Convergence of type 1 spiral ganglion neuron subtypes onto principal neurons of the anteroventral cochlear nucleus

The mammalian auditory system encodes sounds with subtypes of spiral ganglion neurons (SGNs) that differ in sound level sensitivity, permitting discrimination across a wide range of levels. Recent work suggests the physiologically-defined SGN subtypes correspond to at least three molecular subtypes. It is not known how information from the different subtypes converges within the cochlear nucleus. We examined this issue using transgenic mice of both sexes that express Cre recombinase in SGNs that are positive for markers of two of these subtypes: CALB2 (calretinin) in type 1a SGNs, and LYPD1 in type 1c SGNs, which correspond to high- and low-sensitivity subtypes, respectively. We crossed these with mice expressing floxxed channelrhodopsin, which allowed specific activation of axons from type 1a or 1c SGNs using optogenetics. We made voltage-clamp recordings from bushy cells in the anteroventral cochlear nucleus (AVCN) and found that the synapses formed by CALB2- and LYPD1-positive SGNs had similar EPSC amplitudes and short-term plasticity. Immunohistochemistry revealed that individual bushy cells receive a mix of 1a, 1b, and 1c synapses with VGluT1-positive puncta of similar sizes. We used optogenetic stimulation during in vivo recordings to classify chopper and primary-like units as receiving vs. not-receiving 1a- or 1c-type inputs. These groups showed no significant difference in threshold or spontaneous rate, suggesting the subtypes do not segregate into distinct processing streams in the AVCN. Our results indicate that principal cells in the AVCN integrate information from all SGN subtypes with extensive convergence, which could optimize sound encoding across a large dynamic range.Significance statement Sound information is carried to the brain by auditory afferents that differ in their sensitivity to sound. Auditory afferents fall into three subtypes differing in their spontaneous and sound-evoked activity. These subtypes can be distinguished by anatomical, physiological, and molecular features. However, it is not well understood how the three subtypes relay information to the brain. We addressed this question using optogenetic stimulation to study the properties of two afferent subtypes in the anteroventral part of the cochlear nucleus. We found that the properties of synapses are indistinguishable between subtypes, and they show extensive convergence, suggesting that combining inputs with different sound level sensitivity is important for processing sound.