How the brain perceives sensory information and generates meaningful behavior depends critically on its underlying circuitry. The protocerebral bridge (PB) is a major part of the insect central complex (CX), a premotor center that may be analogous to the human basal ganglia. Here, by deconstructing hundreds of PB single neurons and reconstructing them into a common three-dimensional framework, we have constructed a comprehensive map of PB circuits with labeled polarity and predicted directions of information flow. Our analysis reveals a highly ordered information processing system that involves directed information flow among CX subunits through 194 distinct PB neuron types. Circuitry properties such as mirroring, convergence, divergence, tiling, reverberation, and parallel signal propagation were observed; their functional and evolutional significance is discussed. This layout of PB neuronal circuitry may provide guidelines for further investigations on transformation of sensory (e.g., visual) input into locomotor commands in fly brains.
Understanding the overall patterns of information flow within the brain has become a major goal of neuroscience. In the current study, we produced a first draft of the Drosophila connectome at the mesoscopic scale, reconstructed from 12,995 images of neuron projections collected in FlyCircuit (version 1.1). Neuron polarities were predicted according to morphological criteria, with nodes of the network corresponding to brain regions designated as local processing units (LPUs). The weight of each directed edge linking a pair of LPUs was determined by the number of neuron terminals that connected one LPU to the other. The resulting network showed hierarchical structure and small-world characteristics and consisted of five functional modules that corresponded to sensory modalities (olfactory, mechanoauditory, and two visual) and the pre-motor center. Rich-club organization was present in this network and involved LPUs in all sensory centers, and rich-club members formed a putative motor center of the brain. Major intra- and inter-modular loops were also identified that could play important roles for recurrent and reverberant information flow. The present analysis revealed whole-brain patterns of network structure and information flow. Additionally, we propose that the overall organizational scheme showed fundamental similarities to the network structure of the mammalian brain.
Directional signal transmission is essential for neural circuit function and thus for connectomic analysis. The directions of signal flow can be obtained by experimentally identifying neuronal polarity (axons or dendrites). However, the experimental techniques are not applicable to existing neuronal databases in which polarity information is not available. To address the issue, we proposed SPIN: a method of Skeleton-based Polarity Identification for Neurons. SPIN was designed to work with large-scale neuronal databases in which tracing-line data are available. In SPIN, a classifier is first trained by neurons with known polarity in two steps: 1) identifying morphological features that most correlate with the polarity and 2) constructing a linear classifier by determining a discriminant axis (a specific combination of the features) and decision boundaries. Each polarity-undefined neuron is then divided into several morphological substructures (domains) and the corresponding polarities are determined using the classifier. Finally, the result is evaluated and warnings for potential errors are returned. We tested this method on fruitfly (Drosophila melanogaster) and blowfly (Calliphora vicina and Calliphora erythrocephala) unipolar neurons using data obtained from the Flycircuit and Neuromorpho databases, respectively. On average, the polarity of 84-92 % of the terminal points in each neuron could be correctly identified. An ideal performance with an accuracy between 93 and 98 % can be achieved if we fed SPIN with relatively "clean" data without artificial branches. Our result demonstrates that SPIN, as a computer-based semi-automatic method, provides quick and accurate polarity identification and is particularly suitable for analyzing large-scale data. We implemented SPIN in Matlab and released the codes under the GPLv3 license.
Computer simulations play an important role in testing hypotheses, integrating knowledge, and providing predictions of neural circuit functions. While considerable effort has been dedicated into simulating primate or rodent brains, the fruit fly (Drosophila melanogaster) is becoming a promising model animal in computational neuroscience for its small brain size, complex cognitive behavior, and abundancy of data available from genes to circuits. Moreover, several Drosophila connectome projects have generated a large number of neuronal images that account for a significant portion of the brain, making a systematic investigation of the whole brain circuit possible. Supported by FlyCircuit (http://www.flycircuit.tw), one of the largest Drosophila neuron image databases, we began a long-term project with the goal to construct a whole-brain spiking network model of the Drosophila brain. In this paper, we report the outcome of the first phase of the project. We developed the Flysim platform, which (1) identifies the polarity of each neuron arbor, (2) predicts connections between neurons, (3) translates morphology data from the database into physiology parameters for computational modeling, (4) reconstructs a brain-wide network model, which consists of 20,089 neurons and 1,044,020 synapses, and (5) performs computer simulations of the resting state. We compared the reconstructed brain network with a randomized brain network by shuffling the connections of each neuron. We found that the reconstructed brain can be easily stabilized by implementing synaptic short-term depression, while the randomized one exhibited seizure-like firing activity under the same treatment. Furthermore, the reconstructed Drosophila brain was structurally and dynamically more diverse than the randomized one and exhibited both Poisson-like and patterned firing activities. Despite being at its early stage of development, this single-cell level brain model allows us to study some of the fundamental properties of neural networks including network balance, critical behavior, long-term stability, and plasticity.
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