Shared neurocircuitry underlying feeding and drugs of abuse in Drosophila

Abstract

The neural circuitry and molecules that control the rewarding properties of food and drugs of abuse appear to partially overlap in the mammalian brain. This has raised questions about the extent of the overlap and the precise role of specific circuit elements in reward and in other behaviors associated with feeding regulation and drug responses. The much simpler brain of invertebrates including the fruit fly Drosophila, offers an opportunity to make high-resolution maps of the circuits and molecules that govern behavior. Recent progress in Drosophila has revealed not only some common substrates for the actions of drugs of abuse and for the regulation of feeding, but also a remarkable level of conservation with vertebrates for key neuromodulatory transmitters. We speculate that Drosophila may serve as a model for distinguishing the neural mechanisms underlying normal and pathological motivational states that will be applicable to mammals.

Keywords: Behavior; Drugs; Food; Neural circuits; Neuroscience.

Fig. 1

Schematic of the Drosophila adult brain. The diagram depicts the major neuropils and cell types discussed in this review, except for the mushroom body output neurons (MBON) that are excluded for purposes of clarity. All structures are bilaterally symmetric except for the ventral unpaired medial cells that are octopaminergic (OA-VUM) or dopaminergic (TH-VUM). Gustatory information is carried into the brain by gustatory receptor neurons (GRN) that terminate in the SOG. The TH-VUM makes an elaborate tree-like arborization in the SOG. The mushroom bodies are comprised of α/α′, β/β′, and γ lobes. The protocerebral anterior medial (PAM), protocerebral posterior lateral 1 (PPL1), and protocerebral posterior medial 3 (PPM3) clusters are all dopaminergic. The PAM and PPL1 neurons innervate distinct regions of the mushroom bodies and make both ipsilateral and contralateral (not shown) connections. The MBONs send dopamine/mushroom body information to protocerebral integration centers near the mushroom bodies. Individual PPM3 neurons innervate the ellipsoid body (doughnut) and fan-shaped body of the central complex (CC). The insulin-producing cells (IPC) of the pars intercerebralis neuroendocrine gland extend processes (not shown) medially to regions of the brain above the SOG and out of the brain to endocrine organs and other targets. The dorsal lateral protocerebral (DLP) cells express corazonin and extend processes to the IPC.