Variable brain wiring through scalable and relative synapse formation inDrosophila

Abstract

Variability of synapse numbers and partners despite identical genes reveals limits of genetic determinism. Non-genetic perturbation of brain wiring can therefore reveal to what extent synapse formation is precise and absolute, or promiscuous and relative. Here, we show the role of relative partner availability for synapse formation in the fly brain through perturbation of developmental temperature. Unexpectedly, slower development at lower temperatures substantially increases axo-dendritic branching, synapse numbers and non canonical synaptic partnerships of various neurons, while maintaining robust ratios of canonical synapses. Using R7 photoreceptors as a model, we further show that scalability of synapse numbers and ratios is preserved when relative availability of synaptic partners is changed in a DIPγ mutant that ablates R7's preferred synaptic partner. Behaviorally, movement activity scales inversely with synapse numbers, while movement precision and relative connectivity are congruently robust. Hence, the fly genome encodes scalable relative connectivity to develop functional, but not identical, brains.

The geometry of decision-making

“…Such variability in response is expected in animals, and is consistent with recent work on the visual response of flies, which demonstrates a link between stochastic (non-heritable) variation in brain wiring within the visual system and strength of visual orientation response to a vertical stripe target (37). Furthermore, flies that experience high temperatures during development appear to exhibit a particularly strong orientation tendency, exhibiting the most direct paths to targets while flies that experience low developmental temperatures exhibit wandering paths to targets (38). In our model such differences can be accounted for by variation in directional tuning of the neural groups, with high directional tuning (low 𝜈) being associated with a strong orientational response, and such individuals exhibiting direct tracks to targets from the outset (see Fig.…”

Behavior Individuality: A Focus on Drosophila melanogaster

“…This variation modifies the arborization of sensory neurons inducing interindividual variability perceiving temperature (Alpert et al, 2020 ; Huang et al, 2020 ). Those temperature changes affect synaptic connectivity in the D. melanogaster visual system, as flies grown at low temperatures (19°C) have more synapse numbers than the ones grown at higher temperatures (25°C) (Kiral et al, 2021 ). Furthermore, phenotypic plasticity in front of temperature variation is not exclusive of drosophilids as other social insects as honey bees show different learning abilities related to labors within the colony depending on the larvae developmental temperature (Tautz et al, 2003 ; Jeanson, 2019 ).…”

“…The genetic background of the organism and the developmental history of an individual dramatically affect how the animal will express this individuality (Dall et al, 2004 ; Sih et al, 2004 ; Wolf and Weissing, 2010 ). Although animals of the same species share the same genome, subtle changes during development (i.e., axon guidance) can have severe effects on the final connectivity of the neurons due to stochastic events altering specific behaviors (Linneweber et al, 2020 ; Kiral et al, 2021 ). In addition, environmental factors during growth and epigenetic changes will modify gene expression.…”