Brain structure and learning capacities both vary with experience, but the mechanistic link between them is unclear. Here, we investigated whether experience-dependent variability in learning performance can be explained by neuroplasticity in foraging honey bees. The mushroom bodies (MBs) are a brain center necessary for ambiguous olfactory learning tasks such as reversal learning. Using radio frequency identification technology, we assessed the effects of natural variation in foraging activity, and the age when first foraging, on both performance in reversal learning and on synaptic connectivity in the MBs. We found that reversal learning performance improved at foraging onset and could decline with greater foraging experience. If bees started foraging before the normal age, as a result of a stress applied to the colony, the decline in learning performance with foraging experience was more severe. Analyses of brain structure in the same bees showed that the total number of synaptic boutons at the MB input decreased when bees started foraging, and then increased with greater foraging intensity. At foraging onset MB structure is therefore optimized for bees to update learned information, but optimization of MB connectivity deteriorates with foraging effort. In a computational model of the MBs sparser coding of information at the MB input improved reversal learning performance. We propose, therefore, a plausible mechanistic relationship between experience, neuroplasticity, and cognitive performance in a natural and ecological context.

Acetylcholine is the main excitatory neurotransmitter in the honeybee brain and controls a wide range of behaviours that ensure the survival of the individuals and of the entire colony. Neonicotinoid pesticides target this neurotransmission pathway and can thereby affect the behaviours under its control, even at doses far below the toxicity limit. These sublethal effects of neonicotinoids on honeybee behaviours were suggested to be partly responsible for the decline in honeybee populations. However, the neural mechanisms by which neonicotinoids influence single behaviours are still unclear. This is mainly due to the heterogeneity of the exposure pathways, doses and durations between studies. Here, we provide a review of the state of the science in this field and highlight knowledge gaps that need to be closed. We describe the agonistic effects of neonicotinoids on neurons expressing the different nicotinic acetylcholine receptors and the resulting brain structural and functional changes, which are likely responsible for the behavioural alterations reported in bees exposed to neonicotinoids.

Honey bees have emerged as a new model to study the gut–brain axis, as they exhibit complex social behaviors and cognitive abilities, while experiments with gnotobiotic bees have revealed that their gut microbiota alters both brain and behavioral phenotypes. Furthermore, while honey bee brain functions supporting a broad range of behaviors have been intensively studied for over 50 years, the gut microbiota of bees has been experimentally characterized only recently. Here, we combined six published datasets from metabolomic analyses to provide an overview of the neuroactive metabolites whose abundance in the gut, hemolymph and brain varies in presence of the gut microbiota. Such metabolites may either be produced by gut bacteria, released from the pollen grains during their decomposition by bacteria, or produced by other organs in response to different bacterial products. We describe the current state of knowledge regarding the impact of such metabolites on brain function and behavior and provide further hypotheses to explore in this emerging field of research.

The honey bee mushroom bodies (MBs) are brain centers required for specific learning tasks. Here, we show that environmental conditions experienced as young adults affect the maturation of MB neuropil and performance in a MB-dependent learning task. Specifically, olfactory reversal learning was selectively impaired following early exposure to an impoverished environment lacking some of the sensory and social interactions present in the hive. In parallel, the overall number of synaptic boutons increased within the MB olfactory neuropil, whose volume remained unaffected. This suggests that experience of the rich in-hive environment promotes MB maturation and the development of MB-dependent learning capacities.

Social insects exhibit a high degree of intraspecific behavioral variation. Moreover, they often harbor specialized microbial communities in their gut. Recent studies suggest that these two characteristics of social insects are interlinked: insect behavioral phenotypes affect their gut microbiota composition, partly through exposure to different environments and diet, and in return, the gut microbiota has been shown to influence insect behavior. Here, we discuss the bidirectional relationship existing between intraspecific variation in gut microbiota composition and behavioral phenotypes in social insects.