Chemical neuroanatomy of the Drosophila central complex: Distribution of multiple neuropeptides in relation to neurotransmitters

Abstract

The central complex of the insect brain is an integration center, receiving inputs from many parts of the brain. In Drosophila it has been associated with the control of both locomotor and visually correlated behaviors. The central complex can be divided into several substructures and is comprised of a large number of neuronal types. These neurons produce classical neurotransmitters, biogenic amines, and different neuropeptides. However, the distribution of neurotransmitters and neuromodulators in central-complex circuits of Drosophila is poorly known. By immunolabeling and GAL4-directed expression of marker proteins, we analyzed the distribution of acetylcholine, glutamate, GABA, monoamines, and eight different neuropeptides; Drosophila tachykinin, short neuropeptide F, myoinhibitory peptide, allatostatin A, proctolin, SIFamide, neuropeptide F, and FMRFamide. All eight neuropeptides were localized to the fan-shaped body, the largest substructure of the central complex, and were mapped to different layers within this structure. Several populations of peptide-immunoreactive tangential and columnar neurons were identified, of which some colocalized acetylcholine. Fewer peptides were found to be expressed in the other substructures: the ellipsoid body, the protocerebral bridge, and the noduli. The ellipsoid body and the protocerebral bridge were innervated by extrinsic peptide expressing neurons. Our findings reveal that numerous neuropeptides are expressed in the central complex and that each peptide has a distinct distribution pattern, suggesting important roles for neuropeptides as neuromediators and cotransmitters in this brain area.

How ‘Basal' Are the Basal Ganglia?

“…The cellular elements of striatum and pallidum may comingle in one structure [Farries and Perkel, 2002] and exhibit a variety of other connections [Parent and Hazrati, 1995], but a twostep striatopallidal inhibitory circuit is probably the minimal criterion that could distinguish the basal ganglia from other motor-related structures like the cerebellum, midbrain tectum or motor cortex. Strausfeld and Hirth [2013a] associate two central complex neuropils with the striatum -the protocerebral bridge (PB) and the fan-shaped body (FB) -while identifying the ellipsoid body (EB) with pallidal/ As noted by Strausfeld and Hirth [2013a], the EB and parts of the LAL exhibit dense GABA-like immunoreactivity [Hanesch et al, 1989;Homberg et al, 1999;Kahsai and Winther, 2011]; this is consistent with their hypothesis. However, most of the GABAergic innervation of the EB is derived from cells that have what appear to be postsynaptic arbors in specific regions of the LAL and presynaptic arbors in the EB [Hanesch et al, 1989;Müller et al, 1997;Homberg et al, 1999;Young and Armstrong, 2010;Phillips-Portillo, 2012].…”

Single dopaminergic neurons that modulate aggression in Drosophila

“…4A, DsCam: GFP). PPM3 neurons showed strong presynaptic nsyb:GFP labeling in the third layer (20) of the fan-shaped body and in the noduli (Fig. 4C, nsyb:GFP) and strong labeling of dendritic puncta along neuronal processes outside of central complex structures (Fig.…”

Encoding wide-field motion and direction in the central complex of the cockroach, Blaberous discoidalis

“…Interestingly, a recent metaanalysis strongly suggests that the CX is deeply homologous to the mammalian basal ganglia (Strausfeld and Hirth, 2013). Moreover, the CX is heavily invested in GABAergic (inhibitory) receptors as well as receptors for numerous neuromodulators, including dopamine (Homberg et al, 1999;Kahsai and Winther, 2011;Kunst et al, 2011;Kahsai et al, 2012).…”