Neuroarchitecture and neuroanatomy of the Drosophila central complex: A GAL4‐based dissection of protocerebral bridge neurons and circuits

Abstract

Insects exhibit an elaborate repertoire of behaviors in response to environmental stimuli. The central complex plays a key role in combining various modalities of sensory information with an insect's internal state and past experience to select appropriate responses. Progress has been made in understanding the broad spectrum of outputs from the central complex neuropils and circuits involved in numerous behaviors. Many resident neurons have also been identified. However, the specific roles of these intricate structures and the functional connections between them remain largely obscure. Significant gains rely on obtaining a comprehensive catalog of the neurons and associated GAL4 lines that arborize within these brain regions, and on mapping neuronal pathways connecting these structures. To this end, small populations of neurons in the Drosophila melanogaster central complex were stochastically labeled using the multicolor flip-out technique and a catalog was created of the neurons, their morphologies, trajectories, relative arrangements, and corresponding GAL4 lines. This report focuses on one structure of the central complex, the protocerebral bridge, and identifies just 17 morphologically distinct cell types that arborize in this structure. This work also provides new insights into the anatomical structure of the four components of the central complex and its accessory neuropils. Most strikingly, we found that the protocerebral bridge contains 18 glomeruli, not 16, as previously believed. Revised wiring diagrams that take into account this updated architectural design are presented. This updated map of the Drosophila central complex will facilitate a deeper behavioral and physiological dissection of this sophisticated set of structures. J. Comp. Neurol. 523:997–1037, 2015. © 2014 Wiley Periodicals, Inc.

A single-cell level and connectome-derived computational model of the Drosophila brain

“…This issue was resolved by changing the parameter Th DP from 0.01 to 0.001. To validate the performance of the new classifier, we selected the 442 neurons that were reported in Lin et al 2013 (Lin et al 2013) as test neurons because their polarity has been reported in detail by two studies (Lin et al 2013;Wolff, Iyer, and Rubin 2015). We removed the EIP neuron class, which innervates the ellipsoid body, inferior dorsofrontal protocerebrum, and protocerebral bridge, because the reported polarity is inconsistent between the two studies.…”

“…Based on Lin et al 2013 (Lin et al 2013) and Wolff et al 2015(Wolff, Iyer, andRubin 2015), who reported the anatomy of the same circuits, we were able to derive the network connections of these neurons and use them as a reference to optimize our connection estimation protocol. Lin et al 2013 (Lin et al 2013) and Wolff et al 2015(Wolff, Iyer, andRubin 2015) reported the polarity and innervated subregions of each neuron. To construct the reference connectivity of these neurons, we assumed that a neuron that projects its axonal arbor to a glomerulus forms synapses with another neuron that has its dendritic arbor in the same glomerulus.…”

A conserved plan for wiring up the fan-shaped body in the grasshopper and Drosophila

“…The various modules - protocerebral bridge (PB), fan-shaped body (FB; or upper division of the central body), ellipsoid body (EB; or lower division of the central body), noduli (N) and lateral accessory lobes (LAL) (see Strausfeld 2012; Ito et al 2014; Wolff et al 2015) - subserve a range of functions including spatial orientation and memory (Liu et al 2006; Neuser et al 2008; Pan et al 2009), as well as sensory integration for motor control (Ilius et al 1994; Strauss 2002; Heinze and Homberg 2007; Harley and Ritzmann 2010; Strausfeld and Hirth 2013). …”

“…Developmental studies have revealed that the intricate columnar wiring of the fan-shaped body is established quite rapidly, but at stages which also vary with the lifestyle of the insect. In the grasshopper, it develops fully during embryogenesis (Boyan et al 2008b, 2015), while in flies, it happens during pupal stages (Renn et al 1999; Young and Armstrong 2010; Lovick et al, 2013; Riebli et al 2013; Wolff et al 2015; Lovick et al, 2017). The columnar neuroarchitecture itself is generated by a sophisticated mechanism of axogenesis known as “fascicle switching” in which a subset of W-Z axons of the embryonic grasshopper (Boyan et al 2008b) and larval Drosophila (Young and Armstrong 2010; Riebli et al 2013) brain decussates at stereotypic locations along the brain commissure, resulting in a discrete set of fiber bundles oriented orthogonally to the commissure.…”

“…The columnar neuroarchitecture itself is generated by a sophisticated mechanism of axogenesis known as “fascicle switching” in which a subset of W-Z axons of the embryonic grasshopper (Boyan et al 2008b) and larval Drosophila (Young and Armstrong 2010; Riebli et al 2013) brain decussates at stereotypic locations along the brain commissure, resulting in a discrete set of fiber bundles oriented orthogonally to the commissure. The decussating W-Z axons belong to the so-called columnar neurons which interconnect the modules of the central complex (i.e., protocerebral bridge, fan-shaped and ellipsoid bodies, noduli; see Heinze and Homberg 2008; Pfeiffer and Homberg 2014; Wolff et al 2015). Comparative analyses suggest that the number of columns in a given species may relate to the number of lineages participating (see Strausfeld 2012) and that the mechanism is conserved throughout the Panarthropoda (Loesel et al 2002; Boyan et al 2015).…”