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Ronald L Davis - One of the best experts on this subject based on the ideXlab platform.
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larval and pupal development of the Mushroom Bodies in the honey bee apis mellifera
The Journal of Comparative Neurology, 1999Co-Authors: Sarah M. Farris, Ronald L Davis, Gene E Robinson, Susan E. FahrbachAbstract:The Mushroom Bodies are paired neuropils in the insect brain that act as multimodal sensory integration centers and are involved in learning and memory. Our studies, by using 5-bromo-2-deoxyuridine incorporation and the Feulgen technique, show that immediately before pupation, the brain of the developing honey bee (Apis mellifera) contains approximately 2,000 neuroblasts devoted to the production of the Mushroom body intrinsic neurons (Kenyon cells). These neuroblasts are descended from four clusters of 45 or fewer neuroblasts each already present in the newly hatched larva. Subpopulations of Kenyon cells, distinct in cytoarchitecture, position, and immunohistochemical traits, are born at different, but overlapping, periods during the development of the Mushroom Bodies, with the final complement of these neurons in place by the mid-pupal stage. The Mushroom Bodies of the adult honey bee have a concentric arrangement of Kenyon cell types, with the outer layers born first and pushed to the periphery by later born neurons that remain nearer the center of proliferation. This concentricity is further reflected in morphologic and immunohistochemical traits of the adult neurons, and is demonstrated clearly by the pattern of expression of Drosophila myocyte enhancer factor 2 (DMEF2)-like immunoreactivity. This is the first comprehensive study of larval and pupal development of the honey bee Mushroom Bodies. Similarities to patterns of neurogenesis observed in the Mushroom Bodies of other insects and in the vertebrate cerebral cortex are discussed. J. Comp. Neurol. 414:97–113, 1999. © 1999 Wiley-Liss, Inc.
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Larval and pupal development of the Mushroom Bodies in the honey bee, Apis mellifera.
The Journal of comparative neurology, 1999Co-Authors: Sarah M. Farris, Ronald L Davis, Gene E Robinson, Susan E. FahrbachAbstract:The Mushroom Bodies are paired neuropils in the insect brain that act as multimodal sensory integration centers and are involved in learning and memory. Our studies, by using 5-bromo-2-deoxyuridine incorporation and the Feulgen technique, show that immediately before pupation, the brain of the developing honey bee (Apis mellifera) contains approximately 2,000 neuroblasts devoted to the production of the Mushroom body intrinsic neurons (Kenyon cells). These neuroblasts are descended from four clusters of 45 or fewer neuroblasts each already present in the newly hatched larva. Subpopulations of Kenyon cells, distinct in cytoarchitecture, position, and immunohistochemical traits, are born at different, but overlapping, periods during the development of the Mushroom Bodies, with the final complement of these neurons in place by the mid-pupal stage. The Mushroom Bodies of the adult honey bee have a concentric arrangement of Kenyon cell types, with the outer layers born first and pushed to the periphery by later born neurons that remain nearer the center of proliferation. This concentricity is further reflected in morphologic and immunohistochemical traits of the adult neurons, and is demonstrated clearly by the pattern of expression of Drosophila myocyte enhancer factor 2 (DMEF2)-like immunoreactivity. This is the first comprehensive study of larval and pupal development of the honey bee Mushroom Bodies. Similarities to patterns of neurogenesis observed in the Mushroom Bodies of other insects and in the vertebrate cerebral cortex are discussed.
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a novel octopamine receptor with preferential expression in drosophila Mushroom Bodies
The Journal of Neuroscience, 1998Co-Authors: Kyung An Han, Neil S Millar, Ronald L DavisAbstract:Octopamine is a neuromodulator that mediates diverse physiological processes in invertebrates. In some insects, such as honeybees and fruit flies, octopamine has been shown to be a major stimulator of adenylyl cyclase and to function in associative learning. To identify an octopamine receptor mediating this function in Drosophila, putative biogenic amine receptors were cloned by a novel procedure using PCR and single-strand conformation polymorphism. One new receptor, octopamine receptor in Mushroom Bodies (OAMB), was identified as an octopamine receptor because human and Drosophila cell lines expressing OAMB showed increased cAMP and intracellular Ca2+ levels after octopamine application. Immunohistochemical analysis using an antibody made to the receptor revealed highly enriched expression in the Mushroom body neuropil and the ellipsoid body of central complex, brain areas known to be crucial for olfactory learning and motor control, respectively. The preferential expression of OAMB in Mushroom Bodies and its capacity to produce cAMP accumulation suggest an important role in synaptic modulation underlying behavioral plasticity.
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damb a novel dopamine receptor expressed specifically in drosophila Mushroom Bodies
Neuron, 1996Co-Authors: Kyung An Han, Neil S Millar, Michael S Grotewiel, Ronald L DavisAbstract:The modulatory neurotransmitters that trigger biochemical cascades underlying olfactory learning in Drosophila Mushroom Bodies have remained unknown. To identify molecules that may perform this role, putative biogenic amine receptors were cloned using the polymerase chain reaction (PCR) and single-strand conformation polymorphism analysis. One new receptor, DAMB, was identified as a dopamine D1 receptor by sequence analysis and pharmacological characterization. In situ hybridization and immunohistochemical analyses revealed highly enriched expression of DAMB in Mushroom Bodies, in a pattern coincident with the rutabaga-encoded adenylyl cyclase. The spatial coexpression of DAMB and the cyclase, along with DAMB's capacity to mediate dopamine-induced increases in cAMP make this receptor an attractive candidate for initiating biochemical cascades underlying learning.
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Neuroanatomy: Mushrooming Mushroom Bodies
Current biology : CB, 1996Co-Authors: Ronald L Davis, Kyung An HanAbstract:A revolution is spreading in the study of Mushroom Bodies, structures within the insect brain that mediate learning and memory processes and pheromonal discrimination of the opposite sex.
Wulfila Gronenberg - One of the best experts on this subject based on the ideXlab platform.
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the central nervous system of whip spiders amblypygi large Mushroom Bodies receive olfactory and visual input
The Journal of Comparative Neurology, 2020Co-Authors: Irina Sinakevitch, Skye M Long, Wulfila GronenbergAbstract:Whip spiders (Amblypygi) are known for their nocturnal navigational abilities, which rely on chemosensory and tactile cues and, to a lesser degree, on vision. Unlike true spiders, the first pair of legs in whip spiders is modified into extraordinarily long sensory organs (antenniform legs) covered with thousands of mechanosensory, olfactory, and gustatory sensilla. Olfactory neurons send their axons through the leg nerve into the corresponding neuromere of the central nervous system, where they terminate on a particularly large number (about 460) of primary olfactory glomeruli, suggesting an advanced sense of smell. From the primary glomeruli, olfactory projection neurons ascend to the brain and terminate in the Mushroom body calyx on a set of secondary olfactory glomeruli, a feature that is not known from olfactory pathways of other animals. Another part of the calyx receives visual input from the secondary visual neuropil (the medulla). This calyx region is composed of much smaller glomeruli ("microglomeruli"). The bimodal input and the exceptional size of their Mushroom Bodies may support the navigational capabilities of whip spiders. In addition to input to the Mushroom body, we describe other general anatomical features of the whip spiders' central nervous system.
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Higher order visual input to the Mushroom Bodies in the bee, Bombus impatiens.
Arthropod structure & development, 2008Co-Authors: Angelique C. Paulk, Wulfila GronenbergAbstract:To produce appropriate behaviors based on biologically relevant associations, sensory pathways conveying different modalities are integrated by higher-order central brain structures, such as insect Mushroom Bodies. To address this function of sensory integration, we characterized the structure and response of optic lobe (OL) neurons projecting to the calyces of the Mushroom Bodies in bees. Bees are well known for their visual learning and memory capabilities and their brains possess major direct visual input from the optic lobes to the Mushroom Bodies. To functionally characterize these visual inputs to the Mushroom Bodies, we recorded intracellularly from neurons in bumblebees (Apidae: Bombus impatiens) and a single neuron in a honeybee (Apidae: Apis mellifera) while presenting color and motion stimuli. All of the Mushroom body input neurons were color sensitive while a subset was motion sensitive. Additionally, most of the Mushroom body input neurons would respond to the first, but not to subsequent, presentations of repeated stimuli. In general, the medulla or lobula neurons projecting to the calyx signaled specific chromatic, temporal, and motion features of the visual world to the Mushroom Bodies, which included sensory information required for the biologically relevant associations bees form during foraging tasks.
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Segregation of visual input to the Mushroom Bodies in the honeybee (Apis mellifera).
The Journal of comparative neurology, 2002Co-Authors: Birgit Ehmer, Wulfila GronenbergAbstract:Insect Mushroom Bodies are brain regions that receive multisensory input and are thought to play an important role in learning and memory. In most neopteran insects, the Mushroom Bodies receive direct olfactory input. In addition, the calyces of Hymenoptera receive substantial direct input from the optic lobes. We describe visual inputs to the calyces of the Mushroom Bodies of the honeybee Apis mellifera, the neurons' dendritic fields in the optic lobes, the medulla and lobula, and the organization of their terminals in the calyces. Medulla neurons terminate in the collar region of the calyx, where they segregate into five layers that receive alternating input from the dorsal or ventral medulla, respectively. A sixth, innermost layer of the collar receives input from lobula neurons. In the basal ring region of the calyx, medulla neuron terminals are restricted to a small, distal part. Lobula neurons are more prominent in the basal ring, where they terminate in its outer half. Although the collar and basal ring layers generally receive segregated input from both optic neuropils, some overlap occurs at the borders of the layers. At least three different types of Mushroom body input neurons originate from the medulla: (a) neurons with narrow dendritic fields mainly restricted to the vicinity of the medulla's serpentine layer and found throughout the medulla; (b) neurons restricted to the ventral half of the medulla and featuring long columnar dendritic branches in the outer medulla; and (c) a group of neurons whose dendrites are restricted to the most ventral part of the medulla and whose axons form the anterior inferior optic tract. Most medulla neurons (groups a and b) send their axons via the anterior superior optic tract to the Mushroom Bodies. Neurons connecting the lobula with the Mushroom Bodies have their dendrites in a defined dorsal part of the lobula. Their axons form a third tract to the Mushroom Bodies, here referred to as the lobula tract. Our findings match the anatomy of intrinsic Mushroom body neurons (Strausfeld, 2002) and together indicate that the Mushroom Bodies may be composed of many more functional subsystems than previously suggested.
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Modality-specific segregation of input to ant Mushroom Bodies.
Brain behavior and evolution, 1999Co-Authors: Wulfila GronenbergAbstract:The Mushroom Bodies are central brain neuropils involved in the control of complex behavior. In ants, the Mushroom Bodies are relatively large compared to those of honey bees, whereas the optic lobes of ants are considerably smaller. The general morphology of ant Mushroom Bodies is similar to that of honey bees. As in other Hymenoptera, the main input region of the Mushroom Bodies, the calyx, is subdivided into three compartments: the lip, the collar, and the basal ring. In many ant species this compartmentalization is not obvious and can only be visualized using neuronal tracers. The lip region receives antennal input and is large in all ant species. It appears to be composed of at least two different regions that have not yet been characterized in detail. The collar is large in other Hymenoptera, yet in ant workers it varies in size and is always much smaller than the lip region. The collar receives visual input and is relatively larger in males, which generally are more dependant on vision than are workers. The basal ring receives input from both the optic and antennal lobes. In one ant tribe, the Ponerini, the collar region appears to have changed its position, but based on afferent input it appears to be homologous to the hymenopteran collar. Generally, the composition of the Mushroom body calyx correlates with the living conditions of ants, reflecting the great importance of olfaction and the lesser and more variable significance of vision for workers of the observed ant species.
Aike Guo - One of the best experts on this subject based on the ideXlab platform.
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gap junction networks in Mushroom Bodies participate in visual learning and memory in drosophila
eLife, 2016Co-Authors: Qingqing Liu, Aike Guo, Xing Yang, Jingsong Tian, Zhongbao Gao, Meng WangAbstract:Gap junctions are widely distributed in the brains across species and play essential roles in neural information processing. However, the role of gap junctions in insect cognition remains poorly understood. Using a flight simulator paradigm and genetic tools, we found that gap junctions are present in Drosophila Kenyon cells (KCs), the major neurons of the Mushroom Bodies (MBs), and showed that they play an important role in visual learning and memory. Using a dye coupling approach, we determined the distribution of gap junctions in KCs. Furthermore, we identified a single pair of MB output neurons (MBONs) that possess a gap junction connection to KCs, and provide strong evidence that this connection is also required for visual learning and memory. Together, our results reveal gap junction networks in KCs and the KC-MBON circuit, and bring new insight into the synaptic network underlying fly's visual learning and memory.
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the gaba system regulates the sparse coding of odors in the Mushroom Bodies of drosophila
Biochemical and Biophysical Research Communications, 2013Co-Authors: Zhengchang Lei, Ke Chen, He Liu, Aike GuoAbstract:In the Mushroom Bodies (MBs) of Drosophila, an analogue of the mammalian olfactory cortex, olfactory stimuli are sparsely encoded by Kenyon cells (KCs) that exhibit a high level of odor selectivity. Sparse coding of olfactory stimuli has significant advantages for maximizing the discrimination power and storage capacity of MBs. The inhibitory gamma-aminobutyric acid (GABA) system is important for regulating information processing in MBs, but its specific role in the sparse coding of odors is unclear. In this study, we investigated the role of the GABA system in the sparse coding of odors using an in vivo calcium imaging strategy, which allowed us to measure the activity of the KC population at single cell resolution while the components of the GABA system were genetically manipulated. We found that the down-regulation of GABAA but not GABAB receptors in KCs reduced the sparseness of odor representations in the MB, as shown by an increase in the population response probability and decrease in the odor selectivity of single KCs. Furthermore, the down-regulation of GABA synthesis in a pair of large GABAergic neurons innervating the entire MB reduced the sparseness of odor representations in KCs. In conclusion, the sparse coding of odors in MBs is regulated by a pair of GABAergic neurons through the GABAA receptors on KCs, thus demonstrating a specific role of the inhibitory GABA system on information processing in the MB.
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go signaling in Mushroom Bodies regulates sleep in drosophila
Sleep, 2011Co-Authors: Fang Guo, Mingmin Zhou, Aike GuoAbstract:Study Objectives: Sleep is a fundamental physiological process and its biological mechanisms are poorly understood. In Drosophila melanogaster, heterotrimeric Go protein is abundantly expressed in the brain. However, its post-developmental function has not been extensively explored. Design: Locomotor activity was measured using the Drosophila Activity Monitoring System under a 12: 12 LD cycle. Sleep was defined as periods of 5 min with no recorded activity. Results: Pan-neuronal elevation of Go signaling induced quiescence accompanied by an increased arousal threshold in flies. By screening region-specific GAL4 lines, we mapped the sleep-regulatory function of Go signaling to Mushroom Bodies (MBs), a central brain region which modulates memory, decision making, and sleep in Drosophila. Up-regulation of Go activity in these neurons consolidated sleep while inhibition of endogenous Go via expression of Go RNAi or pertussis toxin reduced and fragmented sleep, indicating that the Drosophila sleep requirement is affected by levels of Go activity in the MBs. Genetic interaction results showed that Go signaling serves as a neuronal transmission inhibitor in a cAMP-independent pathway. Conclusion: Go signaling is a novel signaling pathway in MBs that regulates sleep in Drosophila.
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Mushroom Bodies modulate salience based selective fixation behavior in drosophila
European Journal of Neuroscience, 2008Co-Authors: Yueqing Peng, Jianzeng Guo, Ke Zhang, Aike GuoAbstract:Mushroom Bodies (MBs), one of the central brain structures in Drosophila melanogaster, are involved in several cognitive behaviors, such as olfactory learning and memory, visual context generalization, choice behavior facing conflicting cues. Attention is a cognitive behavior, and it facilitates a focus on the attended event while filtering out irrelevant events, thereby allowing more rapid and accurate reactions at a lower threshold in primates. Using the visual orientation paradigm in a flight simulator, we observed that MBs modulate salience-based selective fixation behavior, which resembles attention in primates to a certain degree. We found that the fixation ability of MB-deficient flies was significantly reduced when the contrast levels were lowered as well as when a certain amount of background noise was applied. Moreover, MB-deficient flies exhibited poor object fixation ability in the presence of an olfactory 'distracter'. Furthermore, during visual selection among multiple objects of different contrast, flies with MBs were able to 'pop-out' of the most salient object in a three-object selection paradigm. Finally, we determined that flies exhibited cross-modal synergistic integration between olfactory and visual signals during object-fixation behavior, which was independent of MBs. Taken together, our findings suggest that MBs do not contribute to cross-modal synergetic integration between olfactory and visual signals; instead, they confer sensory gain control and inhibitory gating in flies, this property allows entry of the salient signal as well as filters out background noise and irrelevant signals.
Kim Kaiser - One of the best experts on this subject based on the ideXlab platform.
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metamorphosis of the Mushroom Bodies large scale rearrangements of the neural substrates for associative learning and memory in drosophila
Learning & Memory, 1998Co-Authors: Douglas J Armstrong, Steven J De Belle, Zongsheng Wang, Kim KaiserAbstract:Paired brain centers known as Mushroom Bodies are key features of the circuitry for insect associative learning, especially when evoked by olfactory cues. Mushroom Bodies have an embryonic origin, and unlike most other brain structures they exhibit developmental continuity, being prominent components of both the larval and the adult CNS. Here, we use cell-type-specific markers, provided by the P{GAL4} enhancer trap system, to follow specific subsets of Mushroom body intrinsic and extrinsic neurons from the larval to the adult stage. We find marked structural differences between the larval and adult Mushroom Bodies, arising as the consequence of large-scale reorganization during metamorphosis. Extensive, though incomplete, degradation of the larval structure is followed by establishment of adult specific α and β lobes. Kenyon cells of embryonic origin, by contrast, were found to project selectively to the adult γ lobe. We propose that the γ lobe stores information of relevance to both developmental stages, whereas the α and β lobes have uniquely adult roles.
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Early development of the Drosophila Mushroom Bodies, brain centres for associative learning and memory.
Development genes and evolution, 1997Co-Authors: Marco Tettamanti, Mingyao Yang, J. Douglas Armstrong, Kim Kaiser, Keita Endo, Katsuo Furukubo-tokunaga, Heinrich ReichertAbstract:We have studied the formation of Drosophila Mushroom Bodies using enhancer detector techniques to visualize specific components of these complex intrinsic brain structures. During embryogenesis, neuronal proliferation begins in four Mushroom body neuroblasts and the major axonal pathways of the Mushroom Bodies are pioneered. During larval development, neuronal proliferation continues and further axonal projections in the pedunculus and lobes are formed in a highly structured manner characterized by spatial heterogeneity of reporter gene expression. Enhancer detector analysis identifies many genomic locations that are specifically activated in Mushroom body intrinsic neurons (Kenyon cells) during the transition from embryonic to postembryonic development and during metamorphosis.
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Subdivision of the drosophila Mushroom Bodies by enhancer-trap expression patterns
Neuron, 1995Co-Authors: Mingyao Yang, J. Douglas Armstrong, Ilya Vilinsky, Nicholas J. Strausfeld, Kim KaiserAbstract:Phylogenetically conserved brain centers known as Mushroom Bodies are implicated in insect associative learning and in several other aspects of insect behavior. Kenyon cells, the intrinsic neurons of Mushroom Bodies, have been generally considered to be disposed as homogenous arrays. Such a simple picture imposes constraints on interpreting the diverse behavioral and computational properties that Mushroom Bodies are supposed to perform. Using a P[GAL4] enhancer-trap approach, we have revealed axonal processes corresponding to intrinsic cells of the Drosophila Mushroom Bodies. Rather than being homogenous, we find the Drosophila Mushroom Bodies to be compound neuropils in which parallel subcomponents exhibit discrete patterns of gene expression. Different patterns correspond to hitherto unobserved differences in Kenyon cell trajectory and placement. On the basis of this unexpected complexity, we propose a model for Mushroom body function in which parallel channels of information flow, perhaps with different computational properties, subserve different behavioral roles.
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Functional dissection of the drosophila Mushroom Bodies by selective feminization ofagenetically defined subcompartments
Neuron, 1995Co-Authors: Kevin M.c. O'dell, Mingyao Yang, J. Douglas Armstrong, Kim KaiserAbstract:Relatively little is known about the neural circuitry underlying sex-specific behaviors. We have expressed the feminizing gene transformer in genetically defined subregions of the brain of male Drosophila, and in particular within different domains of the Mushroom Bodies. Mushroom Bodies are phylogenetically conserved insect brain centers implicated in associative learning and various other aspects of behavior. Expression of transformer in lines that mark certain subsets of Mushroom body intrinsic neurons, and in a line that marks a component of the antennal lobe, causes males to exhibit nondiscriminatory sexual behavior: they court mature males in addition to females. Expression of transformer in other Mushroom body domains, and in control lines, has no such effect. Our data support the view that genetically defined subsets of Mushroom body intrinsic neurons perform different functional roles.
Martin Heisenberg - One of the best experts on this subject based on the ideXlab platform.
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visual attention in flies dopamine in the Mushroom Bodies mediates the after effect of cueing
PLOS ONE, 2016Co-Authors: Sebastian Koenig, Reinhard Wolf, Martin HeisenbergAbstract:Visual environments may simultaneously comprise stimuli of different significance. Often such stimuli require incompatible responses. Selective visual attention allows an animal to respond exclusively to the stimuli at a certain location in the visual field. In the process of establishing its focus of attention the animal can be influenced by external cues. Here we characterize the behavioral properties and neural mechanism of cueing in the fly Drosophila melanogaster. A cue can be attractive, repulsive or ineffective depending upon (e.g.) its visual properties and location in the visual field. Dopamine signaling in the brain is required to maintain the effect of cueing once the cue has disappeared. Raising or lowering dopamine at the synapse abolishes this after-effect. Specifically, dopamine is necessary and sufficient in the αβ-lobes of the Mushroom Bodies. Evidence is provided for an involvement of the αβposterior Kenyon cells.
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context generalization in drosophila visual learning requires the Mushroom Bodies
Nature, 1999Co-Authors: Li Liu, R Ernst, Reinhard Wolf, Martin HeisenbergAbstract:The world is permanently changing. Laboratory experiments on learning and memory normally minimize this feature of reality, keeping all conditions except the conditioned and unconditioned stimuli as constant as possible1. In the real world, however, animals need to extract from the universe of sensory signals the actual predictors of salient events by separating them from non-predictive stimuli (context2). In principle, this can be achieved ifonly those sensory inputs that resemble the reinforcer in theirtemporal structure are taken as predictors. Here we study visual learning in the fly Drosophila melanogaster, using a flight simulator3,4, and show that memory retrieval is, indeed, partially context-independent. Moreover, we show that the Mushroom Bodies, which are required for olfactory5,6,7 but not visual or tactile learning8, effectively support context generalization. In visual learning in Drosophila, it appears that a facilitating effect of context cues for memory retrieval is the default state, whereas making recall context-independent requires additional processing.
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drosophila Mushroom Bodies are dispensable for visual tactile and motor learning
Learning & Memory, 1998Co-Authors: Reinhard Wolf, T Wittig, G Wustmann, D Eyding, Li Liu, Martin HeisenbergAbstract:Possible roles of the insect Mushroom Bodies (corpora pedunculata) in behavior have been debated for nearly 150 years (Dujardin 1850). It took more than a century before some of the hypotheses could be tested experimentally and even then, the means of intervention proved unsatisfactory. Lesions and electrical stimulation in the Mushroom Bodies (MBs) caused a large variety of behavioral symptoms that were difficult to reconcile with a common function (for review, see Erber et al. 1987). Among the behavioral properties affected by lesions were cocoon spinning in Cecropia larvae (van der Kloot and Williams 1954), the organization of behavioral sequences in bees and locusts (Howse 1974), odor thresholds and optomotor latencies in the cockroach (Drescher 1960), as well as the suppression of locomotor activity in crickets and grasshoppers (Huber 1960). Fortunately, one behavioral impairment has now been consistently found with different lesioning techniques and in different insect species: olfactory learning and memory. First hints indicating that the MBs are required for the retention of odors came from extensive bilateral lesions in bees (Voskresenskaja 1957) and ants (Vowles 1964). Later, Masuhr (1976) applied more confined lesions in the calyces or α-lobes of the honeybee with similar results. Subsequently, he developed a special probe for locally cooling small areas of the bee brain. With this elegant technique he was able to interfere with short-term memory in the antennal lobe, calyces, or α-lobe (Erber et al. 1980). A decade later, two Drosophila mutants with severe structural defects in the MBs, but entirely different etiologies of the mutant defects, were shown to be impaired in olfactory memory (Heisenberg et al. 1985). A further decade later, it became possible to ablate the MBs in wild-type Drosophila by applying a cytostatic drug, hydroxyurea (HU), to the first larval instar (Prokop and Technau 1994). The result was the same—a severe defect in olfactory memory (de Belle and Heisenberg 1994). Recently, Connolly et al. (1996) went a step farther and confined the block to the Kenyon cells by specifically expressing a constitutively activated Gαs protein subunit in these cells. Again, odor retention was specifically impaired. If the expression of the mutated transgene leaves the circuitry of the MB pathway intact, the experiment shows that blocking modulation of the Kenyon cell output synapses is sufficient to impair olfactory memory. The cumulative evidence from hymenopterans and flies leaves little doubt that MBs are involved in olfactory memory. This finding calls to mind the proposal of Hanstrom (1928), suggesting that the MBs may be general association organs. The MBs do receive many types of sensory input (for review, see Erber et al. 1987; Schurmann 1987), and in Drosophila the MBs have been shown recently to be structurally affected by visual experience (Barth and Heisenberg 1997). However, outside the realm of chemoreception little evidence supports Hanstrom’s view. Flies of the Mushroom Bodies deranged (mbd) mutant stock with severely defective MBs have been shown to remember colors (Heisenberg et al. 1985; Heisenberg 1989). Moreover, mutant mbd as well as Mushroom body miniature1 (mbm1) flies are able to reorganize their visuomotor interface in response to inverted coupling in the flight simulator (preliminary data cited in Heisenberg 1989). Here we reinvestigate the question whether the MBs might be involved in visual and other kinds of associative learning and memory besides odor preference conditioning. We take advantage of the HU ablation technique (Prokop and Technau 1994) for the generation of MB-less flies (HU-flies). The HU technique seems particularly suited for studying the role of the MBs in visual behavior because the optic anlagen do not start postembryonic development until after HU treatment (Ito and Hotta 1991). The volume of the adult optic lobes is not affected in HU flies (deBelle and Heisenberg 1994). In the time window of the treatment, in each brain hemisphere only five neuroblasts proliferate. Four of them, the MB neuroblasts, give birth to the postembryonic Kenyon cells, and a fifth one generates neurons of the antennal lobe (Ito and Hotta 1991; Prokop and Technau 1994). In the adult animal, HU treatment leads to the virtually complete absence of MBs and, in addition, to a 30% reduction of the volume of the antennal lobe (de Belle and Heisenberg 1994). In this study we test MB-less flies in six learning paradigms, four of which involve visual orientation. Five are operant and one is a classic form of conditioning. In four paradigms, the animals are tethered in flight; in two paradigms, freely walking flies are tested. Different kinds of reinforcements and various conditioned stimuli are used. In all these situations MB-less flies perform as well as normal ones. The involvement of the MBs in learning and memory seems to be confined to olfaction and possibly taste.
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associative odor learning in drosophila abolished by chemical ablation of Mushroom Bodies
Science, 1994Co-Authors: J S De Belle, Martin HeisenbergAbstract:The corpora pedunculata, or Mushroom Bodies (MBs), in the brain of Drosophila melanogaster adults consist of approximately 2500 parallel Kenyon cell fibers derived from four MB neuroblasts. Hydroxyurea fed to newly hatched larvae selectively deletes these cells, resulting in complete, precise MB albation. Adult flies developing without MBs behave normally in most respects, but are unable to perform in a classical conditioning paradigm that tests associative learning of odor cues and electric shock. This deficit cannot be attributed to reductions in olfactory sensitivity, shock reactivity, or locomotor behavior. The results demonstrate that MBs mediate associative odor learning in flies.
