Reconstruction of virtual neural circuits in an insect brain

Namiki, Shigehiro; Haupt, Shuichi S; Kazawa, Tomoki; Takashima, Akira; Ikeno, Hidetoshi; Kanzaki, Ryohei

doi:10.3389/neuro.01.028.2009

Cited by 15 publications

(7 citation statements)

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“…It is thus possible to create both spatial and functional maps of the AL. Anatomical and physiological maps have been generated for Drosophia melanogaster (Stocker, ; Couto et al, ; Laissue and Vosshall, ; Knaden et al, ), the honeybee Apis mellifera (Galizia et al, ), and several moth species: the turnip moth Agotis segetum (Hansson et al, ), the tobacco budworm Heliothis virescens (Lofaldli et al, ), the silk moth Bombyx mori (Namiki et al, ), and the tobacco hawk moth Manduca sexta (el Jundi et al, ; Grosse‐Wilde et al, ).…”

Section: Al Synaptic Organizationmentioning

confidence: 99%

Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster

Rybak

Talarico

Ruíz

et al. 2016

J of Comparative Neurology

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In Drosophila melanogaster olfactory sensory neurons (OSNs) establish synapses with projection neurons (PNs) and local interneurons within antennal lobe (AL) glomeruli. Substantial knowledge regarding this circuitry has been obtained by functional studies, whereas ultrastructural evidence of synaptic contacts is scarce. To fill this gap, we studied serial sections of three glomeruli using electron microscopy. Ectopic expression of a membrane-bound peroxidase allowed us to map synaptic sites along PN dendrites. Our data prove for the first time that each of the three major types of AL neurons is both pre-and postsynaptic to the other two types, as previously indicated by functional studies. PN dendrites carry a large proportion of output synapses, with approximately one output per every three input synapses. Detailed reconstructions of PN dendrites showed that these synapses are distributed unevenly, with input and output sites partially segregated along a proximal-distal gradient and the thinnest branches carrying solely input synapses. Moreover, our data indicate synapse clustering, as we found evidence of dendritic tiling of PN dendrites. PN output synapses exhibited T-shaped presynaptic densities, mostly arranged as tetrads. In contrast, output synapses from putative OSNs showed elongated presynaptic densities in which the T-bar platform was supported by several pedestals and contacted as many as 20 postsynaptic profiles. We also discovered synaptic contacts between the putative OSNs. The average synaptic density in the glomerular neuropil was about two synapses/mm 3 . These results are discussed with regard to current models of olfactory glomerular microcircuits across species. J. Comp. Neurol. 524:1920-1956, 2016. INDEXING TERMS: Drosophila melanogaster; olfactory system; glomerulus; projection neuron; ultrastructure; synaptic microcircuitsThe neural circuitry of the antennal lobe (AL) of the vinegar fly Drosophila melanogaster is one of the principal models for the study of how chemosensory information is processed in the brain. Thus it has been investigated intensively with a variety of anatomical, physiological, and genetic methods (Stocker, 1994;Vosshall and Stocker, 2007;Wilson, 2011). Very little is known, however, about the synaptic circuitry, synapse structure, numbers, and identity of pre-and postsynaptic components of this brain center.The olfactory sensory neurons (OSNs) located in the antennae and maxillary palps send axons to the AL, where they form synapses with different types of interneurons within functional and morphological units called glomeruli (Stocker, 1994;Couto et al., 2005). These generic structural features of glomerular anatomy are preserved across species (Hildebrand and Shepherd, 1997;Ache and Young, 2005;Martin et al., 2011). Olfactory glomeruli are spherical structures of synaptic neuropilThis is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work...

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Section: Al Synaptic Organizationmentioning

confidence: 99%

Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster

Rybak

Talarico

Ruíz

et al. 2016

J of Comparative Neurology

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“…We investigated PNs in the AL of the silkmoth Bombyx mori, in which neural mechanisms for olfactory processing have been well investigated (Kanzaki and Shibuya, 1983;Hill et al, 2003;Ai and Kanzaki, 2004;Namiki et al, 2009;Kaissling, 2009). A conventional intracellular staining technique performed under blind conditions is suitable for random sampling of PNs.…”

Section: Introductionmentioning

confidence: 99%

Heterogeneity in dendritic morphology of moth antennal lobe projection neurons

Namiki

Kanzaki

2011

J of Comparative Neurology

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A population of projection neurons (PNs) in the antennal lobe (AL) integrates sensory information from the antenna and is essential for processing odor information in the insect brain. We examined the anatomy of this neuronal population in the brain of the silkmoth Bombyx mori. Using intracellular dye injection, we labeled a total of 246 PNs and systematically analyzed their morphological features, including the soma position, antennocerebral tract, and number of innervating glomeruli. For example, we analyzed PNs that had somata in the different cell clusters, innervated overlapping but different groups of glomeruli, and ran through different pathways. We also identified glomeruli innervated by PNs using a previously established procedure that first classifies glomeruli into regional groups and then identifies individual glomeruli. We analyzed uniglomerular PNs (75.6% of the total) and found heterogeneity in the dendritic morphology of the PNs that was dependent on the regions and/or the innervating glomeruli. For example, most PNs innervating the macroglomerular complex did not have extraglomerular processes, whereas most PNs innervating ordinary glomeruli did. Moreover, PNs innervating the toroid glomerulus showed heterogeneity in their dendritic morphology. These PNs had dendritic arborization in different areas within the glomerulus. We found that, in some cases, the innervation pattern of the PN dendrite correlated with individual variation in the glomerular organization. These results indicate that PNs are not homogeneous populations, and in some cases morphological heterogeneity in PNs correlated with change in glomerular organization in the silkmoth AL.

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“…This mating race is not only fascinating in itself but also particularly convenient to study the chain linking perception to action, and for the investigation of search tasks in general. The advantages are the rich adaptive behavioral repertoire of insects generated by a relatively simple neuronal system [7] , [8] , a clear instinct-based task, and its suitability for testing and comparing different types of search strategies. Moths, as well as other insects, have developed a specifically adapted behavior, in addition to a specialized neuronal subsystem for the processing of pheromone information [9] , [10] .…”

Section: Introductionmentioning

confidence: 99%

Reactive Searching and Infotaxis in Odor Source Localization

et al. 2014

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Male moths aiming to locate pheromone-releasing females rely on stimulus-adapted search maneuvers complicated by a discontinuous distribution of pheromone patches. They alternate sequences of upwind surge when perceiving the pheromone and cross- or downwind casting when the odor is lost. We compare four search strategies: three reactive versus one cognitive. The former consist of pre-programmed movement sequences triggered by pheromone detections while the latter uses Bayesian inference to build spatial probability maps. Based on the analysis of triphasic responses of antennal lobe neurons (On, inhibition, Off), we propose three reactive strategies. One combines upwind surge (representing the On response to a pheromone detection) and spiral casting, only. The other two additionally include crosswind (zigzag) casting representing the Off phase. As cognitive strategy we use the infotaxis algorithm which was developed for searching in a turbulent medium. Detection events in the electroantennogram of a moth attached to a robot indirectly control this cyborg, depending on the strategy in use. The recorded trajectories are analyzed with regard to success rates, efficiency, and other features. In addition, we qualitatively compare our robotic trajectories to behavioral search paths. Reactive searching is more efficient (yielding shorter trajectories) for higher pheromone doses whereas cognitive searching works better for lower doses. With respect to our experimental conditions (2 m from starting position to pheromone source), reactive searching with crosswind zigzag yields the shortest trajectories (for comparable success rates). Assuming that the neuronal Off response represents a short-term memory, zigzagging is an efficient movement to relocate a recently lost pheromone plume. Accordingly, such reactive strategies offer an interesting alternative to complex cognitive searching.

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Reconstruction of virtual neural circuits in an insect brain

Cited by 15 publications

References 50 publications

Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster

Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster

Heterogeneity in dendritic morphology of moth antennal lobe projection neurons

Reactive Searching and Infotaxis in Odor Source Localization

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