Acoustic communication & 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.
Adaptive sensorimotor feedback control for spatial orientation
The echolocating bat presents a powerful animal model to investigate sensorimotor integration and feedback between action and perception, as the bat produces the very acoustic signals that guide its behaviors.
Moreover, the echolocating bat adapts its echolocation signal design with changes in attentional/behavioral state, which provides an extraordinary experimental window to investigate the information the bat has processed and the information it is seeking.
By combining high-speed stereo videography and ultrasound microphone array recordings, we have made fundamental discoveries on adaptive sensorimotor control, predictive tracking, spatial attention, perception and memory, which hold importance across diverse mammalian systems.
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.
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.
Photo credit: Elisabeth Kalko
Neural mechanisms of spatial orientation
We discovered neural specializations in the bat 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.
We 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, 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.
Spatial Attention, Memory and Navigation
Echolocating bats are powerful mammalian models to investigate spatial attention, memory and navigation, due to their natural behaviors and key features of their active sensing.
Just as humans foveate objects they attend, bats direct the aim of their echolocation (acoustic flashlight) and therefore present an extraordinary opportunity to study the contribution of spatial attention to performance in natural tasks.
Indeed, the directional aim of the bat’s sonar provides a direct metric of their overt attention. We are conducting experiments that take advantage of specializations of bat species that differ in size, foraging behaviors and sensing modalities.
Examples of broad research questions we aim to answer are:
To what extend do spatial memory, attention and perception operate together to guide navigation?
Do bats use landmarks to negotiate complex environments?
Does covert attention to environmental stimuli guide navigation?
Figure taken from Kothari et al., 2018, Elife
Figure taken from Wohlgemuth, Luo and Moss, 2016, Current Opinion in Neurobiology
Figure taken from Sterbing et al., 2016, Journal of Neurophysiology