Burst firing in neurons that represent visual information in the Drosophila compass network

About This Grant

Abstract Successful navigation requires that our brains continuously maintain and update a sense of our orientation in space. This internal sense, called head direction (HD), is computed in dedicated neural circuits found across diverse organisms. The network mediating this representation is “dynamically stable.” In new environments, rapid synaptic plasticity between sensory neurons and HD neurons enables the HD representation to be updated by available sensory cues, so that the animal will know the direction that it is facing based on its view of the current surroundings. Conversely, the HD network must also be able to stably hold the heading representation even when environmental cues are sparse, such as when the sun becomes obscured on a cloudy day. Local excitatory loops in the network support a “bump” of high activity that reinforces the location of the HD representation, while broad inhibition is required to ensure that only a subset of HD neurons is active at once making the HD representation unique and stable. In the Drosophila HD network, a class of sensory neurons called ring neurons have been proposed to play a role in both sensory plasticity and widespread inhibition. Ring neurons form inhibitory synapses onto all HD neurons and these synapses undergo associative plasticity to link heading angle with features in the environment, though the synaptic mechanisms mediating this plasticity are not understood. My preliminary data has revealed that a subset of ring neurons that respond to visual cues fire large voltage events called “bursts” in addition to sodium spikes. I hypothesize that visual ring neuron bursts and spikes encode for strong or weak visual inputs, respectively, and that bursts are required for plasticity to link HD representation to visual cues while spikes are important for global inhibition to stabilize the network. I will address this hypothesis using cell-specific molecular perturbations, whole-cell patch-clamp electrophysiology, and in vivo voltage or calcium imaging during the presentation of visual stimuli. This project presents a rare opportunity to gain a molecular-level understanding of parallel neural codes and its importance in HD network dynamics. This work will inform how visual input entering the HD network are transformed by ring neuron spikes and bursts. I anticipate that the mechanism I discover will inform models of how HD networks in invertebrate and vertebrate systems balance flexibility and stability.