Variation in Synaptic Inputs Drives Functional Versatility for Sound Encoding in Globular Bushy Cells

Synaptic convergence is fundamental to neuronal circuit function, enabling diverse processing such as coincidence detection and reliable signal transmission. In sensory systems, the architecture of convergence and strengths of synaptic inputs are pivotal for extracting distinct features of the sensory stimulus. In auditory system, globular bushy cells (GBC) in the cochlear nucleus receive multiple axosomatic endbulb of Held terminals from the auditory nerves, which vary considerably in size, even among inputs targeting the same cell. However, the functional consequences of this input strength variation for sound encoding remain unclear. Here, we investigated how synaptic input variation shapes sound encoding in GBC of Mongolian gerbils, using in vitro conductance-clamp recordings and computational modeling, in which synaptic inputs with varying strengths were simulated. We found that input variation critically shapes GBC sound encoding by influencing temporal precision and firing rates. Low input variation allows GBC to act as coincidence detectors, thereby improving temporal precision. Conversely, high input variation increases overall firing rates and enhances the encoding of amplitude modulations, albeit at the expense of temporal precision. These findings suggest that inherent endbulb strength heterogeneity allows GBC to operate along a functional continuum. This variation in input strength may provide the basis for generating diverse information streams to downstream targets including the medial nucleus of the trapezoid body (MNTB).