Growth and pruning of mushroom body Kenyon cell dendrites during worker behavioral development in the paper wasp, Polybia aequatorialis (Hymenoptera: Vespidae)

The mushroom bodies in the protocerebrum are believed to be the structures of the insect brain most closely associated with higher-order sensory integration and learning. Drosophila melanogaster mutants with olfactory learning deficits have anatomically abnormal mushroom bodies or altered patterns of gene expression in mushroom body neurons. In addition, anatomical reorganization of the mushroom bodies occurs in adult flies, and possibly in adult honeybees; disturbance of electrical activity in this region disrupts memory formation in honeybees. Little is known, however, about the relationship of naturally occurring anatomical changes in the mushroom bodies to naturally occurring behavioural plasticity. We now report that age-based division of labour in adult worker honeybees (Apis mellifera) is associated with substantial changes in certain brain regions, notably the mushroom bodies. Moreover, these striking changes in brain structure are dependent, not on the age of the bee, but on its foraging experience, thus demonstrating a robust anatomical plasticity associated with complex behaviour in an adult insect.

To determine general or species-specific properties in neural systems, it is necessary to use comparative data in evaluating experimental findings. Presented here are data on associative learning and memory formation in honeybees, emphasizing a comparative approach. We focus on four aspects: (1) the role of an identified neuron, VUM(mx1), as a neural substrate of appetitive reinforcement; (2) the sequences of molecular events as they correlate with five forms of memory stages; (3) the localization of the memory traces following appetitive olfactory learning; and (4) the brief description of several forms of complex learning in bees (configuration in olfactory conditioning, categorization in visual feature learning, delayed matching-to-sample learning, and latent learning in navigation). VUM(mx1) activity following the conditioned stimulus odor is sufficient to replace the unconditioned stimulus, and VUM(mx1) changes its response properties during learning similarly to what is known from dopamine neurons in the basal ganglia of the mammalian brain. The transition from short- to mid- and long-term forms of memory can be related to specific activation of second messenger cascades (involving NOS, PKA, PKC, and PKM) resembling general features of neural plasticity at the cellular level. The particular time course of the various memory traces may be adapted to the behavioral context in which they are used; here, the foraging cycle of the bee. Memory traces for even such a simple form of learning as olfactory conditioning are multiple and distributed, involving first- and second-order sensory neuropils (antennal lobe and mushroom bodies), but with distinctly different properties. The wealth of complex forms of learning in the context of foraging indicates basic cognitive capacities based on rule extraction and context-dependent learning. It is believed that bees might be a useful model for studying cognitive faculties at a middle level of complexity.