Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes

Abstract

Studies of the mushroom bodies of Drosophila melanogaster have suggested that their gamma lobes specifically support short-term memory, whereas their vertical lobes are essential for long-term memory. Developmental studies have demonstrated that the Drosophila gamma lobe, like its equivalent in the cockroach Periplaneta americana, is supplied by a special class of intrinsic neuron-the clawed Kenyon cells-that are the first to differentiate during early development. To date, however, no account identifies a corresponding lobe in the honey bee, another taxon used extensively for learning and memory research. Received opinion is that, in this taxon, each of the mushroom body lobes comprises three parallel divisions representing one of three concentric zones of the calyces, called the lip, collar, and basal ring. The present account shows that, although these zones are represented in the lobes, they occupy only two thirds of the vertical lobe. Its lowermost third receives the axons of the clawed class II Kenyon cells, which are the first to differentiate during early development and which represent the whole calyx. This component of the lobe is anatomically and developmentally equivalent to the gamma lobe of Drosophila and has been here named the gamma lobe of the honey bee. A new class of intrinsic neurons, originating from perikarya distant from the mushroom body, provides a second system of parallel fibers from the calyx to the gamma lobe. A region immediately beneath the calyces, called the neck, is invaded by these neurons as well as by a third class of intrinsic cell that provides connections within the neck of the pedunculus and the basal ring of the calyces. In the honey bee, the gamma lobe is extensively supplied by afferents from the protocerebrum and gives rise to a distinctive class of efferent neurons. The terminals of these efferents target protocerebral neuropils that are distinct from those receiving efferents from divisions of the vertical lobe that represent the lip, collar, and basal ring. The identification of a gamma lobe unites the mushroom bodies of evolutionarily divergent taxa. The present findings suggest the need for critical reinterpretation of studies that have been predicated on early descriptions of the mushroom body's lobes.