Philosophical Transactions of the Royal Society of London. B, Biological Sciences
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The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies

    The mushroom bodies of the bee are paired neuropils in the dorsal part of the brain. Each is composed of the arborizations of over 17 x 104 small interneurons of similar architecture called Kenyon cells. Golgi staining demonstrates that these neurons can be divided into five groups distinguished on the basis of their dendritic specializations and geometry. The mushroom body neuropils each consist of a pair of cup-shaped structures, the calyces, connected by two short fused stalks, the pedunculus, to two lobes, the α- and β-lobes. Each calyx is formed from three concentric neuropil zones, the basal ring, the collar and the lip. The calyces are organized in a polar fashion; within the calyces each of the five categories of Kenyon cell has a distribution limited to particular polar contours. The dendritic volumes of neighbouring Kenyon cells arborizing within each individual contour are greatly overlapped. Fibres from groups of neighbouring cells within a calycal contour are gathered into bundles that project into the pedunculus, each fibre dividing to enter both the the α- and β-lobes. The pedunculus and the lobes are conspicuously layered. Kenyon cells with neighbouring dendritic fields within the same calycal contour occupy a single layer in the pedunculus and lobes. Thus the two- polar organization of the calyces is transformed into a Cartesian map within the pedunculus, which continues into the α- and β-lobes. The calyx receives input fibres from both the antennal lobes and the optic neuropils. The branching patterns of these cells reflect the polar organization of the calyces as their terminals are restricted to one or more of the three gross compartments of the calycal neuropil. The course of these tracts and the morphologies of the fibres that they contain are described. Cells considered to represent outputs from the mushroom bodies arborize in the pedunculus and α- and β-lobes. Generally the arborizations of the output neurons reflect the layered organization of these neuropils. Fibres from the two lobes run to the anterior median and lateral protocerebral neuropil, and the anterior optic tubercle. Additionally there is an extensive network of feedback interneurons that inter- connect the α- and β-lobes with the ipsi- and contralateral calyces. Many individual neurons have branches in both the α- and β-lobes and in the pedunculus. The pathways and geometries of the fibres subserving the two lobes are described. The hypothesis of Vowles (1955) that the individual lobes represent a separation of sensory and motor output areas is shown to be incorrect. The anatomy of the bee’s mushroom bodies suggests that they process second-order antennal and fourth- and higher-order visual information. The feedback pathways are discussed as possible means of creating long-lasting after-effects which may be important in complex timing processes and possibly the formation of short-term memory.

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