Direction selectivity mediated by adaptation in the owl's inferior colliculus

Motion direction is a crucial cue for predicting future states in natural scenes. In the auditory system, the mechanisms that confer direction selectivity to neurons are not well understood. Neither is it known whether sound motion is encoded independently of stationary sound location. Here we investigated these questions in neurons of the owl's external nucleus of the inferior colliculus, where auditory space is represented in a map. Using a high-density speaker array, we show that the preferred direction and the degree of direction selectivity can be predicted by response adaptation to sounds moving over asymmetric spatial receptive fields. At the population level, we found that preference for sounds moving toward frontal space increased with eccentricity in spatial tuning. This distribution was consistent with larger receptive-field asymmetry in neurons tuned to more peripheral auditory space. A model of suppression based on spatiotemporal summation predicted the observations. Thus, response adaptation and receptive-field shape can explain direction selectivity to acoustic motion and an orderly distribution of preferred direction.