GABA‐immunoreactive neurons in the mushroom bodies of the honeybee: An electron microscopic study

Ganeshina, Olga; Menzel, Randolf

doi:10.1002/cne.1287

Cited by 170 publications

(187 citation statements)

References 55 publications

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“…In honey bees, these neurons have been proposed to function as an inhibitory feedback loop (Grünewald, 1999b;Ganeshina and Menzel, 2001). Such differences between hemi-and holometabolous insects regarding the dendritic placement of GABAimmunoreactive neurons suggest that there may have been an evolutionary change from the basal (hemimetabolous) condition, where dendrites of GABA-immunoreactive neurons supplying the calyces were originally located in protocerebral areas outside the pedunculus and lobes.…”

Section: Discussionmentioning

confidence: 99%

Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis

Sinakevitch¹,

Sjöholm

Hansson

et al. 2008

Arthropod Structure & Development

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The moth Spodoptera littoralis, is a major pest of agriculture whose olfactory system is tuned to odorants emitted by host plants and conspecifics. As in other insects, the paired mushroom bodies are thought to play pivotal roles in behaviors that are elicited by contextual and multisensory signals, amongst which those of specific odors dominate. Compared with species that have elaborate behavioral repertoires, such as the honey bee Apis mellifera or the cockroach Periplaneta americana, the mushroom bodies of S. littoralis were originally viewed as having a simple cellular organization. This has been since challenged by observations of putative transmitters and neuromodulators. As revealed by immunocytology, the spodopteran mushroom bodies like those of other taxa, are subdivided longitudinally into discrete neuropil domains. Such divisions are further supported by the present study, which also demonstrates discrete affinities to different mushroom body neuropils by antibodies raised against two putative transmitters, glutamate and γ-aminobutyric acid, and against three putative neuromodulatory substances: serotonin, A-type allatostatin, and tachykinin-related peptides. The results suggest that in addition to longitudinal divisions of the lobes, circuits in the calyces and lobes are likely to be independently modulated.

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Section: Discussionmentioning

confidence: 99%

Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis

Sinakevitch¹,

Sjöholm

Hansson

et al. 2008

Arthropod Structure & Development

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“…Previous reports showed that synaptic complexes in MB calyces both from Drosophila and in honeybees, present a typical ring-like shape (34)(35)(36)(37). To test whether DenMark is indeed present at these ring-like synaptic structures, we labeled the presynaptic terminals by revealing ChAT (Choline Acetyl Transferase) immunoreactivity.…”

Section: J)mentioning

confidence: 99%

Genetically encoded dendritic marker sheds light on neuronal connectivity inDrosophila

Nicolaï

Ramaekers

Raemaekers

et al. 2010

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

259

227

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In recent years, Drosophila melanogaster has emerged as a powerful model for neuronal circuit development, pathology, and function. A major impediment to these studies has been the lack of a genetically encoded, specific, universal, and phenotypically neutral marker of the somatodendritic compartment. We have developed such a marker and show that it is effective and specific in all neuronal populations tested in the peripheral and central nervous system. The marker, which we name DenMark (Dendritic Marker), is a hybrid protein of the mouse protein ICAM5/Telencephalin and the red fluorescent protein mCherry. We show that DenMark is a powerful tool for revealing novel aspects of the neuroanatomy of developing dendrites, identifying previously unknown dendritic arbors, and elucidating neuronal connectivity.T o discover neuronal circuit architecture, genetic tools that specifically mark the pre-and postsynaptic cells and compartments are necessary. Drosophila is a leading genetic model organism in this regard; however, most neuronal circuits remain unmapped. Of particular note is the lack of a universal, phenotypically neutral, and specific marker of the somatodendritic and postsynaptic compartments. Several molecular differences between dendrites and axons, including the presence of different membrane and cytoskeletal proteins in neuronal subregions, have been identified (1, 2). Drosophila neurons exhibit the major kinds of compartmentalization present in mammalian neurons and the fly has emerged as a powerful system to study the establishment and maintenance of neuronal connections (3, 4). Almost all studies of neuronal circuits in the fly have relied on genetic markers such as CD8::GFP that outline the morphology of entire cells rather than particular subcellular compartments (5), as well as presynaptic markers such as Synaptotagmin, Synaptobrevin, and Bruchpilot GFP fusion proteins (6-11). However, more accurate identification and mapping of novel neuronal circuits has been hampered by the lack of a genetically encoded and phenotypically neutral dendritic marker. Over the years, many such markers have been proposed and several were recently examined (12), namely MAP2 (13, 14), Nod::YFP (4, 15-18), Homer::GFP (19), and DSCAM17.1::GFP (20, 21). The analysis of these markers reveals that none of them labels the entire somatodendritic field. Furthermore, it remains unclear whether the markers tested are neutral with respect to dendritic morphology.Intercellular adhesion molecules (ICAMs) mediate neuronal migration, axon elongation, and fasciculation, synaptogenesis, and synaptic plasticity (22). ICAM5, or Telencephalin, is a 130-kDa type I transmembrane glycoprotein comprising a characteristic extracellular domain, a single transmembrane region, and a short cytoplasmic region (23). The expression of ICAM5 is restricted to the mammalian brain telencephalon (24) but there is no homolog in invertebrates and lower vertebrates. The developmental appearance of ICAM5 parallels the time of dendritic elongation, branching, a...

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“…Others had no obvious morphological defects. From these groups (29,30,31, and 37°C), only those bees with no apparent morphological defects were used for neuroanatomical analyses.…”

Section: Temperature Dependence Of Emergence Rate and Duration Of Pupalmentioning

confidence: 99%

“…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.

222

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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GABA‐immunoreactive neurons in the mushroom bodies of the honeybee: An electron microscopic study

Cited by 170 publications

References 55 publications

Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis

Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis

Genetically encoded dendritic marker sheds light on neuronal connectivity inDrosophila

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

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