Acoustic communication and auditory scene analysis
The sensory world of an animal is noisy, complex and dynamic. From a barrage of stimuli, an organism must detect, sort, group and track biologically relevant signals to communicate with conspecifics, seek food, engage in courtship, avoid predators and navigate in space. Parsing, integrating and organizing complex acoustic stimuli to support such behaviors are tasks of auditory scene analysis, which must be coordinated with motor behaviors to enable successful orientation and navigation in the environment. For the echolocating bat, the analysis of auditory scenes builds upon its active production of sounds that reflect from objects in the environment. Echolocating bats not only rely on acoustic signals to track sonar objects but also to communicate with neighboring conspecifics. The features of echolocation and social calls are sometimes overlapping, raising questions about how the bat auditory receiver sorts similar acoustic signals that carry different meanings. This line of research motivates Angie Salles’s independent research plan.
Adaptive sensorimotor feedback control for spatial orientation and navigation
The sensory world of an animal is noisy, complex and dynamic. From a barrage of stimuli, an organism must detect, sort, group and track biologically relevant signals to communicate with conspecifics, seek food, engage in courtship, avoid predators and navigate in space. Parsing, integrating and organizing complex acoustic stimuli to support such behaviors are tasks of auditory scene analysis, which must be coordinated with motor behaviors to enable successful orientation and navigation in the environment. For the echolocating bat, the analysis of auditory scenes builds upon its active production of sounds that reflect from objects in the environment. Echolocating bats not only rely on acoustic signals to track sonar objects but also to communicate with neighboring conspecifics. The features of echolocation and social calls are sometimes overlapping, raising questions about how the bat auditory receiver sorts similar acoustic signals that carry different meanings. This line of research motivates Angie Salles’s independent research plan.
Comparative studies of spatial representation
Bats are mammals that have evolved a biological sonar system that is used to represent the spatial location of targets and obstacles. In turn, this spatial information is used to build a cognitive map that can guide navigation in the absence of sensory cues. My former postdoc, Nachum Ulanovsky, and I made the first neural recordings from the hippocampus of the freely behaving echolocating bat. This work broke new ground, as we characterized hippocampal place cells in bats, which share their basic features with those reported in other mammals, coupled with bouts of theta, which occurred when animals were relatively stationary and producing echolocation calls at a higher rate. The absence of continuous theta raised many questions about models of spatial representation, which has been the topic of intense debate and further investigation. In collaboration with Michael Hasselmo’s group we performed in vitro whole cell patch recordings from neurons in layer II of MEC in slices from the adult big brown bat and showed that the membrane potential resonance frequency in the bat was only 1.67 Hz, compared with 8.45 Hz (p<0.01) in the rat. We are now extending our empirical studies of the bat hippocampal formation to record activity from perched bats tracking moving targets and from the free-flying bat as it navigates in complex spatial environments. Collectively, our work demonstrates the value of a comparative approach to investigate neural systems and build a more complete understanding of spatial representation.
Neural mechanisms of spatial orientation
My lab has discovered that bats show neural specializations to support echolocation in the midbrain superior colliculus (SC), a brain region implicated in eye movement control and visual orienting in other animals. We have conducted extracellular recording studies revealing that auditory neurons in the bat SC show 3D spatial response profiles, which guide the bat’s orienting to sonar targets in azimuth, elevation and distance. This work was, in fact, the first report of 3D neurons in the mammalian midbrain (Valentine and Moss, 1997). More recently, we have carried out extracellular recordings from the SC of the free-flying bat. Implementing a real-time model of the bat’s echo scene, based on 3D video position data and microphone array recordings, we have characterized the 3D response areas of audiomotor neurons in the free-flying animal. This research exploits the bat’s natural orienting behaviors and holds broad importance for understanding brain organization and function in other mammalian species.
Resolution of sonar images
Echolocating bats perceive the distance to objects by listening to the delay of echoes, and their range resolution is better than a fraction of a millimeter, corresponding to echo delay resolution of less than a millisecond. Bats can also use echolocation to discriminate the shape and texture of objects. Over the past three decades, there has been an intense debate over the sonar range resolution of the echolocating bat. Early in my career, I conducted psychophysical experiments and theoretical work, which confirmed the bat’s sub-millimeter range resolution and served to settle this debate. The finding that bats can resolve time delay differences in the sub-milisecond range has broad applications in computational neuroscience and has motivated novel approaches to image processing and sonar and radar technology
Tactile sensing for flight control
The bat wing is a highly adaptive airfoil that enables demanding flight maneuvers, which are performed with an astonishing robustness under turbulent conditions, and stability at slow flight speeds. We have shown that the bat wing is covered with microscopically small, tactile hairs, which play a role in sensing airflow for flight control. Our data also demonstrate that tactile sensitivity of the bat wing is greater than that of the human fingertip. In collaboration with Ellen Lumpkin’s group at Columbia University, we characterized the tactile receptors on the bat wing and their innervation patterns in the dorsal root ganglia. This research revealed that wing sensory innervation differs from other vertebrate forelimbs, indicating a peripheral basis for the atypical topographic organization reported for bat somatosensory nuclei. Merkel cells were juxtaposed to almost half of wing hair follicles. These discoveries contribute to our knowledge of somatosensory signals guiding movement and inspires new technology for aerial vehicles.