Dendritic synapse geometry optimizes binaural computation in a sound localization circuit

Abstract

Clustering of synapses allows neurons to overcome attenuation of electrical signals at dendrites. However, we show in avian binaural coincidence detectors computing interaural time difference for sound localization that clustering of synapses rather promotes the dendritic attenuation but augments the intensity tolerance of the binaural computations. Using glutamate uncaging, we found in the neurons that synapses were clustered at distal dendritic branches. Modeling revealed that this strengthened sublinear integration within a dendritic tree but enabled the integration of signals from different trees when inputs grow stronger, preventing monoaural output and maintaining the dynamic range of binaural computation. The extent of this clustering differed according to dendritic length and frequency tuning of neurons, being most prominent for long dendrites and low-frequency tuning. This ensures binaural spatial hearing for wide intensity and frequency ranges, highlighting the importance of coupling of synapse geometry with dendritic morphology and input frequency in sensory signal processing.