Differential conditioning and long-term olfactory memory in individual Camponotus fellah ants

Individual Camponotus fellah ants perceive and learn odours in a Y-maze in which one odour is paired with sugar (CS+) while a different odour (CS-) is paired with quinine (differential conditioning). We studied olfactory retention in C. fellah to determine whether olfactory learning leads to long-term memory retrievable 24h and 72 h after training. One and 3days after training, ants exhibited robust olfactory memory through a series of five successive retention tests in which they preferred the CS+ and stayed longer in the arm presenting it. In order to determine the nature of the associations memorized, we asked whether choices within the Y-maze were driven by excitatory memory based on choosing the CS+ and/or inhibitory memory based on avoiding the CS-. By confronting ants with a novel odour vs either the CS+ or the CS- we found that learning led to the formation of excitatory memory driving the choice of the CS+ but no inhibitory memory based on the CS- was apparent. Ants even preferred the CS- to the novel odour, thus suggesting that they used the CS- as a contextual cue in which the CS+ was embedded, or as a second-order cue predicting the CS+ and thus the sugar reward. Our results constitute the first controlled account of olfactory long-term memory in individual ants for which the nature of associations could be precisely characterized.Fil:Josens, R. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.Fil:Giurfa, M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina

Information Certainty Determines Social and Private Information Use in Ants

Decision-making in uncertain environments requires animals to evaluate, contrast and integrate various information sources to choose appropriate actions. In consensus-making groups, quorum responses are commonly used to combine private and social information, leading to both robust and flexible decisions. Here we show that in house-hunting ant colonies, individuals fine-tune the parameters of their quorum responses depending on their private knowledge: informed ants evaluating a familiar new nest rely relatively more on social than private information when the certainty of their private information is low, and vice versa. This indicates that the ants follow a highly sophisticated `copywhen-uncertain' social learning strategy similar to that observed in a few vertebrate species. Using simulations, we further show that this strategy improves colony performance during emigrations and confers well-informed individuals more weight in the decision process, thus representing a novel mechanism for the emergence of leadership in collective decision-making

Cognitive adaptation in asexual and sexual wasps living in contrasted environments.

Differences in learning and memory dynamics between populations are suspected to result from differences in ecological constraints such as resource distribution. The two reproductive modes (strains) of the parasitoid wasp Venturia canescens share the same geographical areas but live in contrasting habitats: arrhenotokous wasps live in the wild (generally orchards), whereas thelytokous ones live mostly in stored-products buildings (e.g. granaries). This species thus represents a relevant biological model for understanding the relationship between the ecological constraints faced by a species and its memory and learning ability. We showed that after having laid eggs in presence of both a synthetic odour and natural olfactory cues of their host, arrhenotokous wasps exhibited a change in their behavioural response towards the synthetic odour that was at least as pronounced as in thelytokous ones even though they were faster in their decision-making process. This is consistent with better learning skills in arrhenotokous wasps. The corresponding memory trace persisted in both strains for at least 51 h. We compare and discuss the learning and memory ablities of both strains as a function of their costs and benefits in their preferential habitats

Syntax-induced pattern deafness

Perceptual systems often force systematically biased interpretations upon sensory input. These interpretations are obligatory, inaccessible to conscious control, and prevent observers from perceiving alternative percepts. Here we report a similarly impenetrable phenomenon in the domain of language, where the syntactic system prevents listeners from detecting a simple perceptual pattern. Healthy human adults listened to three-word sequences conforming to patterns readily learned even by honeybees, rats, and sleeping human neonates. Specifically, sequences either started or ended with two words from the same syntactic category (e.g., noun–noun–verb or verb–verb–noun). Although participants readily processed the categories and learned repetition patterns over nonsyntactic categories (e.g., animal–animal–clothes), they failed to learn the repetition pattern over syntactic categories, even when explicitly instructed to look for it. Further experiments revealed that participants successfully learned the repetition patterns only when they were consistent with syntactically possible structures, irrespective of whether these structures were attested in English or in other languages unknown to the participants. When the repetition patterns did not match such syntactically possible structures, participants failed to learn them. Our results suggest that when human adults hear a string of nouns and verbs, their syntactic system obligatorily attempts an interpretation (e.g., in terms of subjects, objects, and predicates). As a result, subjects fail to perceive the simpler pattern of repetitions—a form of syntax-induced pattern deafness that is reminiscent of how other perceptual systems force specific interpretations upon sensory input

Sex and lifestyle dictate learning performance in a neotropical wasp

In contrast to extensive investigations on bee cognition, the cognitive capacities of wasps remain largely unexplored despite their key role as pollinators and predators of insect pests. Here we studied learning and memory in the neotropical wasp Mischocyttarus cerberus using a Pavlovian conditioning in which harnessed wasps respond with conditioned movements of their mouthparts to a learned odorant. We focused on the different castes, sexes, and ages coexisting within a nest and found that adults of M. cerberus learned and memorized efficiently the odor-sugar associations. In contrast, newly emerged females, but not males, were unable to learn odorants. This difference concurs with their different lifestyle as young males perform regular excursions outside the nest while young females remain in it until older age. Our results thus highlight the importance of socio-ecological constraints on wasp cognition and set the basis for mechanistic studies on learning differences across ages and castes

Strategies of the honeybee Apis mellifera during visual search for vertical targets presented at various heights: a role for spatial attention?

When honeybees are presented with a colour discrimination task, they tend to choose swiftly and accurately when objects are presented in the ventral part of their frontal visual field. In contrast, poor performance is observed when objects appear in the dorsal part. Here we investigate if this asymmetry is caused by fixed search patterns or if bees can use alternative search mechanisms such as spatial attention, which allows flexible focusing on different areas of the visual field. We asked individual honeybees to choose an orange rewarded target among blue distractors. Target and distractors were presented in the ventral visual field, the dorsal field or both. Bees presented with targets in the ventral visual field consistently had the highest search efficiency, with rapid decisions, high accuracy and direct flight paths. In contrast, search performance for dorsally located targets was inaccurate and slow at the beginning of the test phase, but bees increased their search performance significantly after a few learning trials: they found the target faster, made fewer errors and flew in a straight line towards the target. However, bees needed thrice as long to improve the search for a dorsally located target when the target's position changed randomly between the ventral and the dorsal visual field. We propose that honeybees form expectations of the location of the target's appearance and adapt their search strategy accordingly. Different possible mechanisms of this behavioural adaptation are discussed.L.M. was recipient of a DOC-fFORTE fellowship of the Austrian Academy of Science at the Department of Integrative Zoology, University of Vienna. L.C. is supported by an ERC Advanced Grant and a Royal Society Wolfson Research Merit Award

Aversive Learning in Honeybees Revealed by the Olfactory Conditioning of the Sting Extension Reflex

Invertebrates have contributed greatly to our understanding of associative learning because they allow learning protocols to be combined with experimental access to the nervous system. The honeybee Apis mellifera constitutes a standard model for the study of appetitive learning and memory since it was shown, almost a century ago, that bees learn to associate different sensory cues with a reward of sugar solution. However, up to now, no study has explored aversive learning in bees in such a way that simultaneous access to its neural bases is granted. Using odorants paired with electric shocks, we conditioned the sting extension reflex, which is exhibited by harnessed bees when subjected to a noxious stimulation. We show that this response can be conditioned so that bees learn to extend their sting in response to the odorant previously punished. Bees also learn to extend the proboscis to one odorant paired with sugar solution and the sting to a different odorant paired with electric shock, thus showing that they can master both appetitive and aversive associations simultaneously. Responding to the appropriate odorant with the appropriate response is possible because two different biogenic amines, octopamine and dopamine subserve appetitive and aversive reinforcement, respectively. While octopamine has been previously shown to substitute for appetitive reinforcement, we demonstrate that blocking of dopaminergic, but not octopaminergic, receptors suppresses aversive learning. Therefore, aversive learning in honeybees can now be accessed both at the behavioral and neural levels, thus opening new research avenues for understanding basic mechanisms of learning and memory

Mechanisms, functions and ecology of colour vision in the honeybee.

notes: PMCID: PMC4035557types: Journal Article© The Author(s) 2014.This is an open access article that is freely available in ORE or from Springerlink.com. Please cite the published version available at: http://link.springer.com/article/10.1007%2Fs00359-014-0915-1Research in the honeybee has laid the foundations for our understanding of insect colour vision. The trichromatic colour vision of honeybees shares fundamental properties with primate and human colour perception, such as colour constancy, colour opponency, segregation of colour and brightness coding. Laborious efforts to reconstruct the colour vision pathway in the honeybee have provided detailed descriptions of neural connectivity and the properties of photoreceptors and interneurons in the optic lobes of the bee brain. The modelling of colour perception advanced with the establishment of colour discrimination models that were based on experimental data, the Colour-Opponent Coding and Receptor Noise-Limited models, which are important tools for the quantitative assessment of bee colour vision and colour-guided behaviours. Major insights into the visual ecology of bees have been gained combining behavioural experiments and quantitative modelling, and asking how bee vision has influenced the evolution of flower colours and patterns. Recently research has focussed on the discrimination and categorisation of coloured patterns, colourful scenes and various other groupings of coloured stimuli, highlighting the bees' behavioural flexibility. The identification of perceptual mechanisms remains of fundamental importance for the interpretation of their learning strategies and performance in diverse experimental tasks.Biotechnology and Biological Sciences Research Council (BBSRC