Structural aspects of plasticity in the nervous system of Drosophila

Abstract

Neurons extend and retract dynamically their neurites during development to form complex morphologies and to reach out to their appropriate synaptic partners. Their capacity to undergo structural rearrangements is in part maintained during adult life when it supports the animal's ability to adapt to a changing environment or to form lasting memories. Nonetheless, the signals triggering structural plasticity and the mechanisms that support it are not yet fully understood at the molecular level. Here, we focus on the nervous system of the fruit fly to ask to which extent activity modulates neuronal morphology and connectivity during development. Further, we summarize the evidence indicating that the adult nervous system of flies retains some capacity for structural plasticity at the synaptic or circuit level. For simplicity, we selected examples mostly derived from studies on the visual system and on the mushroom body, two regions of the fly brain with extensively studied neuroanatomy.

Keywords: Active zone; Drosophila; Learning; Mushroom body; Mushroom body calyx; Photoreceptors; Structural plasticity; Synapse.

Fig. 1

Activity dependent modulation of neuronal connectivity during development in the Drosophila visual and MB circuits. Steps supporting the establishment of neuronal circuits in the adult Drosophila visual and olfactory systems during development

Fig. 2

Visual system and olfactory circuit in the adult fly brain. a Dorsal view of the adult Drosophila head and schematic drawing of major brain centers, including the visual system and the MB (boxes). b Horizontal section of the visual system including the retina, lamina, medulla, lobula and lobula plate. Representative neuron types cited in this review are shown, including photoreceptors (blue; R1–6, R7 and R8), lamina neurons (orange; L1-L5), medulla neurons (green) and a Lobula plate tangential cell (magenta; LPTC). c Schematic representation of the pathways delivering olfactory information to the MB. Olfactory sensory neurons (OSN) in the antennae and maxillary palps send axons to specific glomeruli in the antennal lobe (AL), where they form synaptic contacts with projection neurons (PNs). PNs convey olfactory sensory input to the lateral horn and to the calyx of the mushroom bodies (MB). In the MB calyx PN axonal projections and MB dendrites create synaptic complexes, named microglomeruli (MG). MB neurons process the olfactory information by integration of signals of anterior paired lateral neuron (APL) and dopaminergic neurons (DANs) to control mushroom body output neurons (MBONs)

Fig. 3

Environment-dependent modulation of synaptic components in the Drosophila visual and MB circuits. a Modulation of active zone components upon prolonged exposure to light. In constant darkness (DD) or in a light/dark cycle (LD), the divergent canonical Wnt pathway stabilizes the active zone structure. Constant light (LL) suppresses the divergent canonical Wnt pathway, leading to delocalization of BRP, DLiprin-α, and DRBP from active zone. Cryptochrome (Cry) forms a complex with BRP under light exposure. b Age-related structural changes in synapses of MB calyx. Ageing induces a consistent enlargement of the AZ associated with an increased number of BRP molecules