Mushroom body input connections form independently of sensory activity in Drosophila melanogaster

Hayashi, Tatsuya; MacKenzie, Alexander John; Ganguly, Ishani; Ellis, Kaitlyn; Smihula, Hayley Marie; Jacob, Miles Solomon; Litwin-Kumar, Ashok; Caron, Sophie

doi:10.1016/j.cub.2022.07.055

Cited by 14 publications

(31 citation statements)

References 56 publications

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“…To gauge the extent to which the Jensen-Shannon distance indicates overall similarity of the observed distributions in connectivity frequencies, we compared the distributions of connectivity frequencies measured in the experimental matrices to those measured using the corresponding uniform shuffle matrices and obtained distances ranging from 0.23 to 0.27; when we compared the distributions of connectivity frequencies measured in the experimental matrices to those measured using the biased shuffle matrices, we obtained distances ranging from 0.08 to 0.09 (Extended Data Figure 5). When we compared the distributions of connectivity frequencies measured using two D. melanogaster female matrices — one matrix was generated in this study and the other was generated in a previous study 28 — we obtained a relatively short distance of 0.17 (Figure 2c). Likewise, we obtained a relatively short distance of 0.15 when we compared the distributions measured in D. melanogaster females and males.…”

Section: Resultsmentioning

confidence: 90%

“…We performed an unbiased search for potential structural features in these connectivity matrices using principal component analysis. The variance associated with individual principal component projections provides a sensitive measure of structure as we have previously shown 25,28 . We extracted correlations within a given experimental connectivity matrix and compared them to correlations extracted from matrices in which connections were randomly shuffled.…”

Section: Resultsmentioning

confidence: 98%

“…(c) The Jensen-Shannon distances were measured by comparing the distributions in connectivity frequencies observed experimentally and reported as a heat map; the color bar denotes the length of the distances measured. See Extended Data Figure 5 for the complete set of Jensen-Shannon distances including those measured when comparing the experimental matrices to their shuffle versions or when comparing the experimental matrices to an experimental matrix obtained in a previous study 28 . (d) The p-value measured for each type of projection neuron was plotted against the log2 fold change measured when comparing the connectivity frequencies measured for that type of projection neuron in the two matrices indicated on the plot.…”

Section: Resultsmentioning

confidence: 99%

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Evolution of connectivity architecture in theDrosophilamushroom body

Caron

Ellis

Smihula

et al. 2023

Preprint

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Brain evolution has primarily been studied at the macroscopic level by comparing the relative size of homologous brain centers between species. How neuronal circuits change at the cellular level over evolutionary time remains largely unanswered. Here, using a phylogenetically informed framework, we compare the olfactory circuits of three closely related Drosophila species that differ radically in their chemical ecology: the generalists Drosophila melanogaster and Drosophila simulans that feed on fermenting fruit, and Drosophila sechellia that specializes on ripe noni fruit. We examine a central part of the olfactory circuit that has not yet been investigated in these species, the connections between the projection neurons of the antennal lobe and the Kenyon cells of the mushroom body, an associative brain center, to identify species-specific connectivity patterns. We found that neurons encoding food odors, the DC3 neurons in D. melanogaster and D. simulans and the DL2d neurons in D. sechellia, connect more frequently with Kenyon cells, giving rise to species-specific biases in connectivity. These species-specific differences in connectivity reflect two distinct neuronal phenotypes: in the number of projection neurons or in the number of presynaptic boutons formed by individual projection neurons. Our study shows how fine-grained aspects of connectivity architecture in a higher brain center can change during evolution to reflect the chemical ecology of a species.

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Section: Resultsmentioning

confidence: 90%

Section: Resultsmentioning

confidence: 98%

Section: Resultsmentioning

confidence: 99%

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Evolution of connectivity architecture in theDrosophilamushroom body

Caron

Ellis

Smihula

et al. 2023

Preprint

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“…Disruption of signaling in PNs was shown to affect the physiology and morphology of microglomeruli in the MB (Kremer et al, 2010;Pech et al, 2015;Doll et al, 2017), suggesting that experience-dependent plasticity is also a feature of olfactory neuropils other than the AL. Similarly, silencing OSNs affects the morphology of axonal terminals of PNs in the MB (Figure 3 in Hayashi et al, 2022). However, not only the inability to experience odors evokes plasticity effects in the MB, but also the sensation of odorants during appetitive learning.…”

Section: Frontiers Inmentioning

confidence: 98%

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

Fabian

Sachse

2023

Front. Cell. Neurosci.

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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.

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“…Instead, MBONs could count either Kenyon cell anatomic structures or the Kenyon cell: MBON synapse weight could be scaled by patterned, stimulus-independent neuronal activity ("PSINA") (Bajar et al, 2022). Sensory drive was also recently shown to be dispensable for PN:Kenyon cell connectivity, as animals lacking the obligate olfactory receptor subunit Orco have PN: Kenyon cell connections that are indiscriminable from controls (Hayashi et al, 2022).…”

Section: Characteristics Of Expansion Layer Neurons Govern Both Input...mentioning

confidence: 99%

Hacking brain development to test models of sensory coding

Ahmed

Rajagopalan

Pan

et al. 2023

Preprint

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Animals can discriminate myriad sensory stimuli but can also generalize from learned experience. You can probably distinguish the favorite teas of your colleagues while still recognizing that all tea pales in comparison to coffee. Tradeoffs between detection, discrimination, and generalization are inherent at every layer of sensory processing. During development, specific quantitative parameters are wired into perceptual circuits and set the playing field on which plasticity mechanisms play out. A primary goal of systems neuroscience is to understand how material properties of a circuit define the logical operations--computations--that it makes, and what good these computations are for survival. A cardinal method in biology--and the mechanism of evolution--is to change a unit or variable within a system and ask how this affects organismal function. Here, we make use of our knowledge of developmental wiring mechanisms to modify hard-wired circuit parameters in the Drosophila melanogaster mushroom body and assess the functional and behavioral consequences. By altering the number of expansion layer neurons (Kenyon cells) and their dendritic complexity, we find that input number, but not cell number, tunes odor selectivity. Simple odor discrimination performance is maintained when Kenyon cell number is reduced and augmented by Kenyon cell expansion.

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Mushroom body input connections form independently of sensory activity in Drosophila melanogaster

Cited by 14 publications

References 56 publications

Evolution of connectivity architecture in theDrosophilamushroom body

Evolution of connectivity architecture in theDrosophilamushroom body

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

Hacking brain development to test models of sensory coding

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