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Simultaneous mastering of two abstract concepts by
the miniature brain of bees
Aurore Avarguès-Webera,b,c,1, Adrian G. Dyerc,d, Maud Combea,b, and Martin Giurfaa,b,2
a
Université de Toulouse, Centre de Recherches sur la Cognition Animale, F-31062 Toulouse Cedex 9, France; bCentre National de la Recherche Scientifique
(CNRS), Centre de Recherches sur la Cognition Animale, F-31062 Toulouse Cedex 9,France; cDepartment of Physiology, Monash University, Clayton VIC 3800,
Australia; and dSchool of Media and Communication, RMIT University, Melbourne VIC 3001, Australia

Edited* by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved March 16, 2012 (received for review February 13, 2012)

concept learning

| vision | insect | Apis mellifera

C

oncepts and categories promotecognitive economy by sparing
us the learning of every particular instance encountered in our
daily lives (1–5). Instead, we group specific instances in broad
classes that allow responses to novel situations, which are deemed
equivalent to the classified items. Stimulus classification can be
governed by perceptual similarities: The belonging to a given class
is defined, in this case, by common physicalfeatures predictive of
the category (6). Alternate classifications that are independent of
perceptual similarity can be achieved by using relations as
grouping criterion (6). Relations such as “same” or “different” and
“better than” or “worse than” can serve as the basis for a form of
classification that can be considered abstract because it involves
learning beyond perceptual generalization. Given thatthe terms
“category” and “concept” are often used indiscriminately (7), we
will use here the former to refer to perceptual classification and
the latter to relational classification. Manipulating concepts presupposes a high level of cognitive sophistication because the relational concept has to be coded as a specific entity by the brain
independently of the physical nature of objects linked by thisrelation (8). Such ability requires time to develop during human
infancy and is not necessarily suspected to be possible with in an
insect brain (3, 5).
Honey bees are a powerful model for studies of visual cognition
because they can be reliably trained to associate visual stimuli with
sucrose reward (9–11). In this experimental framework, bees can
learn, through experience, to navigate in complexmazes (12), to
categorize objects based on coincident visual features (11, 13–15),
and to master discriminations based on identity (16, 17) and
www.pnas.org/cgi/doi/10.1073/pnas.1202576109

Results
To answer this question, marked honey bees were individually
trained to fly into a Y-shaped maze where they had to discriminate between two stimuli presented vertically on the back walls
of the maze.Stimuli were composed of two different elements,
which were arranged in one of two spatial configurations: above/
below (one above the other) or left/right (one on the right of the
other). Importantly, stimulus components were always different
from one another, be they achromatic patterns or chromatic
discs (Figs. 1A, 2A, and 3A, training). Bees were trained to enter
the Y maze and were rewarded withsucrose solution for
choosing either the above/below stimuli or the left/right stimuli.
A drop of quinine solution was delivered for any incorrect choice
because it significantly enhances visual attention while learning
perceptually difficult tasks (23). Thus, during 30 learning trials (i.
e., 30 foraging bouts between the hive and the Y maze), half of
the bees (n = 14) were rewarded for recognizingthe above/below
relationship (and penalized for choosing the left/right relationship), with the conditions reversed for the other half (n = 14)
(i.e., reward: right/left; punishment: above/below). Within each
group, bees were either trained with achromatic patterns (half of
the bees) or with color discs (Fig. S1). Stimulus features and
positions were systematically varied between trials (Fig....