Periodic Reporting for period 1 - GlassBrain (Brain-wide processing and whole-body biophysics of directional sound)
Reporting period: 2023-01-01 to 2025-06-30
Locating sound sources such as prey or predators is critical for survival in many vertebrates. Terrestrial vertebrates achieve this by measuring the time delay and amplitude difference of sound waves arriving on each ear. For fish however, the faster speed of sound in water and the proximity of the two ears make such cues useless. Yet, directional hearing has been confirmed behaviorally, and the mechanisms have puzzled researchers for decades. Theoretical studies attempted to explain this remarkable ability, proposing that acoustic pressure and particle velocity signals must be measured separately and then be compared. However, the locus of this computation is unknown and its neuronal and biophysical mechanisms remain obscure. This is because most vertebrate brains and inner ears are highly opaque, rendering them inaccessible to systemic optical investigation.
Addressing this challenge, we recently identified the tiny glass fish Danionella as a unique vertebrate model for neuroscience. Danionella are among the smallest living vertebrates and are transparent throughout their lifespan. Despite having the smallest known vertebrate brain, they display a rich set of complex behaviors, including acoustic communication, illustrating the ethological relevance of hearing for this species. Building on our experience with acoustics and brain-wide imaging, we will exploit this model to (1) image the vibrational response of the inner ear, (2) study the neuronal activity of the sensory organs, and (3) follow the neuronal integration of sensory signals by circuits across the brain with functional imaging. These measurements will, for the first time, allow us to study the entire acoustic processing chain from acoustic stimulus, via mechanical transmission, to brain-wide neuronal integration at single cell resolution. If successful, they will constitute a major step for our understanding of hearing mechanisms in fish and illuminate the evolutionary origin of vertebrate audition.
Addressing this challenge, we recently identified the tiny glass fish Danionella as a unique vertebrate model for neuroscience. Danionella are among the smallest living vertebrates and are transparent throughout their lifespan. Despite having the smallest known vertebrate brain, they display a rich set of complex behaviors, including acoustic communication, illustrating the ethological relevance of hearing for this species. Building on our experience with acoustics and brain-wide imaging, we will exploit this model to (1) image the vibrational response of the inner ear, (2) study the neuronal activity of the sensory organs, and (3) follow the neuronal integration of sensory signals by circuits across the brain with functional imaging. These measurements will, for the first time, allow us to study the entire acoustic processing chain from acoustic stimulus, via mechanical transmission, to brain-wide neuronal integration at single cell resolution. If successful, they will constitute a major step for our understanding of hearing mechanisms in fish and illuminate the evolutionary origin of vertebrate audition.
One of the primary objectives of this project was to elucidate the mechanisms underlying directional hearing in fish, a longstanding biological puzzle that has challenged researchers for decades. The theoretical challenge arises from the physical impossibility of utilizing terrestrial-like binaural cues underwater due to the faster speed of sound in water and the close proximity of the two ears in fish. Addressing this challenge, the project successfully quantified and characterized directional hearing behavior in Danionella fish, in line with Aim 1 of the proposal. Behavioral experiments confirmed the remarkable ability of Danionella to localize sound sources with high precision, despite the constraints imposed by the aquatic environment. In parallel, an in-depth biophysical characterization was conducted (in line with Aim 2), revealing novel strategies fish use to overcome these physical limitations. The work demonstrated that Danionella employs a unique combination of acoustic pressure and particle velocity signals, which are measured separately by their sensory organs. This dual-channel processing provides the necessary information for accurate sound localization. These findings were published in Nature (2024), marking a significant advance in our understanding of auditory mechanisms in fish. Moreover, this work has provided clear predictions for the neuronal implementation of these processes. These predictions suggest the existence of specialized neural circuits capable of integrating acoustic pressure and particle velocity signals to generate directional hearing cues. The identification and functional mapping of these circuits will be a central focus for the remainder of the project, as outlined in Aims 4. By bridging biophysical measurements with behavioral outputs, this research sets the stage for uncovering the neuronal basis of directional hearing and its evolutionary significance.
These results have not only addressed key questions about fish auditory biology but also have broader implications for understanding the evolutionary origins of vertebrate hearing, paving the way for future studies in neurobiology and sensory ecology.