Representing three-dimensional space with sound: Adaptive behaviors and neural recordings from free-flying echolocating bats
Animals that rely on active sensing present particularly powerful models for investigating the neural substrates of behavior, as their actions directly influence signals used to sense the environment. Echolocating bats, for example, transmit high frequency sounds and process information carried by returning echoes to determine the three-dimensional (3D) location of objects in the environment. In turn, bats adapt the direction, duration and temporal patterning of echolocation signals in response to spatial information extracted from echoes. To investigate the neural underpinnings of 3D spatial representation and the influence of adaptive sonar behavior on sensory-evoked activity, we characterized the response profiles of auditory neurons in the midbrain superior colliculus of free-flying bats engaged in naturalistic echolocation tasks. Our study reveals that single midbrain neurons respond selectivity to both the direction and distance (echo delay) of sonar returns from physical objects along the bat’s flight path. Further, we discovered that 3D spatial tuning and response areas of midbrain neurons were modulated by the bat’s temporal patterning of its echolocation calls. These findings highlight the importance of engaging animals in natural tasks to investigate the dynamics of neural systems.