[Calcium and olfaction in an insect model: activity marker and actor of plasticity].
Explore the source record for details and available documents.
Animals↗
Biomedical subjects
Martin Giurfa
Publications and source records attributed to Martin Giurfa.
The trial-spacing effect in olfactory patterning discriminations in honeybees.
Harnessed bees conditioned to associate odors and sucrose reward learn to discriminate between olfactory mixtures and their odor components in negative (NP: A+, B+, AB-) and positive (PP: A-, B-, AB+) patterning experiments. They thus extend the proboscis to the reinforced (CS+) but not to the non-reinforced (CS-) stimuli. Using the same protocol, we studied whether or not trials, which are spaced in time, are more effective in supporting patterning discrimination than massed trials which succeed fast to each other ('trial-spacing effect'). Training followed a NP (4 A+, 4 B+, 8 AB-) or a PP (4 A-, 4 B-, 8 AB+) schedule, with a 1:1 ratio between CS+ and CS- trials (8 CS+ and 8 CS- trials). ITIs of 1, 3, 5 and 8min were used in both tasks. Increasing ITI resulted in better differentiation between reinforced and non-reinforced CSs in both NP and PP tasks. However, whereas only the longest ITI of 8min allowed discrimination in NP, PP could already be solved with an ITI of 5min. This difference might be due to the fact that NP, but not PP, would require the formation of a unique cue and thus longer processing times. We thus show that the trial-spacing effect, previously demonstrated for single stimulus conditioning, also determines performance in patterning tasks in which three different stimuli (A, B, AB) alternate so that elements have to be discriminated from their compound.
Analysis of Variance↗
Associative learning: the instructive function of biogenic amines.
Biogenic amines like dopamine or octopamine modify neural function at multiple levels, sensitizing or depressing behaviour. Recent studies in insects have now shown that, besides a role in motivational modulation, biogenic amines substitute the reinforcer function in associative learning, thus instructing the nervous system about the relevance of external events.
Animals↗
Categorization of visual stimuli in the honeybee Apis mellifera.
Categorization refers to the classification of perceptual input into defined functional groups. We present and discuss evidence suggesting that stimulus categorization can also be found in an invertebrate, the honeybee Apis mellifera, thus underlining the generality across species of this cognitive process. Honeybees show positive transfer of appropriate responding from a trained to a novel set of visual stimuli. Such a transfer was demonstrated for specific isolated features such as symmetry or orientation, but also for assemblies (layouts) of features. Although transfer from training to novel stimuli can be achieved by stimulus generalization of the training stimuli, most of these transfer tests involved clearly distinguishable stimuli for which generalization would be reduced. Though in most cases specific experimental controls such as stimulus balance and discriminability are still required, it seems appropriate to characterize the performance of honeybees as reflecting categorization. Further experiments should address the issue of which categorization theory accounts better for the visual performances of honeybees.
Animals↗
Neural representation of olfactory mixtures in the honeybee antennal lobe.
Natural olfactory stimuli occur as mixtures of many single odors. We studied whether the representation of a mixture in the brain retains single-odor information and how much mixture-specific information it includes. To understand mixture representation in the honeybee brain, we used in vivo calcium imaging at the level of the antennal lobe, and systematically measured odor-evoked activity in 24 identified glomeruli in response to four single odorants and all their possible binary, ternary and quaternary mixtures. Qualitatively, mixture-induced activity patterns always contained glomeruli belonging to the pattern of at least one of the components, suggesting a high conservation of component information in olfactory mixtures. Quantitatively, glomerular activity saturated quickly and increasing the number of components resulted in an increase of cases in which the response of a glomerulus to the mixture was lower than that to the strongest component ('suppression'). This shows global inhibition in the antennal lobe, probably acting as overall gain control. Single components were not equally salient (in terms of number of active glomeruli) and mixture activity patterns were always more similar to the more salient components, in a way that could be predicted linearly. Thus, although a gain control system in the honeybee antennal lobe prevents saturation of the olfactory system, mixture representation follows essentially elemental rules.
Animals↗
Dimensions of cognition in an insect, the honeybee.
This review provides evidence for the enormous richness of insect behavior, its high flexibility, and the cross-talk between different behavioral routines. The memory structure established by multiple forms of learning represents sensory inputs and relates behaviors in such a way that representations of complex environmental conditions are formed. Navigation and communication in social hymenoptera are particularly telling examples in this respect, but it is fair to conclude that similar integrated forms of dealing with the environment will be found in other insects when they are studied more closely. In this sense, research addressing behavioral complexity and its underlying neural substrates is necessary to characterize the real potential of insect learning and memory. Usually, such an approach has been used to characterize behavioral simplicity rather than complexity. It seems therefore timely to focus on the latter by studying problem solving alongside and in addition to elemental forms of learning.
Animal Communication↗
Convergent evolution: floral guides, stingless bee nest entrances, and insectivorous pitchers.
Several recent hypotheses, including sensory drive and sensory exploitation, suggest that receiver biases may drive selection of biological signals in the context of sexual selection. Here we suggest that a similar mechanism may have led to convergence of patterns in flowers, stingless bee nest entrances, and pitchers of insectivorous plants. A survey of these non-related visual stimuli shows that they share features such as stripes, dark centre, and peripheral dots. Next, we experimentally show that in stingless bees the close-up approach to a flower is guided by dark centre preference. Moreover, in the approach towards their nest entrance, they have a spontaneous preference for entrance patterns containing a dark centre and disrupted ornamentation. Together with existing empirical evidence on the honeybee's and other insects' orientation to flowers, this suggests that the signal receivers of the natural patterns we examined, mainly Hymenoptera, have spontaneous preferences for radiating stripes, dark centres, and peripheral dots. These receiver biases may have evolved in other behavioural contexts in the ancestors of Hymenoptera, but our findings suggest that they have triggered the convergent evolution of visual stimuli in floral guides, stingless bee nest entrances, and insectivorous pitchers.
Animals↗
Spectral heterogeneity of honeybee ommatidia.
The honeybee compound eye is equipped with ultraviolet, blue, and green receptors, which form the physiological basis of a trichromatic color vision system. We studied the distribution of the spectral receptors by localizing the three mRNAs encoding the opsins of the ultraviolet-, blue- and green-absorbing visual pigments. The expression patterns of the three opsin mRNAs demonstrated that three distinct types ommatidia exist, refuting the common assumption that the ommatidia composing the bee compound eye contain identical sets of spectral receptors. We found that type I ommatidia contain one ultraviolet and one blue receptor, type II ommatidia contain two ultraviolet receptors, and type III ommatidia have two blue receptors. All the three ommatidial types contain six green receptors. The ommatidia appear to be distributed rather randomly over the retina. The ratio of type I, II, and III ommatidia was about 44:46:10. Type III ommatidia appeared to be slightly more frequent (18%) in the anterior part of the ventral region of the eye. Retinal heterogeneity and ommatidial randomness, first clearly demonstrated in butterflies, seems to be a common design principle of the eyes of insects.
Animals↗
The influence of training length on generalization of visual feature assemblies in honeybees.
Generalization is a fundamental cognitive ability that allows treating similar stimuli as equivalents, and thus responding to them in the same manner. Here, we show that after training free-flying bees with a single, constant pair of patterns made of four quadrants, each displaying different oriented gratings, bees extract the orientation information corresponding to each quadrant and integrate it in a generic layout that preserved the spatial relationship between oriented edges. Our results show that the amount of experience with the training patterns is critical to determine or not generalization to novel stimuli sharing the layout of the rewarded stimulus. Increasing experience results in higher generalization levels reflected in significant responding to novel stimuli. With ongoing training, redundant information seems to be eliminated and reduced to the minimum that is necessary and sufficient to solve the task. Controlling precisely the level of experience of individuals is therefore crucial in experiments on visual recognition.
Analysis of Variance↗
Perceptual and neural olfactory similarity in honeybees.
The question of whether or not neural activity patterns recorded in the olfactory centres of the brain correspond to olfactory perceptual measures remains unanswered. To address this question, we studied olfaction in honeybees Apis mellifera using the olfactory conditioning of the proboscis extension response. We conditioned bees to odours and tested generalisation responses to different odours. Sixteen odours were used, which varied both in their functional group (primary and secondary alcohols, aldehydes and ketones) and in their carbon-chain length (from six to nine carbons). The results obtained by presentation of a total of 16 x 16 odour pairs show that (i) all odorants presented could be learned, although acquisition was lower for short-chain ketones; (ii) generalisation varied depending both on the functional group and the carbon-chain length of odours trained; higher generalisation was found between long-chain than between short-chain molecules and between groups such as primary and secondary alcohols; (iii) for some odour pairs, cross-generalisation between odorants was asymmetric; (iv) a putative olfactory space could be defined for the honeybee with functional group and carbon-chain length as inner dimensions; (v) perceptual distances in such a space correlate well with physiological distances determined from optophysiological recordings of antennal lobe activity. We conclude that functional group and carbon-chain length are inner dimensions of the honeybee olfactory space and that neural activity in the antennal lobe reflects the perceptual quality of odours.
Afferent Pathways↗
Partial unilateral lesions of the mushroom bodies affect olfactory learning in honeybees Apis mellifera L.
The mushroom bodies (MBs) are central structures in the insect brain that have been associated with olfactory learning and memory. Here we used hydroxyurea (HU) to treat honeybee larvae and induce partial MB ablations at the adult stage. We studied olfactory learning in honeybees with unilateral loss of the median calyces of their MBs and compared their ability to solve different forms of olfactory discrimination. When odorants were delivered in a side-specific manner, ablated bees could not solve either discrimination of the unambiguous problem (Paradigm 1: A+, B- on one antenna, C+, D- on the other; A+B-/C+D-) whereas they could solve at least one of both discriminations of the ambiguous problem (Paradigm 2: A+B-/A-B+), namely that proposed to their intact brain side. Non-ablated bees could learn side-specific discriminations on both brain sides. When odorants were delivered simultaneously to both antennae (Paradigm 3: A+B-C+D-), HU-ablated bees learned slower than HU-normal bees. Thus, in all three paradigms, the unilateral loss of a median calyx affected olfactory learning. We propose that the MBs are required for solving elemental olfactory tasks whose complexity is increased by the number of stimuli involved and that MB ablations could have an effect on the inhibition of information exchange between brain hemispheres.
Animals↗
Electrophysiological and behavioural characterization of gustatory responses to antennal 'bitter' taste in honeybees.
We combined behavioural and electrophysiological experiments to study whether bitter taste is perceived at the antennal level in honeybees, Apis mellifera. Our behavioural studies showed that neither quinine nor salicin delivered at one antenna at different concentrations induced a retraction of the proboscis once it was extended in response to 1 M sucrose solution delivered to the opposite antenna. Bees that extended massively their proboscis to 1 M sucrose responded only partially when stimulated with a mixture of 1 M sucrose and 100 mM quinine. The mixture of 1 m sucrose and 100 mM salicin had no such suppressive effect. No behavioural suppression was found for mixtures of salt solution and either bitter substance. Electrophysiological recordings of taste sensillae at the antennal tip revealed sensillae that responded specifically either to sucrose or salt solutions, but none responded to the bitter substances quinine and salicin at the different concentrations tested. The electrophysiological responses of sensillae to 15 mM sucrose solution were inhibited by a mixture of 15 mM sucrose and 0.1 mM quinine, but not by a mixture of 15 mM sucrose and 0.1 mM salicin. The responses of sensillae to 50 mM NaCl were reduced by a mixture of 50 mm NaCl and 1 mM quinine but not by a mixture of 50 mM NaCl and 1 mM salicin. We concluded that no receptor cells for the bitter substances tested, exist at the level of the antennal tip of the honeybee and that antennal bitter taste is not represented as a separate perceptual quality.
Action Potentials↗
Symmetry is in the eye of the beeholder: innate preference for bilateral symmetry in flower-naïve bumblebees.
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.
Animal Feed↗
Local-feature assembling in visual pattern recognition and generalization in honeybees.
Generalization is a cognitive ability that allows similar stimuli along a given dimension to be treated as equivalents. Insects exhibit high levels of visual generalization. Honeybees trained to recognize complex visual stimuli on the basis of a single feature generalize their choice to novel stimuli sharing that common feature with the trained stimuli. The demonstration of this kind of performance has been limited to the use of a single visual feature, and the possibility that bees link different features in learning a visual pattern has been denied. Here we show that honeybees trained with a series of complex patterns sharing a common layout comprising four edge orientations remember these orientations simultaneously in their appropriate positions, and generalize their response to novel stimuli that preserve the trained layout. Honeybees also generalize their response to patterns with fewer correct orientations, depending on their match with the trained layout. Stimulation of the achromatic L-photoreceptor input is necessary for this task. The mini-brain of the honeybee can thus extract regularities in its environment and establish correspondences among correlated features. It can thus generate a large set of object descriptions from a finite set of elements.
Animals↗
Conditioning procedure and color discrimination in the honeybee Apis mellifera.
We studied the influence of the conditioning procedure on color discrimination by free-flying honeybees. We asked whether absolute and differential conditioning result in different discrimination capabilities for the same pairs of colored targets. In absolute conditioning, bees were rewarded on a single color; in differential conditioning, bees were rewarded on the same color but an alternative, non-rewarding, similar color was also visible. In both conditioning procedures, bees learned their respective task and could also discriminate the training stimulus from a novel stimulus that was perceptually different from the trained one. Discrimination between perceptually closer stimuli was possible after differential conditioning but not after absolute conditioning. Differences in attention inculcated by these training procedures may underlie the different discrimination performances of the bees.
Animals↗
The effect of cumulative experience on the use of elemental and configural visual discrimination strategies in honeybees.
We addressed the question of whether the amount of individual experience determines the use of elemental or configural visual discrimination strategies in free-flying honeybees Apis mellifera. We trained bees to fly into a Y-maze to collect sucrose solution on a rewarded stimulus presented in one of the arms of the maze. Stimuli were colour disks, violet (V), green (G) or yellow (Y), which were of equal psychophysical salience for honeybees. Training followed an A+, BC+ design, followed by an AC versus BC test. Training consisted of 6 (3 A+ and 3 BC+), 20 (10 A+ and 10 BC+) or 40 (20 A+ and 20 BC+) acquisition trials. Elemental models of compound processing predict a preference for the non-trained stimulus AC while configural models predict a preference for the trained stimulus BC. Our results show that increasing the number of acquisition trials results in a change of the internal representation of stimuli. After six training trials, bees favoured an elemental strategy and preferred AC to BC during the tests. Generally, increasing the number of training trials resulted in an increase of the choice of BC. Thus, short training favoured processing of the compound as the sum of its elements (elemental account) while long training favoured its processing as being different from the sum of its elements (configural account). Additionally, we observed that the change in stimulus processing was also influenced by stimulus similarity. Colour perceptual similarity favoured configural processing with increasing experience.
Animals↗
Non-elemental processing in olfactory discrimination tasks needs bilateral input in honeybees.
In patterning discriminations, animals have to differentiate a compound stimulus AB from each of its elements A and B. In positive patterning (PP), the compound is reinforced whilst the single elements are non-reinforced. In negative patterning (NP), single elements are reinforced whilst the compound is non-reinforced. Using olfactory conditioning of the proboscis extension response (PER), we asked whether honeybees (Apis mellifera) can solve these patterning problems when odorants are given unilaterally as well as bilaterally to the antennae. Separating the olfactory input space of bees into two independent zones using plastic walls placed between the antennae, we conditioned bees in PP and NP procedures, with input on one side, on both sides, or in an ambiguous problem where bees had to solve PP on one side and NP on the other side. We found that bees with simultaneous bilateral input solve both patterning tasks efficiently. In contrast, PP but not NP was learned by bees receiving unilateral olfactory input. Bees subjected to the ambiguous NP/PP problem only solved PP. As PP can be solved through mere elemental processes, but NP is critically dependent on the use of non-elemental learning processes, our results suggest that bilateral olfactory input is necessary for non-elemental processing to take place in the bee brain.
Animals↗
Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain.
The brain of a honeybee contains only 960,000 neurons and its volume represents only 1 mm3. However, it supports impressive behavioral capabilities. Honeybees are equipped with sophisticated sensory systems and have well developed learning and memory capacities, whose essential mechanisms do not differ drastically from those of vertebrates. Here, I focus on non-elemental forms of learning by honeybees. I show that bees exhibit learning abilities that have been traditionally ascribed to a restricted portion of vertebrates, as they go beyond simple stimulus-stimulus or response-stimulus associations. To relate these abilities to neural structures and functioning in the bee brain we focus on the antennal lobes and the mushroom bodies. We conclude that there is a fair chance to understand complex behavior in bees, and to identify the potential neural substrates underlying such behavior by adopting a cognitive neuroethological approach. In such an approach, behavioral and neurobiological studies are combined to understand the rules and mechanisms of plastic behavior in a natural context.
Animals↗