Metabolic constraints on growth explain how developmental temperature scales synaptic connectivity relevant for behavior

Abstract

SummaryEnvironmental temperature dictates the developmental pace of poikilothermic animals, but it remains unclear whether this has consequences for brain wiring and function. InDrosophilatemperature scales synaptic connectivity in the visual system, yet the underlying reasons for such scaling, the generality of this scaling across neural circuits, and the functional implications for behavior are not understood. Here we combine anatomical, functional, and theoretical approaches to gain insights into the nature and consequences of temperature dependent synaptic scaling within the fly olfactory pathway. We show that synaptic scaling leads to heterogeneous functional effects in different olfactory subcircuits, with striking consequences for odor-driven behaviors. A first-principle model that imposes different metabolic constraints on the neural system and organism development explains these findings, and generalizes to predict brain wiring under ecologically relevant temperature cycles. Our data argue that metabolic constraints dictate the extent of synaptic scaling within neural subcircuit and that the resulting circuit architecture and function are contingent upon the availability of synaptic partners. This complex interplay between synaptic scaling and partner availability underscores the intricate impact of temperature-dependent developmental plasticity on the behavior of poikilothermic animals.