Multiple factors shape development of olfactory glomeruli: Insights from an insect model system

Oland, Lynne A.; Tolbert, Leslie P.

doi:10.1002/(sici)1097-4695(199605)30:1<92::aid-neu9>3.0.co;2-b

Cited by 103 publications

(32 citation statements)

References 113 publications

(117 reference statements)

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“…The dorsal migration of the whole AL slows down and eventually stalls. The volume curve indicates for the AL three developmental phases, which correspond to earlier studies (Figure 7; Oland and Tolbert, 1996; Dubuque et al, 2001; see Discussion). …”

Section: Resultssupporting

confidence: 85%

3D-reconstructions and virtual 4D-visualization to study metamorphic brain development in the sphinx moth Manduca sexta

Huetteroth

2010

Front. Syst. Neurosci.

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During metamorphosis, the transition from the larva to the adult, the insect brain undergoes considerable remodeling: new neurons are integrated while larval neurons are remodeled or eliminated. One well acknowledged model to study metamorphic brain development is the sphinx moth Manduca sexta. To further understand mechanisms involved in the metamorphic transition of the brain we generated a 3D standard brain based on selected brain areas of adult females and 3D reconstructed the same areas during defined stages of pupal development. Selected brain areas include for example mushroom bodies, central complex, antennal- and optic lobes. With this approach we eventually want to quantify developmental changes in neuropilar architecture, but also quantify changes in the neuronal complement and monitor the development of selected neuronal populations. Furthermore, we used a modeling software (Cinema 4D) to create a virtual 4D brain, morphing through its developmental stages. Thus the didactical advantages of 3D visualization are expanded to better comprehend complex processes of neuropil formation and remodeling during development. To obtain datasets of the M. sexta brain areas, we stained whole brains with an antiserum against the synaptic vesicle protein synapsin. Such labeled brains were then scanned with a confocal laser scanning microscope and selected neuropils were reconstructed with the 3D software AMIRA 4.1.

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Section: Resultssupporting

confidence: 85%

3D-reconstructions and virtual 4D-visualization to study metamorphic brain development in the sphinx moth Manduca sexta

Huetteroth

2010

Front. Syst. Neurosci.

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“…In a first phase including stages P5 to P7/8, the glomerular templates are formed by ORN axons and presumably by neurites of PNs (Malun et al 1994;Oland and Tolbert 1996). In a second phase lasting from P7/8 to about P12, the principal glomeruli are formed.…”

Section: Discussionmentioning

confidence: 99%

“…After a short delay, mainly between P7/8 and P12, the interaction of ingrowing ORNs, glial cells, local (LNs) and projection (PNs) neurons leads to increased synaptogenesis in a distoproximally directed wave and to the stabilization of the glomeruli (Oland et al 1990;Tolbert and Sirianni 1990;Dubuque et al 2001). After P12, the glomeruli increase in size, probably because of the increasing neurite diameters, but the main wave of synaptogenesis seems to be complete (Tolbert et al 1983;Tolbert 1989; for reviews, see Oland and Tolbert 1996;Tolbert et al 2004). Nevertheless, the synaptic connections in the glomeruli are thought to undergo further maturation and refinement until eclosion (Tolbert et al 1983;Dubuque et al 2001).…”

Section: Introductionmentioning

confidence: 99%

Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study both developmental and adult neuronal plasticity

Huetteroth

Schachtner

2005

Cell Tissue Res

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The metamorphosing antennal lobe (AL) of the sphinx moth Manduca sexta serves as an established model system for studying neuronal development. To improve our understanding of mechanisms involved in neuronal plasticity, we have analyzed the size, shape, and localization of ten identified glomeruli at three different time points during development and in the adult, viz., (1) 13 days after pupal eclosion (P13), which reflects a time when the basic glomerular map has formed, (2) immediately after adult eclosion (A0), which represents a time when the newly formed glomeruli are uninfluenced by external odors, and (3) 4 days after adult eclosion (A4), which reflects a time when the animals have been exposed to surrounding odors. Our data from normally developing ALs of male M. sexta from P13 to A0 revealed an increase in size of all examined glomeruli of between 40% and 130%, with the strongest increases occurring in two of the three sex-specific glomeruli (cumulus, toroid). From A0 to A4, the cumulus and toroid increased significantly when correlated to AL volume, whereas the other glomeruli reached the sizes gained after A0. This study was based on antibody staining against the ubiquitous synaptic vesicle protein synaptotagmin, confocal laser scan microscopy, and the three-dimensional (3D) analysis tool AMIRA. Tissue permeability and therefore reliability of the staining quality was enhanced by using formalin/methanol fixation. The standard 3D glomeruli introduced in this study can now be used as basic tools for further examination of neuronal plasticity at the level of the identified neuropil structures, viz., the glomeruli of the AL of M. sexta.

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“…In other insects such as the fruit fly, Drosophila melanogaster, the hawk moth, Manduca sexta, as well as in social insects such as ants and bees, molecular tools (e.g., antibodies) have been very useful for understanding the development of peripheral and central chemosensory systems (Oland and Tolbert 1996;Rodrigues and Hummel 2008;Groh and Rössler 2008;Mysore et al 2010). Notably, in the genetic model Drosophila, a wealth of monoclonal and polyclonal antibodies generated against numerous molecular antigens involved in nervous system development and function are currently available and have been used extensively to understand the various aspects of peripheral and central nervous system development, including olfactory system development (reviewed by Rodrigues and Hummel 2008).…”

Section: Communicated By V Hartensteinmentioning

confidence: 99%

Brain development in the yellow fever mosquito Aedes aegypti: a comparative immunocytochemical analysis using cross-reacting antibodies from Drosophila melanogaster

et al. 2011

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Considerable effort has been directed towards understanding the organization and function of peripheral and central nervous system of disease vector mosquitoes such as Aedes aegypti. To date, all of these investigations have been carried out on adults but none of the studies addressed the development of the nervous system during the larval and pupal stages in mosquitoes. Here, we first screen a set of 30 antibodies, which have been used to study brain development in Drosophila, and identify 13 of them cross-reacting and labeling epitopes in the developing brain of Aedes. We then use the identified antibodies in immunolabeling studies to characterize general neuroanatomical features of the developing brain and compare them with the well-studied model system, Drosophila melanogaster, in larval, pupal, and adult stages. Furthermore, we use immunolabeling to document the development of specific components of the Aedes brain, namely the optic lobes, the subesophageal neuropil, and serotonergic system of the subesophageal neuropil in more detail. Our study reveals prominent differences in the developing brain in the larval stage as compared to the pupal (and adult) stage of Aedes. The results also uncover interesting similarities and marked differences in brain development of Aedes as compared to Drosophila. Taken together, this investigation forms the basis for future cellular and molecular investigations of brain development in this important disease vector.

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Multiple factors shape development of olfactory glomeruli: Insights from an insect model system

Cited by 103 publications

References 113 publications

3D-reconstructions and virtual 4D-visualization to study metamorphic brain development in the sphinx moth Manduca sexta

3D-reconstructions and virtual 4D-visualization to study metamorphic brain development in the sphinx moth Manduca sexta

Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study both developmental and adult neuronal plasticity

Brain development in the yellow fever mosquito Aedes aegypti: a comparative immunocytochemical analysis using cross-reacting antibodies from Drosophila melanogaster

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