Mismatch of structural and functional tonotopy for natural sounds in the auditory midbrain

Neurons in the auditory system are spatially organized in their responses to pure tones, and this tonotopy is expected to predict neuronal responses to more complex sounds such as vocalizations. We presented vocalizations with low-, medium- and high-frequency content to determine if selectivity of neurons in the inferior colliculus (IC) of mice respects the tonotopic spatial structure. Tonotopy in the IC predicts that neurons located in dorsal regions should only respond to low-frequency vocalizations and only neurons located in ventral regions should respond to high-frequency vocalizations. We found that responses to vocalizations were independent of location, and many neurons in the dorsal, low-frequency region of IC responded to high-frequency vocalizations. To test whether this was due to dorsal neurons having broad frequency tuning curves, we convolved each neuron's frequency tuning curve with each vocalization, and found that the tuning curves were not good predictors of the actual neural responses to the vocalizations. We then used a nonlinear model of signal transduction in the cochlea that generates distortion products to predict neural responses to the vocalizations. We found that these predictions more closely matched the actual neural responses. Our findings suggest that the cochlea distorts the frequency representation in vocalizations and some neurons use this distorted representation to encode the vocalizations.