Color-advertising strategies of invasive plants through the bee eye.

Invasive plants represent a significant global challenge as they compete with native plants for limited resources such as space, nutrients and pollinators. Here, we focused on four invasive species that are widely spread in the French Pyrenees, Buddleja davidii, Reynoutria japonica, Spiraea japonica and Impatiens glandulifera, and analyzed their visual advertisement signals with respect to those displayed by their surrounding native species using a perceptual approach based on the neural mechanisms of bee vision given that bees are regular pollinators of these plants. We collected 543 spectral reflections from the 4 invasive species, and 66 native species and estimated achromatic and chromatic similarities to the bee eye. R. japonica, S. japonica and B. davidii were inconspicuous against the foliage background and could be hardly discriminated in terms of color from their surrounding native plants. These characteristics promote generalization, potentially attracting pollinators foraging on similar native species. Two morphs of I. glandulifera were both highly salient in chromatic and achromatic terms and different from their surrounding native species. This distinctive identity facilitates detection and learning in association with rich nectar. While visual signals are not the only sensory cue accounting for invasive-plant success, our study reveals new elements for understanding biological invasion processes from the perspective of pollinator perceptual processes.

Mechanisms and rules of social learning in crickets.

A new study on insect social learning shows that crickets learn to prefer a rewarded odorant by observing the choice of a conspecific and without experiencing the reward themselves. The mere perception of the conspecific activates octopaminergic reward neurons in the brain of the observer, thus facilitating odorant learning.

Response to comment on "Food Wanting is Mediated by Transient Activation of Dopaminergic Signaling in the Honeybee Brain".

In a technical comment, Barron et al. (1) criticized the work of Huang et al. (2) putting the accent on the quantification of dopamine levels via high-performance liquid chromatography (HPLC), yet also including data interpretation through alternative hypotheses aimed at invalidating the original ones proposed by Huang et al. We thank the authors of this technical comment, which allows us to clarify technical aspects of our work that may have been unclear, and for promoting discussion around the conclusions of our work. Below we provide answers to the points raised in their comment.

A behavioral tagging account of kinase contribution to memory formation after spaced aversive training.

Long-term memory (LTM) can be induced by repeated spaced training trials. Using the weak inhibitory avoidance (wIA) task, we showed that one wIA session does not lead to a 24-h LTM, whereas two identical wIA sessions spaced by 15 min to 6 h induce a 24-h LTM. This LTM promotion depends both on hippocampal protein synthesis and the activity of several kinases. In agreement with the behavioral tagging (BT) hypothesis, our results suggest that the two training sessions induce transient learning tags and lead, via a cooperative effect, to the synthesis of plasticity-related proteins (PRPs) that become available and captured by the tag from the second session. Although ERKs1/2 are needed for PRPs synthesis and CaMKs are required for tag setting, PKA participates in both processes. We conclude that the BT mechanism accounts for the molecular constraints underlying the classic effect of spaced learning on LTM formation.

Neuroethology: Perceived danger inhibits the wanting system of bees.

A dopaminergic wanting system drives foraging in honey bees. A new study shows that encounters with the Asian hornet, a fierce bee predator, decrease brain dopamine levels and thus foraging. Stop signals, used to terminate the waggle dances of receivers, have the same effect, showing the power of bee communication.

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.

A cognitive account of trace conditioning in insects.

Trace conditioning is a form of Pavlovian learning in which the conditioned stimulus (CS) and the unconditioned stimulus (US) are separated by a temporal gap. Insects learn trace associations of variable nature (appetitive, aversive) and involving CSs of different sensory modalities (olfactory, visual). The accessibility of the insect neural system in behaving animals allowed identifying neural processes driving trace conditioning: the existence of prolonged neural responses to the CS after stimulus offset and the anticipation of US responses during the free-stimulus gap. Specific brain structures, such as the mushroom bodies seem to be allocated to this learning form. Here, we posit that a further component facilitating trace conditioning in insects relates to neuromodulatory mechanisms underlying enhanced attention. We thus propose a model based on different types of mushroom-body neurons, which provides a cognitive account of trace conditioning in insects.

Neonicotinoid effects on tropical bees: Imidacloprid impairs innate appetitive responsiveness, learning and memory in the stingless bee Melipona quadrifasciata.

Together with other anthropogenic factors, pesticides play a major role in pollinator decline worldwide. Most studies on their influence on pollinators have focused on honey bees given the suitability of this insect for controlled behavioral testing and raising. Yet, studies on pesticide impact should also contemplate tropical species, which contribute a major part of biodiversity and which have remained so far neglected. Here we focused on the stingless bee Melipona quadrifasciata and asked if the widely used neonicotinoid imidacloprid disrupts its learning and memory capabilities. We fed stingless bees with 0.1, 0.5 or 1 ng of imidacloprid, tested their innate appetitive responsiveness and trained them to associate odors and sucrose reward using the olfactory conditioning of the proboscis extension response. The same experiments were performed on Africanized honey bees. One hour after intoxication, both species decreased their innate responsiveness to sucrose but the effect was more accentuated in stingless bees. In both species, learning and memory were affected in a dose-dependent manner. These results indicate that pesticides have dramatic consequences on tropical bee species and claim for rational policies regulating their use in the tropics.

Efficient visual learning by bumble bees in virtual-reality conditions: Size does not matter.

Recent developments allowed establishing virtual-reality (VR) setups to study multiple aspects of visual learning in honey bees under controlled experimental conditions. Here, we adopted a VR environment to investigate the visual learning in the buff-tailed bumble bee Bombus terrestris. Based on responses to appetitive and aversive reinforcements used for conditioning, we show that bumble bees had the proper appetitive motivation to engage in the VR experiments and that they learned efficiently elemental color discriminations. In doing so, they reduced the latency to make a choice, increased the proportion of direct paths toward the virtual stimuli and walked faster toward them. Performance in a short-term retention test showed that bumble bees chose and fixated longer on the correct stimulus in the absence of reinforcement. Body size and weight, although variable across individuals, did not affect cognitive performances and had a mild impact on motor performances. Overall, we show that bumble bees are suitable experimental subjects for experiments on visual learning under VR conditions, which opens important perspectives for invasive studies on the neural and molecular bases of such learning given the robustness of these insects and the accessibility of their brain.

Individual consistency in the learning abilities of honey bees: cognitive specialization within sensory and reinforcement modalities.

The question of whether individuals perform consistently across a variety of cognitive tasks is relevant for studies of comparative cognition. The honey bee (Apis mellifera) is an appropriate model to study cognitive consistency as its learning can be studied in multiple elemental and non-elemental learning tasks. We took advantage of this possibility and studied if the ability of honey bees to learn a simple discrimination correlates with their ability to solve two tasks of higher complexity, reversal learning and negative patterning. We performed four experiments in which we varied the sensory modality of the stimuli (visual or olfactory) and the type (Pavlovian or operant) and complexity (elemental or non-elemental) of conditioning to examine if stable correlated performances could be observed across experiments. Across all experiments, an individual's proficiency to learn the simple discrimination task was positively and significantly correlated with performance in both reversal learning and negative patterning, while the performances in reversal learning and negative patterning were positively, yet not significantly correlated. These results suggest that correlated performances across learning paradigms represent a distinct cognitive characteristic of bees. Further research is necessary to examine if individual cognitive consistency can be found in other insect species as a common characteristic of insect brains.

Pollinator cognition: Framing bee memories in an ecological context.

Bee memory has been well characterized in laboratory experiments, but its relevance for foraging in an ecological context is less well studied. A new study shows that short-term memory in bumble bees correlates with springtime foraging efficiency, when floral resources are abundant, but not with summer foraging efficiency, when resources are scarce.

An insect brain organizes numbers on a left-to-right mental number line.

The "mental number line" (MNL) is a form of spatial numeric representation that associates small and large numbers with the left and right spaces, respectively. This spatio-numeric organization can be found in adult humans and has been related to cultural factors such as writing and reading habits. Yet, both human newborns and birds order numbers consistently with an MNL, thus raising the question of whether culture is a main explanation for MNL. Here, we explored the numeric sense of honey bees and show that after being trained to associate numbers with a sucrose reward, they order numbers not previously experienced from left to right according to their magnitude. Importantly, the location of a number on that scale varies with the reference number previously trained and does not depend on low-level cues present on numeric stimuli. We provide a series of neural explanations for this effect based on the extensive knowledge accumulated on the neural underpinnings of visual processing in honey bees and conclude that the MNL is a form of numeric representation that is evolutionarily conserved across nervous systems endowed with a sense of number, irrespective of their neural complexity.

Flies maintain idiosyncratic learning proficiency across odor-discrimination tasks.

Although insects of a same species appear similar when seen through human eyes, they exhibit considerable differences in behavioral performances, including learning success in conditioning tasks. New work on olfactory conditioning in fruit flies Drosophila melanogaster shows that these insects vary in their idiosyncratic learning proficiency and that this proficiency is consistent across days and variants of the trained task, thus uncovering the existence of different learning profiles within groups of flies.

Martin Giurfa.

Interview with Martin Giurfa, who studies learning and memory in insects at Paul Sabatier University.

Neuroscience: Mechanisms for bridging stimuli in Pavlovian trace conditioning in flies.

A recent study revealed neural mechanisms underlying visual trace conditioning in flies. To associate visual stimuli with heat punishment, the activity of visual- and heat-processing circuits was extended into the gap between them. Distractors delivered during the gap disrupted learning, raising the question of the cognitive processes at play.

Food wanting is mediated by transient activation of dopaminergic signaling in the honey bee brain.

The biological bases of wanting have been characterized in mammals, but whether an equivalent wanting system exists in insects remains unknown. In this study, we focused on honey bees, which perform intensive foraging activities to satisfy colony needs, and sought to determine whether foragers leave the hive driven by specific expectations about reward and whether they recollect these expectations during their waggle dances. We monitored foraging and dance behavior and simultaneously quantified and interfered with biogenic amine signaling in the bee brain. We show that a dopamine-dependent wanting system is activated transiently in the bee brain by increased appetite and individual recollection of profitable food sources, both en route to the goal and during waggle dances. Our results show that insects share with mammals common neural mechanisms for encoding wanting of stimuli with positive hedonic value.

The Neural Signature of Visual Learning Under Restrictive Virtual-Reality Conditions.

Honey bees are reputed for their remarkable visual learning and navigation capabilities. These capacities can be studied in virtual reality (VR) environments, which allow studying performances of tethered animals in stationary flight or walk under full control of the sensory environment. Here, we used a 2D VR setup in which a tethered bee walking stationary under restrictive closed-loop conditions learned to discriminate vertical rectangles differing in color and reinforcing outcome. Closed-loop conditions restricted stimulus control to lateral displacements. Consistently with prior VR analyses, bees learned to discriminate the trained stimuli. Ex vivo analyses on the brains of learners and non-learners showed that successful learning led to a downregulation of three immediate early genes in the main regions of the visual circuit, the optic lobes (OLs) and the calyces of the mushroom bodies (MBs). While Egr1 was downregulated in the OLs, Hr38 and kakusei were coincidently downregulated in the calyces of the MBs. Our work thus reveals that color discrimination learning induced a neural signature distributed along the sequential pathway of color processing that is consistent with an inhibitory trace. This trace may relate to the motor patterns required to solve the discrimination task, which are different from those underlying pathfinding in 3D VR scenarios allowing for navigation and exploratory learning and which lead to IEG upregulation.

The short neuropeptide F (sNPF) promotes the formation of appetitive visual memories in honey bees.

Motivation can critically influence learning and memory. Multiple neural mechanisms regulate motivational states, among which signalling via specific neuropeptides, such as NPY in vertebrates and NPF and its short variant sNPF in invertebrates, plays an essential role. The honey bee (Apis mellifera) is a privileged model for the study of appetitive learning and memory. Bees learn and memorize sensory cues associated with nectar reward while foraging, and their learning is affected by their feeding state. However, the neural underpinnings of their motivational states remain poorly known. Here we focused on the short neuropeptide F (sNPF) and studied if it modulates the acquisition and formation of colour memories. Artificially increasing sNPF levels in partially fed foragers with a reduced motivation to learn colours resulted in significant colour learning and memory above the levels exhibited by starved foragers. Our results thus identify sNPF as a critical component of motivational processes involved in foraging and in the cognitive processes associated with this activity in honey bees.