer in front of the box. They then performed this sequence in front of naive mice assigned to individual cubicles
in a box with a wire mesh front arranged in a row facing the demonstrators. A total of 25 naive mice (13 males and 12 females) were used.

Fifteen mice observed 14 demonstrations a day for 5 days; 10 control mice were placed in similar cubicles, but behind a plastic screen which
prevented them from observing the demonstrators. The mice were post-tested in the demonstrator situation, and 6 of 15 observers immediately
reproduced the complete task successfully, but none of the naive or control mice were able to solve the task. The observers and controls were
then subjected to a five level individual learning schedule. Observers learned the individual task significantly faster than the controls. No sex
difference was found. These results suggest that observational learning processes at work were based on stimulus enhancement and observational
conditioning.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Mouse; Social learning; Observational learning; Stimulus enhancement; Observational conditioning

1. Introduction
Social animals can adapt their behaviour to environmental
requirements by transmitting individual experience. This “social
transmission” is the by-product of a compromise between
exploratory drives and the avoidance of negative experiences [4]
and helps improve individual fitness. Famous field observations
of primates and birds [32] opened new paths that shed light on
aspects of social transmission in animal behaviour. Gradually,
the contribution of social transmission of behaviour, both within
and between generations, has been identified and/or demonstrated [2–4,16,18,26,27,29,54,62,64,68].
Social transmission can be defined as a cultural system of

information transfer [17] that affects the individual phenotype,
in the sense that part of the phenotype is acquired from other
∗

Corresponding author. Tel.: +33 4 91 16 45 89; fax: +33 4 91 77 50 84.
E-mail addresses: carlier@dpm.cnrs-mrs.fr (P. Carlier),
jamon@dpm.cnrs-mrs.fr (M. Jamon).
1 Tel.: +33 4 91 16 43 37; fax: +33 4 91 77 50 84.
0166-4328/$ – see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.bbr.2006.07.014

individuals. Social transmission can either be a merely social
influence (individual B is influenced by individual A but does
not learn any part of mimicry from A) [64], or can be genuine
social learning, when B learns some part of mimicry from A
[4,17,64]. Social transmission can be based on various clues,
but visual clues require special attention as social transmission
related to visual observation of peers involves different levels of different cognitive skills. When visually related social
transmission (i.e. “observational social transmission”) occurs,
the processes at work rely on observational social influence

and observational learning, respectively [64]. Contrary to social
influence genuine observational learning does not require that
the model be present to work [27]. Observational learning has
mainly been documented in vertebrates, with experimental studies on primates [5,20,45,54,60,62,63], cats [9,25,33,70], and
birds [6,8,15,21,24,31,38,39,47,70], and also in invertebrates:
cephalopods [19], insects (e.g. bumblebees [66], crickets [12].
It has been extensively studied in the rat; see, for example
[13,14,28,30,35,36,40,41,46,48,49,51,65,69], while mice were
less studied than rats. Social transmission based on olfactory

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P. Carlier, M. Jamon / Behavioural Brain Research 174 (2006) 125–131

clues has been demonstrated consistently in mice tested for
learned food preferences, both in adults (preference for a food
after an interaction with a recently fed conspecific [57]) and
with mother and pup interaction [44,59]; the effect of the age
of the demonstrator has also been tested [10]. Observational
social transmission, based on visual observation of peers, has

been investigated, testing mice with tasks that consisted in opening baited puzzle boxes [42,43,55,56,58], experiments where
the observers could interact freely with the demonstrator. In
these situations, the visual component of social transmission
was combined with other senses, involving olfactory and tactile
skills, making it impossible to assess the exact contribution of
observational clues to performance. These experiments, therefore, could not provide a clear-cut demonstration of the type of
observational transmission at work. One such study [56] listed
several mechanisms influencing the social context to explain the
results: social exposure [64], a case of social influence (e.g. B,
placed together with A, is exposed to the same environment and
learns to respond to the environment in a way that matches A’s
response), stimulus enhancement [22,27,52,64] which is a case
of social learning [17,62,64] (e.g. B learns from A to what object
to orient its behaviour), and trial-and-error learning, explaining
the performance of mice observing the activities of a demonstrator. In one experiment [11], observers and demonstrators
had limited contact, being separated by a wire mesh. The task
consisted in opening a swinging pendulum door, having to push
either on the right or the left to get a reward. The observers performed significantly better than the controls that were behind
a visual barrier and could not see the demonstrator. The study
showed there was observational learning ability in mice, but the

task was simple, requiring only one action to be conducted in a
single location.
We are proposing a more detailed analysis of the mechanisms
involved in observational learning, using a new paradigm based
on conditional sequences of actions in specific locations. To
break down the complexity of the problem, we defined a linear
task: action A in location ␣, followed by action B in location
␤. The spatial dissociation of the two actions was designed to
produce a clearer understanding of what was being learnt, i.e.
actions and/or locations where the actions occurred, so as to
separate the actions and locations, and determine whether the
animal could repeat a complete sequence, a sequence in order
(in time and/or space), or had simply focused on certain locations
of the actions (e.g. the first or last). The experimental design did
not allow for any close interaction between demonstrators and
observers, to ensure that the information related to the task itself
was obtained visually.
This preliminary study showed that there was a significant
improvement in the performance of observer mice after observing the behaviour of demonstrators. Some of the observers
successfully reproduced the task. For all the observers, the observation of demonstrators enhanced the subsequent learning in

a progressive learning program. These results are discussed
in relation to the cognitive skills of rodents, focusing on the
prospects of this new paradigm for investigating social cognition in mice.

2. Materials and methods
2.1. Animals
C57BL/6j mice were used for the study because they are not visually
impaired and are proficient for both observational learning [11] and spatial learning [1,34,37,50,61]. Thirty-one C57BL/6j mice, from Charles River
France, were housed in same-sex groups, in standard cages (30 cm long × 12 cm
high × 18 cm wide), and in a room at a constant temperature of 21 ◦ C, with
30–40% relative humidity, and a 12/12 h light–dark cycle. Food pellets and
water were available ad libitum. Before the experiment, the mice were divided
in two groups:
• Six females, aged 20 weeks, were used as demonstrators. Females were
selected because they are less absent-minded than males tend to be in the
presence of females [11].
• Twenty-five mice (13 males and 12 females) aged between 6 and 12 weeks
were used as learners. The 25 learners were randomly allocated 15 observers
(8 males and 7 females) and 10 controls (5 males and 5 females).
From the beginning of the experimental sessions, the observers and controls

were housed in single cages 30 cm long × 12 cm high × 18 cm wide.

2.2. Set-up
The set up consisted in a puzzle box and an observation box (Fig. 1). The
puzzle box was a translucent Plexiglas parallelepiped (7.5 cm wideY(Y10Ycm
highY(Y4Ycm deep) with an open tube (inside diameter 0.7 cm) extending 0.5 cm
and positioned 6 cm from the bottom, plus a drawer made of two pieces of
Plexiglas (6.5 cm wide × 2.5 cm high) glued together at right angles to form
a drawer, positioned in front at the bottom, and attached so that it could be
tipped over towards the front (Fig. 1). An electric remote control was used by
the experimenter to lock and unlock the drawer. A small movable metal tab in
the tube prevented the mice from pulling out the food (a piece of dry cookie)
that was placed inside it. To get the food, the mouse first had to go to the side of
the box and push the metal tab with a front paw; this made the food fall into the
drawer. The mice then had to go to the front of the device and open the drawer
to recover the food.
The observation box (outside dimensions: 28 cm wide × 15 cm high × 6 cm
deep) had a wire mesh front, and was divided into five individual cubicles
(inside dimensions: 5 cm wide × 5 cm deep × 15 cm high) (Fig. 1). The partitions between the cubicles and the back wall were made of white Plexiglas
so that the observers had no visual contact with each other. The front wall,

26 cm wide × 13 cm high, was covered with wire mesh and the observers had a
clear view of the set-up. The two end cubicles, one on the left and one on the

Fig. 1. Experimental set-up: To get the food, the mouse first had to go to the
side of the device and push the metal tab with a front paw; this made the food
fall into the drawer. The mouse then had to go to the front of the device and open
the drawer to retrieve the food.

P. Carlier, M. Jamon / Behavioural Brain Research 174 (2006) 125–131
right, were covered with white opaque Plexiglas for the controls. The puzzle
box and observation box were placed in a Plexiglas arena (36 cm long × 30 cm
wide × 15 cm high) opposite each other at a distance of 15 cm. The mice were
monitored throughout the experiment via a video camera (Ikegami ICD 47 E)
attached to a metal bracket above the arena. The experiments were videotaped
for additional analysis.

2.3. Experimental procedure
2.3.1. Shaping demonstrators
The demonstrators were trained over 4 weeks, 3 days a week, following a
weekly schedule. Day 1: food deprived (18 h); days 2–4: training (the mice were

fed 3 g per day to maintain 85–90% of their normal body weight); days 5–7: rest
(free access to usual diet). The shaping schedule had five graded levels (based
on a previous study [7]).
• Level 1. The mouse has to get the food placed on the outside edge of the tube
protruding on the left side of the puzzle box; i.e. “one action—one location.”
• Level 2. The mouse has to get the food placed further inside the tube, but still
outside the metal tab; “one action—one location.”
• Level 3. The mouse has to get the food from inside the tube; the food is
on the inside of the metal tab which is unlocked in the open position; “one
action—one location.”
• Level 4. The mouse has to push the food into the drawer by pushing the metal
tab inside the tube. If the mouse succeeds in doing this, the experimenter
immediately opens the drawer and the mouse can go to the front and retrieve
the food inside the open drawer; “one action—two locations.”
• Level 5. The mouse has to push the food into the drawer by pushing the metal
tab inside the tube. If the mouse succeeds, the experimenter immediately
unlocks the drawer. The mouse has to go to the front side and to tip up the
drawer to get the food; “two actions—two locations.”
The daily shaping sessions lasted 30 min per mouse. The mouse performed
the following trial as soon as the previous one had been successfully completed

(consumption of food) or, if unsuccessful (after 5 min). A minimum of two
consecutive trials had to be successful at each level before moving to the next
level. After two failures at a given level, the mouse was taken back to the previous
level and had to succeed at least once before moving on again to the next level.
If the mouse also failed the previous level, it was taken back to the one before,
and so on. The demonstrators had to be able to carry out the task without any
error or hesitation. Each level could therefore be started over again until it was
carried out perfectly in the training sessions. At level 5 the mice had to perform
perfect sequences with a short latency period (