Abstract
The central complex represents one of the most conspicuous neuroarchitectures to be found in the insect brain and regulates a wide repertoire of behaviors including locomotion, stridulation, spatial orientation and spatial memory. In this review article, we show that in the grasshopper, a model insect system, the intricate wiring of the fan-shaped body (FB) begins early in embryogenesis when axons from the first progeny of four protocerebral stem cells (called W, X, Y, Z, respectively) in each brain hemisphere establish a set of tracts to the primary commissural system. Decussation of subsets of commissural neurons at stereotypic locations across the brain midline then establishes a columnar neuroarchitecture in the FB which is completed during embryogenesis. Examination of the expression patterns of various neurochemicals in the central complex including neuropeptides, a neurotransmitter and the gas nitric oxide (NO), show that these appear progressively and in a substance-specific manner during embryogenesis. Each neuroactive substance is expressed by neurons located at stereotypic locations in a given central complex lineage, confirming that the stem cells are biochemically multipotent. The organization of axons expressing the various neurochemicals within the central complex is topologically related to the location, and hence birthdate, of the neurons within the lineages. The neurochemical expression patterns within the FB are layered, and so reflect the temporal topology present in the lineages. This principle relates the neuroanatomical to the neurochemical architecture of the central complex and so may provide insights into the development of adaptive behaviors.
Highlights
Located in the brain midline, the insect central complex comprises five major modules: the 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), and represents one of the most distinctive neuroarchitectures to be found among arthropods
The most conspicuous central complex module is the FB whose neuroarchitecture is characterized by layers of dendritic arbors accompanying a stereotypic columnar organization, both formed by the axonal projections of clusters of neurons located in the pars intercerebralis (PI) region of each protocerebral hemisphere
Neural circuits mediating respiratory and skeletal muscle activity must mature during the embryonic phase of development, prior to hatching, and in advance of those regulating, for example, feeding, stridulation or reproduction in the freeliving phase
Summary
Modular brain structures such as the insect mushroom bodies (MB) and central complex provide an ideal substrate for studies aiming to understand the developmental/genetic basis of neuronal function and behavior (Wegerhoff and Breidbach, 1992; Ito et al, 1997; Mizunami et al, 1997; Tettamanti et al, 1997; Meinertzhagen et al, 1998; Strausfeld, 1999; Farris and Sinakevitch, 2003; Ito and Awasaki, 2008). It develops fully during embryogenesis (Boyan et al, 2008b, 2015), while in beetles, modules are added sequentially during larval development (Wegerhoff and Breidbach, 1992), and in flies, early-born neurons only become wired into the central complex during the pupal to adult transition (Renn et al, 1999; Young and Armstrong, 2010a,b; Riebli et al, 2013; Wolff et al, 2015) Despite this temporal diversity, the developmental mechanisms involved appear to be conserved and involve a process known as fascicle switching in which the axons of commissural neurons systematically decussate at stereotypic locations across the brain midline and in so doing generate the columnar neuroarchitecture required for adaptive behavior (see Boyan and Reichert, 2011; Boyan et al, 2015). Temporal topology relates the structural to the biochemical neuroarchitecture of the FB and so may provide insights into the development of adaptive behavior
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