From a nonuniform brain map to motion selectivity in the owl’s midbrain

Abstract

The owl’s midbrain displays a map of auditory space. This map is a distorted representation of the environment, where the front is magnified. In addition, sound is differently attenuated by the head depending on direction, where gain increases in the front. Because neurons in the map are functionally interconnected, the nonuniform representation influences the processing of features that rely on integration across space and time. In addition, the nonuniform gain deforms spatial receptive fields, affecting history-dependent responses. As a result, neurons become sensitive to motion direction. Previous work has explained the owl’s localizing behavior by statistical inference, where uncertainty about the sensory input and prior information can be combined optimally to guide behavior. This theory can be applied to moving targets, where sensory cues must be integrated over time. This analysis shows that the midbrain neural population can be readout to predict future positions of moving targets, a critical function for a predator species. Thus, the nonuniform representation of space can induce biased computation of a higher-order stimulus feature, allowing systematic direction-selectivity and predictive power. Because neural representations where ethologically important ranges are overrepresented, are widespread in the brain, these mechanisms are likely observed in other sensory maps that guide behavior.