The Generation of Direction Selectivity in the Auditory System

SummaryBoth human speech and animal vocal signals contain frequency-modulated (FM) sounds. Although central auditory neurons that selectively respond to the direction of frequency modulation are known, the synaptic mechanisms underlying the generation of direction selectivity (DS) remain elusive. Here we show the emergence of DS neurons in the inferior colliculus by mapping the three major subcortical auditory nuclei. Cell-attached recordings reveal a highly reliable and precise firing of DS neurons to FM sweeps in a preferred direction. By using in vivo whole-cell current-clamp and voltage-clamp recordings, we found that the synaptic inputs to DS neurons are not direction selective, but temporally reversed excitatory and inhibitory synaptic inputs are evoked in response to opposing directions of FM sweeps. The construction of such temporal asymmetry, resulting DS, and its topography can be attributed to the spectral disparity of the excitatory and the inhibitory synaptic tonal receptive fields.

► Direction selectivity emerges in the inferior colliculus of auditory system ► Synaptic circuits convert directional nonselective E/I inputs to selective outputs ► Difference of spike temporal precision results from temporal asymmetry of E/I ► Disparity of E/I synaptic receptive fields underlies the temporal asymmetry for DS