Optogenetic circuit mapping reveals connectivity and synaptic physiology of T-stellate projections from the cochlear nucleus to the auditory midbrain

T-stellate neurons in the ventral cochlear nucleus (VCN) receive synaptic input from the cochlear nerve and encode information about sound frequency and intensity, including rapid fluctuations in sound intensity that are important for speech processing. T-stellate neurons are the only neuron class in the VCN that projects directly to the inferior colliculus (IC), the midbrain hub of auditory processing. However, which IC neuron populations receive T-stellate input and how T-stellate input influences IC neuron excitability remain unknown. Using channelrhodopsin-assisted circuit mapping and whole-cell patch clamp recordings in brain slices, we compared the synaptic strength, prevalence, and short-term synaptic plasticity of T-stellate input to two molecularly defined classes of IC neurons: GABAergic neuropeptide Y (NPY) neurons and glutamatergic vasoactive intestinal peptide (VIP) neurons. Our results revealed that T-stellate neurons provide excitatory input to both NPY and VIP neurons, with T-stellate input to NPY neurons having a higher incident rate, larger magnitude, and faster kinetics than T-stellate input to VIP neurons. In many instances, T-stellate input also recruited feedforward inhibition and feedforward excitation onto NPY and VIP neurons. In addition, T-stellate input to NPY and VIP neurons exhibited short-term synaptic depression that became larger in amplitude at higher stimulation frequencies. These data provide insights on how T-stellate neurons influence individual neuron types and local circuits in the IC, laying a mechanistic foundation for investigating how T-stellate input contributes to frequency tuning, amplitude modulation selectivity, and speech processing in the IC.