F‐actin at identified synapses in the mushroom body neuropil of the insect brain

Frambach, Ina; Rößler, Wolfgang; Winkler, Margret; Schürmann, Friedrich‐Wilhelm

doi:10.1002/cne.20165

Cited by 82 publications

(88 citation statements)

References 56 publications

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“…Another possibility is that fascin regulation of the actin cytoskeleton in vivo controls the stability-lability balance at plastic synapses. F-actin localization at mushroom body postsynaptic sites (Frambach et al, 2004) and its dendritic-spine-specific modulation by activity at hippocampal synapses (Ouyang et al, 2005) are consistent with a role for fascin in synaptic plasticity. If true, then one might need high-resolution, real-time brain imaging to reveal dynamic defects in singed mutations.…”

Section: Unsuspected Neuronal Phenotypes Revealed In Vitrosupporting

confidence: 55%

Phenotypes ofDrosophilaBrain Neurons in Primary Culture Reveal a Role for Fascin in Neurite Shape and Trajectory

Kraft¹,

Escobar²,

Narro³

et al. 2006

J. Neurosci.

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Subtle cellular phenotypes in the CNS may evade detection by routine histopathology. Here, we demonstrate the value of primary culture for revealing genetically determined neuronal phenotypes at high resolution. Gamma neurons of Drosophila melanogaster mushroom bodies (MBs) are remodeled during metamorphosis under the control of the steroid hormone 20-hydroxyecdysone (20E). In vitro, wild-type ␥ neurons retain characteristic morphogenetic features, notably a single axon-like dominant primary process and an arbor of short dendrite-like processes, as determined with microtubule-polarity markers. We found three distinct genetically determined phenotypes of cultured neurons from grossly normal brains, suggesting that subtle in vivo attributes are unmasked and amplified in vitro. First, the neurite outgrowth response to 20E is sexually dimorphic, being much greater in female than in male ␥ neurons. Second, the ␥ neuron-specific "naked runt" phenotype results from transgenic insertion of an MB-specific promoter. Third, the recessive, panneuronal "filagree" phenotype maps to singed, which encodes the actin-bundling protein fascin. Fascin deficiency does not impair the 20E response, but neurites fail to maintain their normal, nearly straight trajectory, instead forming curls and hooks. This is accompanied by abnormally distributed filamentous actin. This is the first demonstration of fascin function in neuronal morphogenesis. Our findings, along with the regulation of human Fascin1 (OMIM 602689) by CREB (cAMP response element-binding protein) binding protein, suggest FSCN1 as a candidate gene for developmental brain disorders. We developed an automated method of computing neurite curvature and classifying neurons based on curvature phenotype. This will facilitate detection of genetic and pharmacological modifiers of neuronal defects resulting from fascin deficiency.

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Section: Unsuspected Neuronal Phenotypes Revealed In Vitrosupporting

confidence: 55%

Phenotypes ofDrosophilaBrain Neurons in Primary Culture Reveal a Role for Fascin in Neurite Shape and Trajectory

Kraft¹,

Escobar²,

Narro³

et al. 2006

J. Neurosci.

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“…Second, the adult MBs express ageand experience-dependent volume changes (38)(39)(40), indicating that structural changes in the MBs are related to behavioral plasticity. Third, MG in the MB calyx represent distinct synaptic units (30,31), which we were able to visualize and quantify at excellent resolution (21,27).…”

Section: Discussionmentioning

confidence: 94%

“…1 C-E and M). These microglomeruli (MG) represent distinct synaptic complexes in the calyx neuropil, each comprising a central bouton from PN axons surrounded by many KC dendritic spines and processes from other extrinsic neurons (27,(29)(30)(31). Synapsin-IR, which is associated with synaptic vesicles, stained the central bouton of MG, whereas phalloidin labeled a ring-like surrounding region ( Fig.…”

Section: Temperature Dependence Of Emergence Rate and Duration Of Pupalmentioning

confidence: 99%

Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development

Groh

Tautz

Rößler

2004

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

223

240

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Recent studies have shown that the behavioral performance of adult honey bees is influenced by the temperature experienced during pupal development. Here we explore whether there are temperature-mediated effects on the brain. We raised pupae at different constant temperatures between 29 and 37°C and performed neuroanatomical analyses of the adult brains. Analyses focused on sensory-input regions in the mushroom bodies, brain areas associated with higher-order processing such as learning and memory. Distinct synaptic complexes [microglomeruli (MG)] within the mushroom body calyces were visualized by using fluorophoreconjugated phalloidin and an antibody to synapsin. The numbers of MG were different in bees that had been raised at different temperatures, and these differences persisted after the first week of adult life. In the olfactory-input region (lip), MG numbers were highest in bees raised at the temperature normally maintained in brood cells (34.5°C) and significantly decreased in bees raised at 1°C below and above this norm. Interestingly, in the neighboring visual-input region (collar), MG numbers were less affected by temperature. We conclude that thermoregulatory control of brood rearing can generate area-and modality-specific effects on synaptic neuropils in the adult brain. We propose that resulting differences in the synaptic circuitry may affect neuronal plasticity and may underlie temperature-mediated effects on multimodal communication and learning.I n honey bee colonies, brood temperature is controlled precisely within a temperature range of 33-36°C (1, 2). In the central brood area, fluctuations are as small as 35 Ϯ 0.5°C during the pupal period (3, 4). Exposure to strong deviations from normal brood temperatures is known to result in increased mortality and morphological deficits (1, 5). Environmentally induced temperature changes within the hive are compensated by individual honey bee workers via endothermic heat production or evaporation cooling (4, 6, 7). Thermoregulation during winter is achieved also by endothermic heat production, but with lower absolute temperatures and less precision compared with brood rearing in summer (8,9). A recent study demonstrated that the temperature experienced during pupal development influences the behavioral performance of adult bees (10). Worker bees that had been raised at lower temperatures (within the range of naturally occurring temperatures) performed less well in dance communication and olfactory learning than bees raised at higher temperatures.As in other holometabolous insects, postembryonic development in honey bees includes complete larval-adult metamorphosis. In the pupa, the larval nervous system becomes completely remodeled to accommodate the development of adultspecific sensory organs and motor systems, which are associated with the extraordinary changes in behavior. The hormonal and neuronal processes underlying this remarkable plasticity have been the subject of numerous studies, most of them performed on the sphinx moth (Manduca sexta) and...

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“…The MB lips are well suited for memory storage: they are in adequate position for detecting coincident input from olfactory (through the PNs) and reinforcement (through the VUMmx1 neuron; Hammer, 1993) pathways (Menzel, 2001), and may display reverberant activity through feedback loops (Grünewald, 1999;Krashes et al, 2007), in a manner similar to that of the hippocampus (Rolls and Kesner, 2006). Likewise, the presence of many postsynaptic f-actin-rich spines in the MBs (Frambach et al, 2004) provide a suitable substrate for structural synaptic plasticity like in the vertebrate hippocampus (Halpain, 2000;Bramham, 2008). Spines indeed respond with rapid structural reorganization to adapt to presynaptic input changes (Brunig et al, 2004;Lin et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

Long-Term Memory Leads to Synaptic Reorganization in the Mushroom Bodies: A Memory Trace in the Insect Brain?

Hourcade

Muenz²,

Sandoz³

et al. 2010

J. Neurosci.

170

169

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The insect mushroom bodies (MBs) are paired brain centers which, like the mammalian hippocampus, have a prominent function in learning and memory. Despite convergent evidence for their crucial role in the formation and storage of associative memories, little is known about the mechanisms underlying such storage. In mammals and other species, the consolidation of stable memories is accompanied by structural plasticity involving variations in synapse number and/or size. Here, we address the question of whether the formation of olfactory long-term memory (LTM) could be associated with changes in the synaptic architecture of the MB networks. For this, we took advantage of the modular architecture of the honeybee MB neuropil, where synaptic contacts between olfactory input and MB neurons are segregated into discrete units (microglomeruli) which can be easily visualized and counted. We show that the density in microglomeruli increases as a specific olfactory LTM is formed, while the volume of the neuropil remains constant. Such variation is reproducible and is clearly correlated with memory consolidation, as it requires gene transcription. Thus stable structural synaptic rearrangements, including the growth of new synapses, seem to be a common property of insect and mammalian brain networks involved in the storage of stable memory traces.

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F‐actin at identified synapses in the mushroom body neuropil of the insect brain

Cited by 82 publications

References 56 publications

Phenotypes ofDrosophilaBrain Neurons in Primary Culture Reveal a Role for Fascin in Neurite Shape and Trajectory

Phenotypes ofDrosophilaBrain Neurons in Primary Culture Reveal a Role for Fascin in Neurite Shape and Trajectory

Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development

Long-Term Memory Leads to Synaptic Reorganization in the Mushroom Bodies: A Memory Trace in the Insect Brain?

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