Johns Hopkins School of Medicine

Spatial perception, attention and memory. 

We investigate the mechanisms of spatial perception, attention and memory, systems used by humans and other animals to direct their actions and navigate in the natural environment.  Empirical studies in our lab exploit an animal model that provides explicit information about the signals it uses to guide behavior through an active sensing system.  This animal model, the echolocating bat, coordinates its production of sonar signals with flight maneuvers in response to dynamic echo information, and exhibits a rich display of natural sensory-guided behaviors.   We have established methods to collect multi-channel wireless neural recordings from free-flying bats, which allows us to study brain systems in animals engaged in natural behaviors.  Our neural recordings have focused on three brain regions:  hippocampus, midbrain superior colliculus and somatosensory cortex.

Echolocating bats navigate 3-D space to locate food and find their way home to roosting sites. They build a representation of the environment from information carried by echo returns, which lays the foundation for auditory spatial memory. The hippocampal formation is implicated in spatial memory, and we have carried out the first studies of hippocampal activity in freely echolocating bats.  We have reported on the features of hippocampal place cells in echolocating bats, which resemble those reported in rodents.   Place cells are active when an animal moves through a particular region in space, and the response areas are commonly referred to as place fields.  We have shown that hippocampal place field tuning in bats is sharpest in the time period immediately following echo returns, and place field response areas diffuse over time after sonar calls.  These results demonstrate that auditory input modulates hippocampal place field tuning, and reveals changes in space representation over time.  We are now recording from the hippocampus of free-flying bats, and have collected data demonstrating that bat hippocampal place fields show 3-D space tuning, and place field tuning depends on the rate at which the bat samples spatial information with its sonar signals.  Specifically, place field tuning is tightest when the bat produces sonar calls at a high rate and broadest when the bat produces calls at a low rate.  Interesting, place field location also appears to shift with sonar call rate.  These findings have broad implications for models and mechanisms of spatial memory. 

The success of goal-directed behaviors and spatial orientation depends on the close coordination of sensory information processing and adaptive motor control.  The midbrain superior colliculus (SC) is implicated in sensorimotor integration and species-specific orientation, including auditory-guided behaviors.   In our early work, we demonstrated 3-D auditory spatial response profiles of single neurons in the bat midbrain superior colliculus.  Three-dimensional spatial selectivity of SC neurons supports localization of sonar objects in azimuth, elevation and distance and also guides the bat’s adaptive orienting of the ears, head and echolocation call features, as the bat directs its attention towards sonar targets of interest, such as insect prey.  Furthermore, we showed that activation of neurons in the bat midbrain superior colliculus elicits movements of the head and pinna, along with production of sonar vocalizations required for acoustic orienting.  Recently, we have extended this research to quantify pre-motor, sensorimotor, and auditory responses in the midbrain superior colliculus of free-flying bats engaged in natural orienting tasks.  Importantly, this research allows us to link changes in neural activity with adaptive behaviors.

Bats, the only mammals capable of powered flight, are equipped with exquisitely sensitive and diverse arrays of sensors.  They not only use biological sonar for spatial orientation, but also rely on visual, passive auditory, tactile, magnetic and infrared sensing to guide a rich repertoire of adaptive behaviors.  With complex central nervous systems, bats can be trained to perform behavioral tasks that permit in-depth investigations of multimodal sensing.  We are currently investigating the bat’s use of tactile sensing for flight control.  Bat wings contain arrays of microscopically small and very stiff hairs that show directionally selective responses to airflow.  The bat wing sheds a leading edge vortex in slow and maneuvering flight, and most of the hairs are primarily sensitive to reverse airflow, indicating that the hairs play an important role in flight stabilization and possibly sensing if airflow has separated.  In collaboration with Ellen Lumpkin’s group at Columbia University, we have recently characterized the bat wing tactile receptors, slow-adapting Merkel cell neurite complexes and rapid-adapting lanceolate receptors, associated with the wing hairs.  Our comparative approach in this research offers new insights to sensory neuroscience and can motivate novel bio-inspired assistive devices for individuals with sensory losses.