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The mushroom bodies, substructures of the Drosophila brain, are involved in olfactory learning and short-term memory, but their role in long-term memory is unknown. Here we show that the alpha-lobes-absent (ala) mutant lacks either the two vertical lobes of the mushroom body or two of the three median lobes which contain branches of vertical lobe neurons. This unique phenotype allows analysis of mushroom body function. Long-term memory required the presence of the vertical lobes but not the median lobes. Short-term memory was normal in flies without either vertical lobes or the two median lobes studied.
The organization of the Drosophila brain, which shows highly organized and specialized structures despite its small size, in combination with its sophisticated behavioral repertoires and powerful molecular genetic tools render this organism a model of choice for the study of integrative brain functions, such as associative learning and memory. The mushroom bodies (MBs) constitute a prominent bilateral structure of the insect brain. The MBs are formed and rearranged sequentially during embryonic and postembryonic development (1-3). In adult Drosophila, they are composed of about 5000 neurons, which receive, through the calyx, olfactory inputs from the antennal lobes. The MBs are essential for associative learning and memory (4-- 6). Several proteins involved in learning and short-term memory are detected at high levels in the MBs (7), and chemical ablation of Drosophila MBs abolishes olfactory learning (6). Synaptic transmission from the MBs is required for retrieval of short-term memories but not for acquisition or storage (8, 9). With intensive and spaced training, Drosophila can also display long-term memory (LTM), which depends on protein synthesis after the conditioning paradigm (10). We have now tested whether Drosophila MBs are involved in LTM formation.
Three categories of MB intrinsic neurons (Kenyon cells), associated with five sets of lobes, have been described (Fig. 1A) (1, 11). Two types of neurons branch to give rise to a vertical and a median lobe (alpha/beta lobes and alpha'/beta'' lobes, respectively). The third type composes the median gamma lobe. Uniquely identifiable efferent neurons originate from specific parts of the medial and vertical lobes, and send their axons to characteristic regions of the forebrain (12). Afferents from the forebrain also invade specific parts of the lobes (12). The implication of this...