Review
Cognition with few neurons:
higher-order learning in insects
Martin Giurfa1,2
1
Université de Toulouse (UPS), Centre de Recherches sur la Cognition Animale, 31062 Toulouse cedex 9, France
2
Centre National de la Recherche Scientifique (CNRS), Centre de Recherches sur la Cognition Animale, 31062 Toulouse cedex 9,
France
Insects possess miniature brains but exhibit a sophisti-
cated behavioral repertoire. Recent studies have
reported the existence of unsuspected cognitive capa-
bilities in various insect species that go beyond the
traditionally studied framework of simple associative
learning. Here, I focus on capabilities such as attentional
modulation and concept learning and discuss their
mechanistic bases. I analyze whether these behaviors,
which appear particularly complex, can be explained on
the basis of elemental associative learning and specific
neural circuitries or, by contrast, require an explanatory
level that goes beyond simple associative links. In doing
this, I highlight experimental challenges and suggest
future directions for investigating the neurobiology
of higher-order learning in insects, with the goal of
uncovering the basic neural architectures underlying
cognitive processing.
Introduction
Insects have historically fascinated biologists for the access
they allow to the mechanisms and organization of behav-
ior. The fact that insects possess miniature nervous sys-
tems, with a low number of neurons (e.g., 100 000 neurons
in the fruit fly brain [1] or one million in the bee brain [2]
versus 85 billion in the human brain [3]), does not consti-
tute a limitation for the production of sophisticated and
complex behaviors [4–6]. Numerous insect species such as
bees, ants, parasitoid wasps, fruit flies, moths, butterflies,
hissing bugs, crickets, grasshopper, and locusts, learn and
memorize different sorts of sensory cues as predictors of
reward [7–19] or punishment [20–26] and form memories
of such experiences that can be retrieved at different times
after learning, from the short- long-term range. The neural
circuits underlying such capabilities are only simple in
appearance but exhibit an exquisite architecture [27].
The past decade has generated a wealth of novel re-
search on insect learning and memory that has overcome
the classical framework of simple forms of associative
learning to focus on more elaborate cognitive capabilities
[4,5]. This includes work on attention-like processes in
fruit flies and honey bees [28,29], pessimistic biases [30],
and concept learning in bees [31–33]. These reports shed
new light on the cognitive richness of insect behavior,
which seems to transcend basic Pavlovian and operant
Corresponding author: Giurfa, M. (martin.giurfa@univ-tlse3.fr).
Keywords: associative learning; cognition; non-elemental learning; invertebrate;
insect; neural circuits.
0166-2236/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tins.2012.12.011 Trends in Neurosciences, May 2013, Vol. 36, No. 5
learning. Yet, at the same time, they may tend to create
a feeling of wonder in non-scientific members of the public,
usually promoted by biased media reports or by scientists
themselves, which revolves around a growing tendency of
attributing too easily humanlike qualities to animals [34].
In the light of such an undesired effect, the critical question
is not, therefore, whether insects achieve ‘marvelous feats’,
but how they achieve them. Here, I focus on a selection of
recent findings in insect cognitive behavior and analyze the
neural mechanisms known to mediate such behavior. I
discuss whether behaviors that appear particularly com-
plex can be explained on the basis of elemental associative
learning and specific neural circuits or, by contrast, require
an explanatory level that goes beyond this level.
Protocols for the study of elemental associative learning
in insects
Insects have been traditional models for the study of
elemental associative learning (see Glossary). Multiple
cases of Pavlovian (association between an originally
Glossary
Absolute classical conditioning (A+): a case of classical conditioning in which a
single stimulus A is learned through its association with reinforcement (+).
Concept learning: learning about relations between objects rather than about
absolute physical features of objects (e.g., color, shape, size). Extracting such
relations allows transferring a choice to unknown objects that may differ
dramatically in terms of their physical features but that may fulfill the learned
relation. Learning about concepts therefore comprises extracting from a series of
problems the rule or relation that grants the common solution to these problems.
Delayed matching to sample: a training protocol used to determine whether a
subject can learn the concept of sameness. The subject must match its choice
to a stimulus that corresponds to a sample previously presented. Because the
sample is regularly changed during the training, animals must learn the
concept of sameness; that is ‘always choose what is shown (the sample),
independently of what else is shown’.
Delayed non-matching to sample: a training protocol used to determine
whether a subject can learn the concept of difference. The subject must choose
a stimulus that is explicitly different from a sample previously presented.
Because the sample is regularly changed during the training, animals must
learn the concept of difference; that is, ‘always choose the opposite of what is
shown (the sample), independently of what else is shown’.
Differential classical conditioning (A+ BS): a case of classical conditioning in
which, in its simplest form, a stimulus A is learned through its association with
reinforcement (+) and a stimulus B through its association with absence of
reinforcement ().
Elemental associative learning: learning that is mediated by simple, univocal
links between two (or more) events. For instance, an animal may learn an
elemental link between a tone and a food reward and another elemental link
and between a light and an electric shock as a punishment. Associations
learned are unambiguous and specific for the sensory cues learned and their
respective outcomes.
Stimulus transfer: a process by which a new stimulus evokes a response instead
of a previous known stimulus that evoked originally the same response.
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 Review Trends in Neurosciences May 2013, Vol. 36, No. 5

neutral stimulus, the conditioned stimulus [CS], and a
biologically relevant stimulus, the unconditioned stimulus
[US]) and operant learning (association between a given
behavior and a resulting reinforcement) have been de-
scribed and studied in insects. For instance, in the honey
bee Apis mellifera, olfactory conditioning of the proboscis
extension response (PER) has been repeatedly used for the
study of elemental classical conditioning and its neural
substrates [35–37]. Individually harnessed hungry bees
(Figure 1a) respond to stimulation of their antennae with
sucrose solution (the US) with an extension of their probos-
cis (the PER). If a neutral odor (the CS) is forward-paired
with sucrose, the bees learn an elemental association
between odor and sucrose reward such that they exhibit
conditioned PERs to later presentations of the odor alone
(Figure 1a). The association built is Pavlovian and, depend-
ing on the number of trials, interstimulus interval, intertrial
interval, among other factors, can be consolidated in short-
term memory (STM), mid-term memory (MTM), or long-
term memory (LTM) [11,36]. Classical conditioning has also
been intensively studied in the fruit fly Drosophila melano-
gaster. Flies can easily be trained to associate an odor (the
CS) with an aversive electric shock (the US). The typical
procedure consists of training groups of flies alternatively
presented with two different odors, one paired with an
electric shock (CS+) and another non-paired with shock

(a)

Toothpick with
sucrose

Harnessed
bee CS

US

Odor delivering setup

(b)
Yaw torque signal
Laser Computer
diode Light
Torque source
meter

Color filter

Light
guides

Diffusor
Electric
motor Arena posion

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Figure 1. (a) Conditioning of the proboscis extension response (PER) in restrained honeybees. Left panel: An individual bee is immobilized in a metal tube so that only the
antennae and mouth parts (the proboscis) are free to move. The bee is set in front of an odorant stimulation setup, which is controlled by a computer and which sends a
constant flow of clean air to the bee. The air flow can be rerouted through cartridges presenting chemicals used for olfactory stimulation (conditioned stimuli [CSs]).
Sucrose solution (unconditioned stimulus [US]) is delivered by a toothpick to the antennae and to the proboscis. Right panel: After conditioning, the odor CS, which initially
did not evoke any response, triggers the PER. (b) The flight simulator used for visual conditioning of a tethered fruit fly. By courtesy of B. Brembs. Left panel: A Drosophila is
flying stationary in a cylindrical arena. The fly’s tendency to perform left or right turns (yaw torque) is measured continuously and fed into a computer, which controls arena
rotation. On the screen, four ‘landmarks’ – two Ts and two inverted Ts – are displayed to provide a referential frame for flight-direction choice. A heat beam focused on the
fly’s thorax is used as an aversive reinforcer. The reinforcer is switched on whenever the fly flies toward a prohibitive direction. The fly therefore controls reinforcer delivery
by means of its flight direction. Right panel: Detail of a tethered fly in suspended flight within the simulator.

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 Review Trends in Neurosciences May 2013, Vol. 36, No. 5

(CS–) [38]. Retention is measured in a T-maze where condi-
tioned flies must choose between the CS+ and the CS–.
Several different memories are induced in Drosophila by
this olfactory conditioning depending on trial number, trial
spacing, and retention period [21,24]. These include STM,
intermediate-term memory (ITM), and two separable forms
of LTM defined as anesthesia-resistant memory (ARM) and
long-lasting LTM (l-LTM), of which only the latter depends
on de novo protein synthesis.
Drosophila has also played a pivotal role in the study of
operant learning. In this case, a fruit fly is suspended from
the thorax in the middle of a cylindrical arena that allows
the presentation of visual landmarks (Figure 1b) [39]. The
tethered fly flies stationary and, if some of these landmarks
are paired with the aversive reinforcement of an unpleas-
ant heat beam pointed on the thorax, learns to fly toward a
safe direction, avoiding the dangerous-landmark direc-
tions [39,40] (Figure 1b). The fly learns to control reinforce-
ment delivery because its flight maneuvers determine the
switching off of the heat beam if the appropriate flight
directions are chosen [40], thus constituting a case of
operant learning. Classical associations can also be estab-
lished between the visual landmarks displayed on the
cylinder wall and the reinforcer [41].
The neural circuits responsible for these forms of asso-
ciative learning have been studied extensively, in particu-
lar in the case of olfactory learning (Figure 2). The olfactory
circuit and the nervous circuits mediating appetitive
(mainly through octopaminergic neurons) (Figure 2a)
and aversive reinforcements (mainly through dopaminer-
gic neurons for aversive reinforcement) (Figure 2b) have
been relatively well characterized in bees and flies, but also
in other species such as ants, moths, and crickets
[10,11,21,23,24,36,40,42–44]. In Drosophila, an intercon-
nection between octopaminergic and dopaminergic path-
ways was recently found to mediate the appetitive
reinforcement properties of sucrose [45,46].
Top-down modulation of elemental associative learning
in insects: the role of attentional processes
Attention describes our ability to focus our perception on
one stimulus (or group of related stimuli), while filtering
out other simultaneous stimuli that are less relevant at
any moment [47]. Several reports have recently indicated
that attentional processes similar to those described in
vertebrates can be identified in insects. Studies on bum-
blebee and honey bee color learning [48,49] suggested that
attentional processes may dramatically affect discrimina-
tion capabilities and that the key issue is how the bees
learn the visual task. After absolute conditioning, in which
a bee is trained with a single color rewarded with sugar
water, discrimination of colors that are very similar is
difficult, but this is facilitated after differential condition-
ing in which the bee has to learn the distinction between a
rewarded and a non-rewarded color, which usually takes
more trials [48]. The difference in performance suggests
that attentional processes are involved; in differential
conditioning, the bee has to focus on the difference and

(a) (b)
Mushroom
bodies (MB) 200 μm 50 μm Mushroom
ca bodies (MB) ca

ca
PPL1 α
CN pe ml
α′
EN α PAM pe
γ
β β′
Opc lobe Opc lobe LH β PN EN
LH l-PN m-PN LH
LH Glo
DAL
SEG
Glo SEG
Antennal Antennal
lobe (AL) lobes (AL)
VUMmx1
ORN
ORN

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Figure 2. Neural pathways for conditioned stimulus (CS) and unconditioned stimulus (US) information in the honey bee and the fly brain. Note the different size scales for
each brain. (a) CS and US circuits responsible for appetitive olfactory learning (odor–sucrose association) in the honey bee. Left hemisphere – the olfactory (CS) circuit: The
antennal lobe (AL), first-order olfactory neuropil, receives input from approximately 60 000 olfactory receptor neurons (ORNs) located within sensilla on the antenna. The AL
comprises approximately 160 glomeruli (Glo), which are sites of synaptic interaction between ORNs, inhibitory local neurons (not shown), and approximately 800 projection
neurons (PNs), which convey processed information via different tracts (l-PN and m-PN) to higher brain centers, the mushroom bodies (MBs), and the lateral horn (LH). Each
MB comprises approximately 170 000 Kenyon cells. Their dendrites form the calyces (ca) and their axons form the pedunculus (Pe) and the two output lobes: the vertical (a)
lobe and the horizontal (b) lobe. Within the MBs, feedback neurons (not shown) project from the Pe and lobes back to the calyces, providing inhibitory feedback to the MB
input regions. Extrinsic neurons (ENs) take information from the Pe and the lobes and project to different parts of the protocerebrum, but most conspicuously to the LH.
Centrifugal neurons (CNs) provide feedback from the MBs to the ALs and are thought to be involved in retrograde modulation of antennal lobe circuits. Right hemisphere –
the sucrose (US) circuit: Gustatory sensory neurons on the antennae project to the dorsal lobe [95], whereas those on the mouthparts project to the subesophageal ganglion
(SEG) [96]. A single octopaminergic neuron, the ventral unpaired median neuron of the maxillary neuromere 1 (VUMmx1) (only one side is shown), represents sucrose
during appetitive conditioning. This neuron has its dendrites in the SEG and projects to the AL, the MB calyces, and the LH. (b) CS and US circuits responsible for aversive
olfactory learning (odor–electric shock association) in the fruit fly. Left hemisphere – the olfactory (CS) circuit: The AL receives input from approximately 1400 ORNs located
on the antenna and the maxillary palp. The AL comprises approximately 50 glomeruli (Glo). Approximately 150 PNs convey processed information to higher brain centers,
the MBs and the LH. Each MB comprises approximately 2500 Kenyon cells. Their dendrites form the calyces (ca); their axons form the Pe and the axon collaterals the vertical
lobes (a and a0 ) and the horizontal lobes (b, b0 , and g). ENs take information from the a and a0 lobes and project to both the ipsilateral and the contralateral LH. CNs provide
feedback from the MB to the ipsilateral AL and connect with the contralateral MB. Right hemisphere: The electric shock (US) circuit: Two clusters of dopaminergic neurons,
PP1 and PAM, whose activity is necessary and sufficient to represent the electric shock in aversive olfactory conditioning, project to different subcompartments of the MBs
and induce memories of differing stability.

287
Review
not the mere presence of a visual target, thus making
learning slower. This hypothesis is confirmed by experi-
ments on bumblebees in which incorrect choices in a color
discrimination task, which are usually followed by the
absence of reward, are further penalized by delivery of
quinine solution [50]; in these circumstances, the bumble-
bees’ choices become slower and more accurate, thus re-
vealing a trade-off between speed and accuracy in the
context of foraging decisions. Also, honey bees confronted
with discrimination of colors that are perceptually similar
learn the task only if incorrect choices are penalized with
quinine [51], a penalization that has no effect if the colors
are different enough to facilitate the discrimination task.
These results indirectly suggest that attentional processes
exist in insects and that they can be modulated by experi-
ence.
Evidence for attentional processes requires demonstra-
tion of suppressed responsiveness to competing stimuli
[52]. This requirement has been met in experiments with
honey bees trained to choose a colored disc (‘target’) among
a varying number of differently colored discs (‘distractors’)
[29]. The bees’ task was to suppress responsiveness to
distractors, and accuracy and decision time were measured
as a function of distractor number and color. For all color
combinations, decision time increased and accuracy de-
creased with increasing distractor number, whereas per-
formance improved when more targets were present.
These findings recall serial search strategies in primates,
in which stimuli are examined sequentially. Thus, at the
behavioral level, the strategies implemented by bees con-
verge with those of animals in which attention is commonly
studied [29].
Although behavioral approaches only have been used to
study attention in bees, selective attention in fruit flies has
been retraced to the neural level [28]. A tethered fly flying
stationary within a cylindrical arena (similar to that in
Figure 1b) and tracking a visual object (a vertical black bar
displayed on the cylinder wall) moving at a constant fre-
quency around it exhibits anticipatory behavior consistent
with attention for the bar it tracks. The neural correlate of
such anticipatory response is a transient increase in a
20–30 Hz local field potential recorded in a region of the
brain called the medial protocerebrum [28]. The neural
response is not only anticipatory, but also selective and
specific to the shape presented, increased by novelty and
salience, and reduced when the fly is in a sleep-like state
[28]. Moreover, the use of mutants showed that output of
a- and b-lobe neurons of the mushroom bodies (Figure 2b),
which are higher-order structures of the insect brain
(Figure 2), is required for both the tracking response
and the 20–30 Hz response. In another study, competing
moving gratings were presented to either eye of the fly in
the cylindrical arena [53]. Confronted with these percepts,
flies alternated their flight direction between the right and
left moving grating, in an attention-like process that sup-
pressed responses to the non-followed grating. Brain ac-
tivity recorded in parallel at the two optic lobes of the fly
increased mostly in the 20–50 Hz range and only on the
side associated with a behavioral choice [53], consistent
with previous reports on the involvement of this frequency
domain in attention-like processes [28].
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Trends in Neurosciences May 2013, Vol. 36, No. 5
The key mechanism for attentional processes in insects
may be found in neuromodulatory neurons that set arousal
thresholds for different nervous circuits, including those of
mushroom bodies [54]. The fruit fly mushroom bodies are
richly innervated by different subsets of dopaminergic
neurons[55,56] and although the classic view involves
considering these neurons as the neural substrate for
punishment signaling in aversive olfactory learning [57],
current views relate dopamine levels in the insect brain
with arousal levels [54]. Indeed, transient attenuation of
dopamine release in fly mutants attenuates the 20–30 Hz
responsiveness to the moving black bar in flies and oral
delivery of methamphetamine, which increases dopamine
release, rescued this responsiveness [58]. Thus, dopami-
nergic neurons may modulate selective attention in the
insect brain, acting on a series of nervous circuits underly-
ing different forms of sensory–motor performances.
Cognitive interpretations of elemental learning in
insects: pessimistic biases in bees
Recent work on olfactory learning in honey bees has at-
tributed to them ‘pessimistic cognitive biases’ under nega-
tive, stressful circumstances [30]. In humans, pessimistic
biases are defined as the increased expectation of bad
outcomes after negative affective states such as stress or
anxiety. Is it appropriate to use this anthropocentric ter-
minology to describe an insect’s behavior? Or does it exceed
the specific criteria used to test the behavior of honey bees?
In this study, bees were trained using olfactory condi-
tioning of the PER (see above and Figure 1a) to discrimi-
nate two mixtures of the same two odors A and B. As an
example, a mixture where the ratio A:B was 1:9 was
rewarded with sucrose solution (CS+), whereas another
mixture in which the ratio was 9:1 was punished with
quinine solution (CS–). After training, bees were vigorous-
ly shaken to simulate a predatory attack and induce an
‘anxiety-like state’ that would in turn determine ‘pessimis-
tic’ evaluation of ambiguous stimuli. Bees were then pre-
sented with the trained mixtures (9:1 and 1:9), but also
with novel ratios of A and B that they had not experienced
during training (3:7, 1:1, and 7:3). These stimuli being
novel to the bees, the question was whether shaken bees
would consider, for instance, the 7:3 mixture as being more
similar to the punished 9:1 mixture than would non-shak-
en bees. In this case, shaken bees would respond less to the
7:3 mixture than would non-shaken bees, a result that
would be consistent with a pessimistic judgment bias of the
novel ambiguous mixture. This was exactly what was
observed [30] and it was concluded that these results
‘add an invertebrate animal to the growing list of verteb-
rates. . .that when subjected to various forms of negative,
stressful manipulations exhibit pessimistic judgment
biases’ [30].
Although this interpretation is appealing, an alterna-
tive explanation is possible. The task inculcated by the
training was discrimination between two odor mixtures,
which non-shaken bees achieved at a level of approximate-
ly 35% (the difference between the percentage of responses
to the CS+ and to the CS–). Given this small difference, the
original discrimination was obviously not easy for the bees.
After shaking, differentiation increased to 65%, because
 Review Trends in Neurosciences May 2013, Vol. 36, No. 5

responses to the CS– decreased whereas responses to the
CS+ remained constant, probably due to a ceiling effect.
One can thus argue that shaking induced better discrimi-
nation between the two original mixtures 1:9 (CS+) and 9:1
(CS–) and that, as a consequence of this improved discrim-
ination, bees responded less to the novel 7:3 mixture. In
other words, shaking enhanced attentional processes,
resulting in better discrimination performances and less
generalization between the CS– and a mixture that was
close to it. No terminology centered on pessimism would be
required in this scenario. Rather, these findings could be
depicted as a case of attentional modulation of elemental
olfactory learning after a negative experience.
A critical question is therefore whether basic levels of
interpretation are possible when studying experience-
dependent changes in insect behavior. This argument
should also be applied to vertebrate studies. An interesting
example is provided by two independent sets of experi-
ments in which an entrapped rat is set free by other rats
[59] and an entrapped ant is set free by other ants of its
colony [60]. Whereas the former results have been pre-
sented as a straightforward case of empathy, thus assign-
ing to rats the capacity to recognize and share sensations
experienced by another individual, the ant case has been
interpreted more cautiously without reference to sharing of
sensations; more importantly, this difference in interpre-
tation between the two studies has led to the proposition of
an experimental agenda that should be respected before
speaking about empathy in animals [61].
Non-elemental learning in insects: learning about
concepts
A higher level of complexity is reached when animals
respond in an adaptive manner to novel stimuli that they
have never encountered before and that do not predict a
specific outcome based on the animals’ past experience.
Such positive transfer of learning (also called stimulus
transfer) brings us, therefore, to a domain that differs from
that of elemental forms of learning [62].
Concept learning is particularly interesting for the
study of non-elemental learning, because it requires trans-
fer that occurs independently of the physical nature of the
stimuli considered (e.g., colors, shape, size) [63,64] and
relies on relations between objects [65,66]. Examples of
such relations are ‘same as’, ‘different of’, ‘above/below of’,
and ‘on the left/right of’. Extracting such relations allows
transferring a choice to unknown objects that may differ
dramatically in terms of their physical features but that
may fulfill the learned relation.
Various recent reports have indicated that honey bees
learn relational rules of different sorts. These include
‘sameness/difference’ [31], ‘above/below’ [32], and the
mastering of two rules simultaneously, ‘above/below’ (or
left/right) and ‘different of’ [33]. Similarly, recent reports
on ‘numerosity’ in bees suggest a capacity to extract infor-
mation about number irrespective of the physical features
of the objects counted [67,68].
Sameness/difference concepts
Learning of the concepts of sameness and difference was
demonstrated through the protocols of delayed matching to
sample (DMTS) and delayed non-matching to sample
(DNMTS), respectively [31]. Honey bees foraging in a Y-
maze (Figure 3a) were trained in a DMTS experiment in
which they were presented with a changing non-rewarded
sample (i.e., one of two differently colored disks – ‘color
group’ – or one of two different black-and-white gratings,
vertical or horizontal – ‘pattern group’) at the entrance of a
maze (Figure 3b). The bees were rewarded only if they
chose the stimulus identical to the sample once within the
maze. Bees trained with colors and presented in transfer
tests with black-and-white gratings that they had not
experienced before solved the problem and chose the grat-
ing identical to the sample at the entrance of the maze.
Similarly, bees trained with the gratings and tested with
colors in transfer tests also solved the problem and chose
the novel color corresponding to that of the sample grating
at the maze entrance (Figure 3c). Transfer was not limited

(a) (b) Transfer (c) Transfer tests with paerns Transfer tests with colors
test (training with colors) (training with paerns)
100
Key: Preference for vercal Key: Preference for blue
Preference for horizontal Preference for yellow

80 * * *
*
% Correct choices

60

Training 40
(60 trials)

20

0
Vercal Horizontal Blue Yellow
Paern Color
group group Sample
TRENDS in Neurosciences

Figure 3. Concept learning in honey bees. Sameness learning [31]. (a) Y-maze used to train bees in a delayed matching-to-sample task. Bees had to enter into the maze to
collect sugar solution on one of the back walls of the maze. A sample was shown at the maze entrance before bees accessed the arms of the maze. (b) Training protocol. A
group of bees was trained during 60 trials with black-and-white, vertical, and horizontal gratings (Pattern Group); another group was trained with colors, blue and yellow
(Color Group). After training, both groups were subjected to a transfer test with novel stimuli (patterns for bees trained with colors, colors for bees trained with patterns). (c)
Performance of the Pattern and Color groups in the transfer tests with novel stimuli. Both groups chose the novel stimulus corresponding to the sample, although they had
no experience with such test stimuli. *p < 0.05. Adapted from [31].

289
Review
to different types of visual stimulus (pattern versus color),
but could also operate between drastically different senso-
ry modalities such as olfaction and vision [31]. Bees also
mastered a DNMTS task and learned a rule of difference
that was transferred between different sensory stimuli
such as colors and achromatic patterns [31]. These results
were the first to document that bees learn rules relating
stimuli in their environment. They were later verified in
experiments showing that bees categorize visual images
based on general features common to these images [69] and
in a study showing that the working memory underlying
the solving of the DMTS task lasts for approximately 5 s
[70], a period that coincides with the duration of other
visual and olfactory STMs characterized in simpler forms
of associative learning in honey bees [11]. The capacity to
learn a rule of sameness has been also used to study the
presence of a sense of numerosity in bees (see [68] and
below).
Above/below concepts
For many animals that must operate in complex natural
environments, spatial concepts such as right, left, above,
and below are of crucial importance to generate appropri-
ate relational displacements and orientation. A recent
study investigated whether honey bees learn an above/
below relationship between visual stimuli and transfer it to
novel stimuli that are perceptually different from those
used during the training [32]. Bees were trained to fly into
a Y-maze and choose visual stimuli presented above or
below a horizontal bar. Training followed a differential
conditioning procedure in which one spatial relation (e.g.,
‘target above bar’) was associated with sucrose solution
whereas the other relation (e.g., ‘target below bar’) was
associated with quinine solution. One group of bees was
rewarded on the ‘target above bar’ relation and another
group was rewarded on the ‘target below bar’ relation.
After completing the training, bees were subjected to a
non-rewarded transfer test in which a novel target stimu-
lus (not used during the training) was presented above or
below the bar. Despite the novelty of the test situation,
which preserved the spatial relationship to the bar as the
single criterion predicting or not predicting the presence of
sucrose reward, bees responded appropriately: if trained
for the above relationship they chose the novel stimulus
above the bar and if trained for the below relationship they
chose the novel stimulus below the bar [32].
Because during the training all stimuli always appeared
in the same region of the visual field (e.g., the upper field
for bees trained to ‘above’ and the lower field for bees
trained to ‘below’), an alternative interpretation could posit
that, instead of learning a conceptual relationship, bees
simply relied on the statistic distributions of image differ-
ences, which are different for the two problems. A series of
snapshots acquired during training would determine an
average stimulus that would be spatially distinct between
the above and the below training. Furthermore, if bees
relied on a simple cue like the center of gravity of the
patterns [71], which would be associated with reward, the
problem becomes elemental. These alternative interpreta-
tions were excluded one by one by further experiments
specifically conceived for this aim [32].
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These results showed that the honey bee possesses the
faculty to extract a conceptual above/below relationship
from a set of training stimuli and to transfer this concept to
newly encountered stimuli. This faculty can be useful in a
navigational context in which bees may decide routes
based on spatial relationships between landmarks, which
could be generalized to novel situations [72].
Mastering two concepts simultaneously
Processing several concepts simultaneously presupposes
an even higher level of cognitive sophistication than deal-
ing with one concept at a time. In a recent study [33], honey
bees were shown to rapidly master two abstract concepts
simultaneously, one based on spatial relationships (above/
below and right/left), and another based on the perception
of difference.
Bees that learned to classify visual targets using this
dual concept transferred their choices to unknown stimuli
that offered a best match in terms of dual-concept avail-
ability: their components presented the appropriate spa-
tial relationship and differed from one another. As in the
previous study [32], a series of internal within-subject
controls and simulation algorithms allowed researchers
to exclude confounding low-level cues such as the global
center of gravity, the global orientation of the stimuli, and
the retinotopic similarity between the rewarded stimuli.
These results thus demonstrated that the miniature brains
of bees can extract abstract at least two different concepts
from a set of complex pictures and combine them in a rule
for subsequent choices [33].
Neural bases of concept learning in insects
Neural correlates of rules have been reported in the pre-
frontal cortex of both monkeys and rodents [73–75]. In the
dorsolateral, ventrolateral, and orbitofrontal prefrontal
cortex of monkeys, electrophysiological recordings showed
the presence of neurons exhibiting greater activity during
sameness trials (DMTS) as well as neurons showing great-
er activity during difference trials (DNMTS), regardless of
which visual sample was used to build the sameness/
difference relationship [75]. In the case of insects, with
no prefrontal cortex, the critical question is which neural
architecture could mediate this performance. Given that
stimulus transfer occurs between distinct sensory modali-
ties such as olfaction and vision [31], a neural candidate
should, like the prefrontal cortex of primates, receive
segregated multisensory input, be associated with rein-
forcement systems, and display an intrinsic relationship
with memory systems [76]. Additionally, it should provide
multimodal output consistent with response transfer to
stimuli belonging to different domains. These require-
ments are met by the mushroom bodies of honey bees.
These central structures of the bee brain exhibit multiple
parallel neuron architecture indicative of higher-order
integration (Figure 4). In the bee, each mushroom body
comprises approximately 170 000 tightly packed, parallel
neurons called Kenyon cells. The bee mushroom bodies
receive compartmentalized multisensory input (olfactory,
visual, mechanosensory, gustatory) [77–80] and their ex-
trinsic neurons, such as the Pe1 neuron, respond to various
stimuli including sucrose, odors, mechanosensory, and
 Review
Kenyon cell
somata
Lip
Olf.
Calyx
Vis.
ring Collar Mech.gust.
Basal
Mech.gust.
Olf.
Medial (β) lobe
Figure 4. Scheme of a mushroom body (delineated by dashed straight lines) showing segregated multisensory input at the level of the calyx and integrated multimodal
output at the level of the vertical (a) lobe. The somata of the Kenyon cells (KCs), which integrate the mushroom body, are located in the calyx bowl. The dendrites of the KCs
form the calyx, which is subdivided into three main regions: the lip, receiving olfactory afferences; the collar, receiving mainly visual but also mechanosensory and
gustatory afferences; and the basal ring, receiving olfactory, mechanosensory, and gustatory afferences [77,79,80]. The axons of the KCs subdivide and form the vertical (a)
and medial (b) lobes. An extrinsic, multimodal pedunculus neuron, the Pe1 neuron [81,97,98], is shown, whose dendrites arborize across the vertical lobe; its axon projects
to the lateral horn (delineated by a dashed circle).
visual [81–83] (Figure 4). This multimodal convergence
is consistent with a capacity for integrating sensory infor-
mation across various modalities and mushroom body
subcompartments and equips the mushroom bodies for
higher-order multimodal computations; in particular, for
relational associations. Furthermore, the mushroom bodies
are tightly related to reinforcement systems (Figure 2).
In the bee, octopaminergic neurons such as the ventral
unpaired median neuron of the maxillary neuromere 1
(VUMmx1), which serves as an appetitive reinforcement
system, converge with the regions of olfactory input of the
mushroom bodies. Activity in the VUMmx1 neuron substi-
tutes for sucrose in the olfactory conditioning of the PER [84]
and thus may be the specialized reward system for olfactory
cues. Also, dopaminergic neurons, which act as a punish-
ment system [20,55,57,85], converge with specific regions of
the mushroom bodies [55,56], thereby mediating aversive
memories of an odor-shock association of differing temporal
stability [86]. Finally, mushroom bodies have been histori-
cally characterized as a substrate for associative memories,
particularly LTMs [87–89].
In summary, the question of whether the mushroom
bodies are the insect equivalent of the primate prefrontal
cortex is irrelevant, even if studies of the prefrontal cortex
might inspire research on mushroom body function and
Trends in Neurosciences May 2013, Vol. 36, No. 5
Mushroom
body
(α) lobe
Vercal
Lateral
Pe1 neuron horn
(extrinsic neuron)
TRENDS in Neurosciences
vice versa. The critical questions are whether and how
mushroom body architecture is crucial in mediating con-
cept learning and which neural requisites are important
for the extraction of relational rules. From this perspective,
experiments addressing, through specific mushroom body
blocking and activation, whether these structures are nec-
essary and sufficient for concept learning are of fundamen-
tal importance.
Concluding remarks
The present review highlights novel studies of insect asso-
ciative learning that in most cases had the intention of
transcending the traditional framework of research on
simple stimulus–stimulus (or behavior–stimulus) associa-
tions. They all represent a relatively new tendency of
appreciating the cognitive sophistication of the miniature
brains of insects [4,90–94]. Such a tendency is welcome in a
field where the focus on simple learning forms may have
sometimes overlooked the enormous richness of inverte-
brate behavior. The rigidity of some experimental designs
frequently used in the laboratory to study insect behavior
leads to a danger that the restricted animal can only do
what the experimenter allows it to. Concluding from such
experiments that this is the only behavior the animal
possesses may be fundamentally wrong.
291
Review
Box 1. Outstanding questions
 Experiments on elemental and non-elemental learning have
concentrated on few insect species (mainly bees, fruit flies,
moths, cockroaches, parasitoid wasps, crickets, and ants). In-
creasing the number of species studied should allow the
determination of species-specific differences and common me-
chanisms of learning and memory formation. The huge variety of
species and ecological niches occupied by insects should
stimulate an ecological and evolutionary analysis of the neuro-
biology of neural circuits underlying learning and memory.
 Studies revealing higher-order, non-elemental learning in insects
have been conducted almost exclusively in a single species, the
honey bee A. mellifera. Are honey bees special with respect to
other insects in cognitive terms? Which role do sociality and
central-place navigation (the necessity of always returning to a
constant point in space, the hive) play in the development of
cognitive skills in bees?
 To what extent are higher-order learning capacities uncovered by
experiments in insects applied in the day-to-day activities
performed by these insects? Do they all have an adaptive value?
Or are they the result of neural wiring whose primary function is
different but which nevertheless allows the emergence of these
capacities (exaptation)?
 So far, studies of attention in fruit flies have suggested a role of
dopaminergic signaling in attentional modulation. Do other
biogenic amines/neurotransmitters modulate attention in insects?
How do stress, experience, and reinforcements affect attention in
the insect brain?
 Why do mushroom bodies have two calyces and a fused
pedunculus in some species and a single calyx and pedunculus
in other species? Does this difference relate to relational (includ-
ing spatial) learning capacities and demands?
 Mushroom bodies in the fruit fly D. melanogaster are unimodal
and devoted to olfactory processing, whereas they are multi-
modal and process visual, olfactory, gustatory, and mechanosen-
sory information in honey bees. Does this difference account for
differences in behavioral sophistication between these two
species?
 Are there neurons in the insect brain that are directly related to
concept and context-dependent learning?
 Can insects reveal the minimal neural architecture mediating
concept learning and other forms of higher-order learning?
Yet, as underlined in this review, not all feats presented
as highly cognitive are in fact distinct from non-elemental
learning forms. A fundamental goal in conceiving and
interpreting complex insect behavior is, therefore, critical-
ly to determine whether basic levels of interpretation are
possible and to what extent they account for plastic insect
behavior. Additionally, it is important to implement a
strict agenda in which the use of anthropocentric terms
should be avoided when interpreting insect behavior.
Focusing on the neural bases of insect higher-order learn-
ing is a way to avoid this, because the characterization of
neural architectures should be a dispassionate endeavor.
The study of simple learning forms in insects, both
appetitive and aversive, has shed light on how neural
circuits interact to produce plastic behavior and which
functional and structural changes occur at different stages
of these circuits to support elemental learning and memory
formation. Although many outstanding questions await an
answer (Box 1), two basic neural architectural principles
that many invertebrate brains share with larger brains are
the existence of specialized brain structures and circuits,
which refer to specific sensory domains, and of higher-
order integration centers, in which information pertaining
to these different domains converges and is integrated,
292
Trends in Neurosciences May 2013, Vol. 36, No. 5
thus allowing crosstalking and information transfer. These
characteristics may allow positive transfer from a set of
stimuli to novel ones, even if these belong to different
sensory modalities. This principle seems crucial for certain
tasks such as rule learning. With this in mind, a qualitative
step forward in the study of these phenomena would be to
integrate this knowledge in a characterization of the neu-
ral architectures that make non-elemental learning forms
possible in insects.
Acknowledgments
The author thanks all members of his research team at the University of
Toulouse for providing a stimulating and productive environment. He
also thanks the French Research Council (CNRS), the University of
Toulouse and the Institut Universitaire de France (IUF) for support.
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