Rapid sensorimotor adaptation to auditory midbrain silencing in free-flying bats

Echolocating bats rely on rapid processing of auditory information to guide moment-to-moment decisions related to echolocation call design and flight path selection. The fidelity of sonar echoes, however, can be disrupted in natural settings due to occlusions, noise, and conspecific jamming signals. Behavioral sensorimotor adaptation to external blocks of relevant cues has been studied extensively, but little is known about adaptations that mitigate internal sensory flow interruption. How do bats modify their sensory-guided behaviors in natural tasks when central auditory processing is interrupted? Here, we induced internal sensory interruptions by reversibly inactivating excitatory neurons in the inferior colliculus (IC) using ligand-activated inhibitory designer receptors exclusively activated by designer drugs (DREADDs). Bats were trained to navigate through one of three open windows in a curtain to obtain a food reward, while their echolocation and flight behaviors were quantified with synchronized ultrasound microphone and stereo video recordings. Under control conditions, bats reliably steered through the open window, only occasionally contacting the curtain edge. Suppressing IC excitatory activity elevated hearing thresholds, disrupted overall performance in the task, increased the frequency of curtain contact, and led to striking compensatory sensorimotor adjustments. DREADDs-treated bats modified flight trajectories to maximize returning echo information and adjusted sonar call design to boost detection of obstacles. Sensorimotor adaptations appeared immediately and did not change over successive trials, suggesting that these behavioral adaptations are mediated through existing neural circuitry. Our findings highlight the remarkable rapid adaptive strategies bats employ to compensate for internal sensory interruptions to effectively navigate their environments.