Structural aspects of plasticity in the nervous system of Drosophila

Sugie, Atsushi; Marchetti, Giovanni; Tavosanis, Gaia

doi:10.1186/s13064-018-0111-z

Cited by 43 publications

(42 citation statements)

References 149 publications

(156 reference statements)

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“…Athreya et al, 2017; Jonas and Kording, 2015; Sporns and Betzel, 2016) might also reveal additional networks structure. It will be of interest to learn whether this community is consistent across individuals, and whether it varies as a function of genetic background, neuronal activity levels, and environmental conditions during development (Kremer et al, 2010; Sugie et al, 2018). Even if the observed network structure is conserved across individuals, it is likely that synaptic output from food-responsive KCs is variable, given that MBON odorant responses are highly variable across individuals (Hige et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Structured sampling of olfactory input by the fly mushroom body

Zheng

Fisher

et al. 2020

Preprint

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15Associative memory formation and recall in the adult fruit fly Drosophila melanogaster is 16 subserved by the mushroom body (MB). Upon arrival in the MB, sensory information undergoes 17 a profound transformation. Olfactory projection neurons (PNs), the main MB input, exhibit 18 broadly tuned, sustained, and stereotyped responses to odorants; in contrast, their postsynaptic 19 targets in the MB, the Kenyon cells (KCs), are nonstereotyped, narrowly tuned, and only briefly 20 responsive to odorants. Theory and experiment have suggested that this transformation is 21 implemented by random connectivity between KCs and PNs. However, this hypothesis has been 22 challenging to test, given the difficulty of mapping synaptic connections between large numbers 23 of neurons to achieve a unified view of neuronal network structure. Here we used a recent 24 whole-brain electron microscopy (EM) volume of the adult fruit fly to map large numbers of PN-25 to-KC connections at synaptic resolution. Comparison of the observed connectome to precisely 26 defined null models revealed unexpected network structure, in which a subset of food-responsive 27 PN types converge on individual downstream KCs more frequently than expected. The 28 connectivity bias is consistent with the neurogeometry: axons of the overconvergent PNs tend to 29 arborize near one another in the MB main calyx, making local KC dendrites more likely to 30 receive input from those types. Computational modeling of the observed PN-to-KC network 31showed that input from the overconvergent PN types is better discriminated than input from 32 other types. These results suggest an 'associative fovea' for olfaction, in that the MB is wired to 33 better discriminate more frequently occurring and ethologically relevant combinations of food-34 related odors. 35 36 45 (DasGupta et al., 2014; Dickinson and Muijres, 2016; Ofstad et al., 2011; Owald and Waddell, 46 2015); and the stereotyped morphology and physiology of its cell types allow ready integration 47 of information across individuals (Costa et al., 2016; Nern et al., 2015). Each cell type normally 48

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Section: Discussionmentioning

confidence: 99%

Structured sampling of olfactory input by the fly mushroom body

Zheng

Fisher

et al. 2020

Preprint

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“…Many animals, including humans, exhibit brain plasticity over the course of their lifetime (May, ; Nava and Röder, ; Harris et al , ). Plasticity is widespread even at the adult stage in insects (Fahrbach and Van Nest, ; Fahrbach et al , ; Simões and Rhiner, ; Sugie et al , ). In adult insects, one brain region that exhibits plasticity is the mushroom body (MB).…”

Section: Introductionmentioning

confidence: 99%

Queen Dominance May Reduce Worker Mushroom Body Size in a Social Bee

Jaumann

Seid

Simons

et al. 2019

Developmental Neurobiology

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The mushroom body (MB) is an area of the insect brain involved in learning, memory, and sensory integration. Here, we used the sweat bee Megalopta genalis (Halictidae) to test for differences between queens and workers in the volume of the MB calyces. We used confocal microscopy to measure the volume of the whole brain, MB calyces, optic lobes, and antennal lobes of queens and workers. Queens had larger brains, larger MB calyces, and a larger MB calyces:whole brain ratio than workers, suggesting an effect of social dominance in brain development. This could result from social interactions leading to smaller worker MBs, or larger queen MBs. It could also result from other factors, such as differences in age or sensory experience. To test these explanations, we next compared queens and workers to other groups. We compared newly emerged bees, bees reared in isolation for 10 days, bees initiating new observation nests, and bees initiating new natural nests collected from the field to queens and workers. Queens did not differ from these other groups. We suggest that the effects of queen dominance over workers, rather than differences in age, experience, or reproductive status, are responsible for the queen-worker differences we observed. Worker MB development may be affected by queen aggression directly and/or manipulation of larval nutrition, which is provisioned by the queen. We found no consistent differences in the size of antennal lobes or optic lobes associated with differences in age, experience, reproductive status, or social caste.

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“…Landmark studies in kittens have shown that depriving them of visual input during an early critical period by suturing their eyelids permanently impaired their vision, even after their eyes were opened again (Hubel and Wiesel, 1964). Activity can refine the patterns of connections through Hebbian and/or homeostatic plasticity mechanisms (Kaneko et al, 2017;Marder, 2011;Schulz and Lane, 2017;Sheng et al, 2018;Sugie et al, 2018;Tien and Kerschensteiner, 2018;Tripodi et al, 2008;Turrigiano, 2017;Yuan et al, 2011). However, what kinds of changes are induced within the network in response to selective silencing of specific neuron types is not fully understood.…”

Section: Discussionmentioning

confidence: 99%

“…This raises the possibility that neuronal activity between 28 developing neurons might contribute to wiring specificity (Akin et al, 2019), in addition to specific partner--derived molecular cues. Despite extensive work investigating the role of activity in circuit formation, it is still unclear whether activity is involved in partner specificity (Kaneko and Ye, 2015;Sugie et al, 2018).…”

Section: Lack Of Chordotonal Activity During Development Alters Connementioning

confidence: 99%

“…In such a scenario, additional activity-dependent mechanisms could refine those connections to form functional circuits. Indeed, activity has been shown to refine the patterns of connections in many systems, through Hebbian and/or homeostatic plasticity mechanisms (Giachello and Baines, 2015;; Kaneko et al, 2017;; Marder, 2011;; Schulz and Lane, 2017;; Sheng et al, 2018;; Sugie et al, 2018;; Tien and Kerschensteiner, 2018;; Tripodi et al, 2008;; Turrigiano, 2017;; Yuan et al, 2011). Thus, neurons that fire together have been shown to preferentially wire together in many areas of the vertebrate nervous system through positive feedback (Brown et al, 2009).…”

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confidence: 99%

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Synaptic specificity is collectively determined by partner identity, location and activity

Valdes-Aleman

Fetter

Sales

et al. 2019

Preprint

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Our nervous system is organized into circuits with specifically matched and tuned cell-to-cell connections that are essential for proper function. The mechanisms by which presynaptic axon terminals and postsynaptic dendrites recognize each other and establish the correct number of connections are still incompletely understood. Sperry's chemoaffinity hypothesis proposes that pre- and postsynaptic partners express specific combinations of molecules that enable them to recognize each other. Alternatively, Peters' rule proposes that presynaptic axons and postsynaptic dendrites use non-partner-derived global positional cues to independently reach their target area, and once there they randomly connect with any available neuron. These connections can then be further refined by additional mechanisms based on synaptic activity. We used the tractable genetic model system, the Drosophila embryo and larva, to test these hypotheses and elucidate the roles of 1) global positional cues, 2) partner-derived cues and 3) synaptic activity in the establishment of selective connections in the developing nerve cord. We altered the position or activity of presynaptic partners and analyzed the effect of these manipulations on the number of synapses with specific postsynaptic partners, strength of functional connections, and behavior controlled by these neurons. For this purpose, we combined 2 developmental live imaging, electron microscopy reconstruction of circuits, functional imaging of neuronal activity, and behavioral experiments in wildtype and experimental animals. We found that postsynaptic dendrites are able to find, recognize, and connect to their presynaptic partners even when these have been shifted to ectopic locations through the overexpression of receptors for midline guidance cues. This suggests that neurons use partner-derived cues that allow them to identify and connect to each other. However, while partner-derived cues are sufficient for recognition between specific partners and establishment of connections;; without orderly positioning of axon terminals by positional cues and without synaptic activity during embryonic development, the numbers of functional connections are altered with significant consequences for behavior. Thus, multiple mechanisms including global positional cues, partner-derived cues, and synaptic activity contribute to proper circuit assembly in the developing Drosophila nerve cord.

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Structural aspects of plasticity in the nervous system of Drosophila

Cited by 43 publications

References 149 publications

Structured sampling of olfactory input by the fly mushroom body

Structured sampling of olfactory input by the fly mushroom body

Queen Dominance May Reduce Worker Mushroom Body Size in a Social Bee

Synaptic specificity is collectively determined by partner identity, location and activity

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