Martin Giurfa | Sorbonne University (original) (raw)

Papers by Martin Giurfa

Animal Behaviour, 2006

We studied olfactory learning in two ant species, Camponotus mus from Argentina and Camponotus fe... more We studied olfactory learning in two ant species, Camponotus mus from Argentina and Camponotus fellah from Israel. To this end, we established an experimental laboratory protocol in which individual ants were trained to associate odours with gustatory reinforcers. Ants were trained individually to forage in a Y-maze in which two odours had to be discriminated. One odour was positively reinforced with sucrose solution and the other was negatively reinforced with quinine solution. After a training session of 24 trials, ants of both species learned to differentiate the two odour pairs, the structurally dissimilar limonene and octanal, and the structurally similar heptanal and 2-heptanone. In nonreinforced tests, ants consistently chose the odour previously reinforced with sucrose solution and spent more time searching in the arm of the maze presenting this odour. Learning performances were more robust in the case of limonene versus heptanal. These results thus show for the first time that individual ants perceive and learn odours in controlled laboratory conditions.

Learning & Memory, 2009

Harnessed bees learn to associate an odorant with an electric shock so that afterward the odorant... more Harnessed bees learn to associate an odorant with an electric shock so that afterward the odorant alone elicits the sting extension response (SER). We studied the dependency of retention on interstimulus interval (ISI), intertrial interval (ITI), and number of conditioning trials in the framework of olfactory SER conditioning. Forward ISIs (conditioned stimulus [CS] before unconditioned stimulus [US]) supported higher retention than a backward one (US before CS) with an optimum around 3 sec. Spaced trials (ITI 10 min) supported higher retention than massed trials (ITI 1 min) and led to the formation of a late long-term memory (l-LTM) that depended on protein synthesis. Our results reaffirm olfactory SER conditioning as a reliable tool for the study of learning and memory. Email giurfa@cict.fr; fax 33-561-55-61-54. Article is online at

Wiley interdisciplinary reviews. Cognitive science

Insects possess small brains but exhibit sophisticated behavioral performances. Recent works have... more Insects possess small brains but exhibit sophisticated behavioral performances. Recent works have reported the existence of unsuspected cognitive capabilities in various insect species, which go beyond the traditional studied framework of simple associative learning. In this study, I focus on capabilities such as attention, social learning, individual recognition, concept learning, and metacognition, and discuss their presence and mechanistic bases in insects. I analyze whether these behaviors can be explained on the basis of elemental associative learning or, on the contrary, require higher-order explanations. 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 l architectures underlying cognitive processing.

Journal of Neurophysiology, Feb 1, 2010

Deisig N, Giurfa M, Sandoz JC. Antennal lobe processing increases separability of odor mixture re... more Deisig N, Giurfa M, Sandoz JC. Antennal lobe processing increases separability of odor mixture representations in the honeybee. Local networks within the primary olfactory centers reformat odor representations from olfactory receptor neurons to second-order neurons. By studying the rules underlying mixture representation at the input to the antennal lobe (AL), the primary olfactory center of the insect brain, we recently found that mixture representation follows a strict elemental rule in honeybees: the more a component activates the AL when presented alone, the more it is represented in a mixture. We now studied mixture representation at the output of the AL by imaging a population of second-order neurons, which convey AL processed odor information to higher brain centers. We systematically measured odor-evoked activity in 22 identified glomeruli in response to four single odorants and all their possible binary, ternary and quaternary mixtures. By comparing input and output responses, we determined how the AL network reformats mixture representation and what advantage this confers for odor discrimination. We show that increased inhibition within the AL leads to more synthetic, less elemental, mixture representation at the output level than that at the input level. As a result, mixture representations become more separable in the olfactory space, thus allowing better differentiation among floral blends in nature.

Journal of Experimental Biology, Nov 1, 2000

Honeybees, Apis mellifera, were trained to detect coloured disks with either a strong or a weak i... more Honeybees, Apis mellifera, were trained to detect coloured disks with either a strong or a weak intensity difference against the background. Green, blue, ultraviolet-reflecting white and grey papers were reciprocally combined as targets or backgrounds, providing strong chromatic and/or achromatic cues. The behavioural performance of the honeybees was always symmetrical for both reciprocal target/background combinations of a colour pair, thus showing that target detection is independent of whether the colour is presented as a background or as a target in combination with the other colour. Bright targets against dim backgrounds and vice versa were detected more reliably than dim target/background combinations. This result favours the general assumption that the detectability of a coloured stimulus increases with increasing intensity.

Psychophysiology, Sep 1, 2002

Two human Pavlovian conditioning experiments investigated the impact of reinforcement density~the... more Two human Pavlovian conditioning experiments investigated the impact of reinforcement density~the number of reinforced trials divided by the total number of trials! on discrimination learning. Experiment 1 used a negative patterning problem~Aϩ, Bϩ, ABϪ! and Experiment 2 used a positive patterning problem~AϪ, BϪ, ABϩ!. In both experiments, reinforcement density varied across four levels. Response differentiation between reinforced and nonreinforced stimuli was linearly related to the decrease in reinforcement density. Responses to nonreinforced stimuli did not differ between the four groups in either experiment. In contrast to this, responses to reinforced stimuli were considerably more pronounced in conditions with lower reinforcement density. For negative patterning, this replicates and extends similar observations from other species. For positive patterning, this is a finding that has not yet been reported in other experiments. The results are in agreement with the comparator hypothesis~Miller & Matzel, 1988! and with Wagner's~1981! "standard operating procedures"~SOP! model.

Scientific Reports, 2015

Natural odours are complex blends of numerous components. Understanding how animals perceive odou... more Natural odours are complex blends of numerous components. Understanding how animals perceive odour mixtures is central to multiple disciplines. Here we focused on carpenter ants, which rely on odours in various behavioural contexts. We studied overshadowing, a phenomenon that occurs when animals having learnt a binary mixture respond less to one component than to the other, and less than when this component was learnt alone. Ants were trained individually with alcohols and aldehydes varying in carbon-chain length, either as single odours or binary mixtures. They were then tested with the mixture and the components. Overshadowing resulted from the interaction between chain length and functional group: alcohols overshadowed aldehydes, and longer chain lengths overshadowed shorter ones; yet, combinations of these factors could cancel each other and suppress overshadowing. Our results show how ants treat binary olfactory mixtures and set the basis for predictive analyses of odour perception in insects.

The honey bee Apis mellifera is a robust model for the study of Pavlovian conditioning. The olfac... more The honey bee Apis mellifera is a robust model for the study of Pavlovian conditioning. The olfactory conditioning of the proboscis extension response (PER) is a fundamental tool for the study of Pavlovian learning in bees. We revisit olfactory PER conditioning and define a standardized framework for using this behavioral protocol. We present all the methodological details necessary for successful implementation of olfactory PER conditioning.

J Neurobiol, 2002

Hydroxyurea (HU) treatment of first instar honeybee larvae was previously shown to cause mushroom... more Hydroxyurea (HU) treatment of first instar honeybee larvae was previously shown to cause mushroom body (MB) ablations. Predominantly, either one or both median MB subunits were ablated. This prompted us to analyze the effects of asymmetrical or symmetrical HU-induced MB ablation on both the morphology of the brain and on the level of three proteins (synapsin, PKA RII, and PKC), which are considered to play a role in synaptic plasticity, learning, and memory. In brains with one median MB subunit missing the volume of the overall MB calyx neuropil in the lesioned side was diminished by 35%. This strong reduction occurred although the remaining lateral MB calyx of the lesioned brain side was found to be significantly larger than that of the intact side. Accordingly, in brains with both median MB subunits missing the size of the remaining lateral calyces increased. The various types of MB ablation differentially affected the amounts of synapsin, PKA RII, and PKC expressed in the central brain. In animals with bilateral and thus symmetrical MB ablation (both median calyces ablated) the protein amount was found to be similar to that in control animals. However, unilateral MB ablation causes an increase in the amounts of the tested proteins in the intact brain side, while the levels in the ablated side were the same as in control animals. These findings not only show that HU-induced ablation of MB subunits is accompanied by volume changes and by changes in protein expression, but also suggest that these processes are highly regulated between the brain sides. The latter is of general importance in understanding the potential contribution of the MB subunits to learning and memory and their interaction between the brain sides.

Plos One, Feb 1, 2008

Echolocating bats have successfully exploited a broad range of habitats and prey. Much research h... more Echolocating bats have successfully exploited a broad range of habitats and prey. Much research has demonstrated how time-frequency structure of echolocation calls of different species is adapted to acoustic constraints of habitats and foraging behaviors. However, the intensity of bat calls has been largely neglected although intensity is a key factor determining echolocation range and interactions with other bats and prey. Differences in detection range, in turn, are thought to constitute a mechanism promoting resource partitioning among bats, which might be particularly important for the species-rich bat assemblages in the tropics. Here we present data on emitted intensities for 11 species from 5 families of insectivorous bats from Panamá hunting in open or background cluttered space or over water. We recorded all bats in their natural habitat in the field using a multi-microphone array coupled with photographic methods to assess the bats' position in space to estimate emitted call intensities. All species emitted intense search signals. Output intensity was reduced when closing in on background by 4-7 dB per halving of distance. Source levels of open space and edge space foragers (Emballonuridae, Mormoopidae, Molossidae, and Vespertilionidae) ranged between 122-134 dB SPL. The two Noctilionidae species hunting over water emitted the loudest signals recorded so far for any bat with average source levels of ca. 137 dB SPL and maximum levels above 140 dB SPL. In spite of this ten-fold variation in emitted intensity, estimates indicated, surprisingly, that detection distances for prey varied far less; bats emitting the highest intensities also emitted the highest frequencies, which are severely attenuated in air. Thus, our results suggest that bats within a local assemblage compensate for frequency dependent attenuation by adjusting the emitted intensity to achieve comparable detection distances for prey across species. We conclude that for bats with similar hunting habits, prey detection range represents a unifying constraint on the emitted intensity largely independent of call shape, body size, and close phylogenetic relationships.

Naturwissenschaften, 2004

Bilateral symmetry has been considered as an indicator of phenotypic and genotypic quality suppor... more Bilateral symmetry has been considered as an indicator of phenotypic and genotypic quality supporting innate preferences for highly symmetric partners. Insect pollinators preferentially visit flowers of a particular symmetry type, thus leading to the suggestion that they have innate preferences for symmetrical flowers or flower models. Here we show that flower-naïve bumblebees (Bombus terrestris), with no experience of symmetric or asymmetric patterns and whose visual experience was accurately controlled, have innate preferences for bilateral symmetry. The presence of color cues did not influence the bees' original preference. Our results thus show that bilateral symmetry is innately preferred in the context of food search, a fact that supports the selection of symmetry in flower displays. Furthermore, such innate preferences indicate that the nervous system of naïve animals may be primed to respond to relevant sensory cues in the environment.

. Stimuli used in the study. (A) Achromatic stimuli used for training and testing. Six different ... more . Stimuli used in the study. (A) Achromatic stimuli used for training and testing. Six different patterns were used: a checkerboard, a radial four-sectored pattern, a horizontal grating, a vertical grating, and two concentric patterns (rings and squares). Patterns were 7 × 7 cm. Grating stripes, checkerboard squares, and concentric squares and rings were all 1 cm wide. Sectors in the radial pattern covered 2.5 cm in their largest extension. All achromatic patterns could be well resolved for honey bees. (B) Chromatic stimuli used for training and testing. Colors were cut from HKS papers 1N, 3N, 29N, 32N, 68N,and 71N (from left to right, upper to lower). These stimuli could also be well discriminated from each other. Color disks were 7 cm diameter. (C) Large achromatic and chromatic bars 7 × 18 cm used in transfer tests of the second experiment. Chromatic bars (two examples are shown) were cut from the same HKS-N papers used for the training color disks. (D) Training and testing procedure showing the variation in the center of gravity of patterns along a whole experiment. Centers of gravity are used by insects as a relevant cue for pattern discrimination. The center of gravity, shown at the intersection of the dashed lines, varied during training so that a rewarded spatial relationship had no constant center of gravity. Moreover, during the tests, the center of gravity of both alternatives was identical and centered on the back walls. Our procedure thus precluded the use of this cue as predictive information guiding the bees' choices.

Naturwissenschaften, 1993

... Yoshida, S., Uemura, M., Niki, T., Sakai, A., Gusta, LV: Plant Physiol. ... Since the pioneer... more ... Yoshida, S., Uemura, M., Niki, T., Sakai, A., Gusta, LV: Plant Physiol. ... Since the pioneer work of Karl von Frisch, much knowledge has been gained in relation to the different sensory modalities that a bee can exploit to attain a greater efficiency while foraging on a patch of flowers. ...

Learning Amp Memory, 2001

In an appetitive context, honeybees (Apis mellifera) learn to associate odors with a reward of su... more In an appetitive context, honeybees (Apis mellifera) learn to associate odors with a reward of sucrose solution. If an odor is presented immediately before the sucrose, an elemental association is formed that enables the odor to release the proboscis extension response (PER). Olfactory conditioning of PER was used to study whether, beyond elemental associations, honeybees are able to process configural associations. Bees were trained in a positive and anegative patterning discrimination problem. In the first problem, single odorants were nonreinforced whereas the compound was reinforced. In the second problem, single odorants were reinforced whereas the compound was nonreinforced. We studied whether bees can solve these problems and whether the ratio between the number of presentations of the reinforced stimuli and the number of presentations of the nonreinforced stimuli affects discrimination. Honeybees differentiated reinforced and nonreinforced stimuli in positive and negative patterning discriminations. They thus can process configural associations. The variation of the ratio of reinforced to nonreinforced stimuli modulated the amount of differentiation. The assignment of singular codes to complex odor blends could be implemented at the neural level: When bees are stimulated with odor mixtures, the activation patterns evoked at the primary olfactory neuropile, the antennal lobe, may be combinations of the single odorant responses that are not necessarily fully additive.

F1000posters, Oct 2, 2012

 The mini-brain of honeybees, as Humans', can use spatial configurations to classify and recogni... more  The mini-brain of honeybees, as Humans', can use spatial configurations to classify and recognize complex objects such as faces 1 .

The Journal of Experimental Biology, Feb 15, 2010

We studied whether honeybees can distinguish face-like configurations by using standardized stimu... more We studied whether honeybees can distinguish face-like configurations by using standardized stimuli commonly employed in primate and human visual research. Furthermore, we studied whether, irrespective of their capacity to distinguish between facelike stimuli, bees learn to classify visual stimuli built up of the same elements in face-like versus non-face-like categories. We showed that bees succeeded in discriminating both face-like and non-face-like stimuli and categorized appropriately novel stimuli in these two classes. To this end, they used configural information and not just isolated features or low-level cues. Bees looked for a specific configuration in which each feature had to be located in an appropriate spatial relationship with respect to the others, thus showing sensitivity for first-order relationships between features. Although faces are biologically irrelevant stimuli for bees, the fact that they were able to integrate visual features into complex representations suggests that face-like stimulus categorization can occur even in the absence of brain regions specialized in face processing.

Plos One, 2010

European honeybee (Apis mellifera L.) foragers have a highly developed visual system that is used... more European honeybee (Apis mellifera L.) foragers have a highly developed visual system that is used for navigation. To clarify the neural basis underlying the highly sophisticated visual ability of foragers, we investigated the neural activity pattern of the optic lobes (OLs) in pollen-foragers and re-orienting bees, using the immediate early gene kakusei as a neural activity marker. We performed double-in situ hybridization of kakusei and Amgad, the honeybee homolog of the GABA synthesizing enzyme GAD, to assess inhibitory neural activity. kakusei-related activity in GABAergic and non-GABAergic neurons was strongly upregulated in the OLs of the foragers and re-orienting bees, suggesting that both types of neurons are involved in visual information processing. GABAergic neuron activity was significantly higher than non-GABAergic neuron activity in a part of the OLs of only the forager, suggesting that unique information processing occurs in the OLs of foragers. In contrast, GABAergic neuron activity in the antennal lobe was significantly lower than that of GABAergic neurons in the OLs in the forager and re-orienting bees, suggesting that kakusei-related visual activity is dominant in the brains of these bees. The present study provides the first evidence that GABAergic neurons are highly active in the OL neurons of free-moving honeybees and essential clue to reveal neural basis of the sophisticated visual ability that is equipped in the small and simple brain.