Experience-dependent plasticity in the olfactory system of Drosophila melanogaster and other insects

Abstract

It is long known that the nervous system of vertebrates can be shaped by internal and external factors. On the other hand, the nervous system of insects was long assumed to be stereotypic, although evidence for plasticity effects accumulated for several decades. To cover the topic comprehensively, this review recapitulates the establishment of the term “plasticity” in neuroscience and introduces its original meaning. We describe the basic composition of the insect olfactory system using Drosophila melanogaster as a representative example and outline experience-dependent plasticity effects observed in this part of the brain in a variety of insects, including hymenopterans, lepidopterans, locusts, and flies. In particular, we highlight recent advances in the study of experience-dependent plasticity effects in the olfactory system of D. melanogaster, as it is the most accessible olfactory system of all insect species due to the genetic tools available. The partly contradictory results demonstrate that morphological, physiological and behavioral changes in response to long-term olfactory stimulation are more complex than previously thought. Different molecular mechanisms leading to these changes were unveiled in the past and are likely responsible for this complexity. We discuss common problems in the study of experience-dependent plasticity, ways to overcome them, and future directions in this area of research. In addition, we critically examine the transferability of laboratory data to natural systems to address the topic as holistically as possible. As a mechanism that allows organisms to adapt to new environmental conditions, experience-dependent plasticity contributes to an animal’s resilience and is therefore a crucial topic for future research, especially in an era of rapid environmental changes.

Serotonin acts through multiple cellular targets during an olfactory critical period

“…This increase in volume can be attributed to the increase in PN and LN arborizations in an odor specific manner. [19][20][21]27 A specific subpopulation of GABAergic LNs, the LN1 neurons, the adenylate cyclase rutabaga increases cAMP levels to promote CREB dependent gene transcription. This facilitates the structural plasticity observed in both the LNs and PNs.…”

“…The cellular and molecular mechanisms of structural plasticity observed in olfactory CPP in the fruit fly is well known. [18][19][20][21][22][23][24][25][26][27] Most CPP studies in Drosophila were conducted using either CO 2 or ethyl butyrate exposure as sensory stimuli, or both. With either of the odors, chronic exposure during the critical period induced structural plasticity in the relevant glomerulus causing a change of either an increase or a decrease in the glomerular volume.…”

“…At the circuit level, the structural plasticity resulting in an increase in glomerular volume is manifested through an increase in the number of LN and PN arbors innervating the glomerulus while the total number of neurons remains intact. [19][20][21]27 Glomerular volume decrease, on the other hand is caused by retraction of the OSN axon fibers upon chronic ethyl butyrate exposure in a specific glomerulus. 23 These studies demonstrated that the olfactory CPP in Drosophila shares many of the same molecular mechanisms as visual CPPs.…”

Experience-dependent glial pruning of synaptic glomeruli during the critical period

“…This temporally-restricted circuit remodeling is absolutely essential, as the last chance for significant renovation of genetically-determined brain synaptic connectivity to match the unpredictable, variable environmental input 4 . As in mammals, Drosophila critical periods open with sensory experience 5 – 7 , close to remodeling after a brief window 6 , 8 , 9 , and are only transiently reversible during this tightly restricted interval 10 – 12 . A classic critical period happens in the first few days after Drosophila eclosion, when striking brain olfactory circuit antennal lobe synaptic glomeruli remodeling occurs in response to early sensory input 5 .…”

Experience-dependent plasticity of a highly specific olfactory circuit inDrosophila melanogaster

“…Although it has been known for the past two decades that the volume of glomeruli in the olfactory system of D. melanogaster is affected by long-term exposure to odorants, the underlying cellular processes and cell types involved remained largely elusive so far (Fabian & Sachse, 2023). In our study, we focused on the highly specific olfactory circuit that is involved in the detection of the aversive odorant geosmin (Becher et al, 2010;Stensmyr et al, 2012).…”