Honeybee Brain Oscillations Are Generated by Microtubules. The Concept of a Brain Central Oscillator

Microtubules (MTs) are important structures of the cytoskeleton in neurons. Mammalian brain MTs act as biomolecular transistors that generate highly synchronous electrical oscillations. However, their role in brain function is largely unknown. To gain insight into the MT electrical oscillatory activity of the brain, we turned to the honeybee (Apis mellifera) as a useful model to isolate brains and MTs. The patch clamp technique was applied to MT sheets of purified honeybee brain MTs. High resistance seal patches showed electrical oscillations that linearly depended on the holding potential between ± 200 mV and had an average conductance in the order of ~9 nS. To place these oscillations in the context of the brain, we also explored local field potential (LFP) recordings from the Triton X-permeabilized whole honeybee brain unmasking spontaneous oscillations after but not before tissue permeabilization. Frequency domain spectral analysis of time records indicated at least two major peaks at approximately ~38 Hz and ~93 Hz in both preparations. The present data provide evidence that MT electrical oscillations are a novel signaling mechanism implicated in brain wave activity observed in the insect brain.

Queen pheromone modulates the expression of epigenetic modifier genes in the brain of honeybee workers

Pheromones are used by many insects to mediate social interactions. In the highly eusocial honeybee ( Apis mellifera ), queen mandibular pheromone (QMP) is involved in the regulation of the reproductive and other behaviour of workers. The molecular mechanisms by which QMP acts are largely unknown. Here, we investigate how genes responsible for epigenetic modifications to DNA, RNA and histones respond to the presence of QMP in the environment. We show that several of these genes are upregulated in the honeybee brain when workers are exposed to artificial QMP. We propose that pheromonal communication systems, such as those used by social insects, evolved to respond to environmental signals by making use of existing epigenomic machineries.

Queen pheromone modulates the expression of epigenetic modifier genes in the brain of honeybee workers

Pheromones are used by many insects to mediate social interactions. In the highly eusocial honeybee (Apis mellifera) queen mandibular pheromone (QMP) is involved in the regulation of reproduction and behaviour of workers. The molecular mechanisms by which QMP acts are largely unknown. Here we investigate how genes responsible for epigenetic modifications to DNA, RNA and histones respond to the presence of QMP. We show that several of these genes are upregulated in the honeybee brain when workers are exposed to QMP. This provides a plausible mechanism by which pheromone signalling may influence gene expression in the brain of honeybee workers. We propose that pheromonal communication systems, such as those used by social insects, evolved to respond to environmental signals by making use of existing epigenomic machineries.

The Neurophysiological Bases of the Impact of Neonicotinoid Pesticides on the Behaviour of Honeybees

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.

Valence of social information is encoded in different subpopulations of mushroom body Kenyon cells in the honeybee brain

Over 600 Myr of evolutionary divergence between vertebrates and invertebrates is associated with considerable neuroanatomical variation both across and within these lineages. By contrast, valence encoding is an important behavioural trait that is evolutionarily conserved across vertebrates and invertebrates, and enables individuals to distinguish between positive (potentially beneficial) and negative (potentially harmful) situations. We tested the hypothesis that social interactions of positive and negative valence are modularly encoded in the honeybee brain (i.e. encoded in different cellular subpopulations) as in vertebrate brains. In vertebrates, neural activation patterns are distributed across distinct parts of the brain, suggesting that discrete circuits encode positive or negative stimuli. Evidence for this hypothesis would suggest a deep homology of neural organization between insects and vertebrates for valence encoding, despite vastly different brain sizes. Alternatively, overlapping localization of valenced social information in the brain would imply a ‘re-use' of circuitry in response to positive and negative social contexts, potentially to overcome the energetic constraints of a tiny brain. We used immediate early gene expression to map positively and negatively valenced social interactions in the brain of the western honeybee Apis mellifera . We found that the valence of a social signal is represented by distinct anatomical subregions of the mushroom bodies, an invertebrate sensory neuropil associated with social behaviour, multimodal sensory integration, learning and memory. Our results suggest that the modularization of valenced social information in the brain is a fundamental property of neuroanatomical organization.

Evidence for absence of bilateral transfer of olfactory learned information in Apis dorsata and Apis mellifera

Capacity and condition under which lateral transfer of olfactory memory is possible in insects are still debated. Here we present evidence consistent with lack of ability to transfer olfactory associative memory in two species of honeybees, Apis mellifera and Apis dorsata in a PER associative conditioning paradigm where the untrained antenna is blocked by an insulating coat. We show that the olfactory system on each side of the bee can learn and retrieve independently and the retrieval using the antenna on the side contralateral to the trained one is not affected by the training. Recreating the paradigm in which the memory on the contralateral side has been reported at three hours after training we see that the memory is available on the contralateral side immediately after training and moreover, training with trained side antenna coated with insulator does not prevent learning, pointing to a possible insufficiency of block of odor stimuli in this paradigm. Bee does not learn the odor stimuli applied to one side alone as a stimulus different from odor presented to both sides. Moreover the behaviour of the bee as a whole can be predicted if the sides are assumed to learn and store independently and the organism as a whole is able to retrieve the memory if either of the sides have learned.Summary StatementThe two halves of honeybee brain store and retrieve olfactory associative memories independently.