Neuronal population model of globular bushy cells covering unit-to-unit variability

Computations of acoustic information along the central auditory pathways start in the cochlear nucleus. Bushy cells in the anteroventral cochlear nucleus, which innervate monaural and binaural stations in the superior olivary complex, process and transfer temporal cues relevant for sound localization. These cells are categorized into two groups: spherical and globular bushy cells (SBCs/GBCs). Spontaneous rates of GBCs innervated by multiple auditory nerve (AN) fibers are generally lower than those of SBCs that receive a small number of large AN synapses. In response to low-frequency tonal stimulation, both types of bushy cells show improved phase-locking and entrainment compared to AN fibers. When driven by high-frequency tones, GBCs show primary-like-with-notch or onset-L peristimulus time histograms and relatively irregular spiking. However, previous in vivo physiological studies of bushy cells also found considerable unit-to-unit variability in these response patterns. Here we present a population of models that can simulate the observed variation in GBCs. We used a simple coincidence detection model with an adaptive threshold and systematically varied its six parameters. Out of 567000 parameter combinations tested, 7520 primary-like-with-notch models and 4094 onset-L models were selected that satisfied a set of physiological criteria for a GBC unit. Analyses of the model parameters and output measures revealed that the parameters of the accepted model population are weakly correlated with each other to retain major GBC properties, and that the output spiking patterns of the model are affected by a combination of multiple parameters. Simulations of frequency-dependent temporal properties of the model GBCs showed a reasonable fit to empirical data, supporting the validity of our population modeling. The computational simplicity and efficiency of the model structure makes our approach suitable for future large-scale simulations of binaural information processing that may involve thousands of GBC units.Author summary: In the auditory system, specialized neuronal circuits process various types of acoustic information. A group of neurons, called globular bushy cells (GBCs), faithfully transfer timing information of acoustic signals to their downstream neurons responsible for the perception of sound location. Previous physiological studies found representative activity patterns of GBCs, but with substantial individual variations among them. In this study, we present a population of models, instead of creating one best model, to account for the observed variations of GBCs. We varied all six parameters of a simple auditory neuron model and selected the combinations of parameters that led to acceptable activity patterns of GBCs. In total, we tested more than half a million combinations and accepted ~11600 GBC models. Temporal spiking patterns of real GBCs depend on the sound frequency, and our model population was able to replicate this trend. The model used here is computationally efficient and can thus serve as a building block for future large-scale simulations of auditory information processing.