Auditory processing by distributed circuits in the new vertebrate model Danionella translucida
Final Report Abstract
To ensure an animal’s survival, distributed networks of neurons perform intricate computations to detect and discern the nature of environmental stimuli. In order to study the neural basis of these computations we need to observe the activity of many neurons across multiple brain areas. Yet, methodological constraints have led to a focus on individual cells or small groups of neurons in isolated brain regions. Dense recordings of neuronal population activity across brain regions would not only uncover rare cell and response types that have been missed by single-cell recordings – they would also enable the study of population-level representations, topology, and inter-area interactions. The goal of this project was to understand how acoustic information is transformed by neuronal populations across successive processing steps of the vertebrate auditory pathway. To achieve this goal we took advantage of the unique properties of the transparent vocalizing fish Danionella cerebrum (formerly known as D. translucida), allowing us for the first time to densely measure neuronal population activity across the entire auditory system of an adult vertebrate. In order to map the auditory pathway and the flow of information, we employed a new microscopy approach for fast volumetric calcium imaging, which allowed us to perform whole-brain functional imaging of sensory-evoked neuronal population activity across the auditory hierarchy. We identified the major auditory processing centers in the Danionella brain from hindbrain to pallium. Next, we characterized brain-wide tuning characteristics in response to a broad range of tonal and pulse-like stimuli. To our surprise, we determined that these stimulus categories get segregated early on with almost no overlap. Using carefully selected stimuli, we revealed that this segregation is not a continuum, but represents two sharply segregated response regimes. Danionella generate social sounds consisting of temporally structured sequences of short pulses with species-specific properties. Reasoning that some aspects of their own sounds might carry particular valence and would be detected by dedicated circuits, we probed the brain for responses to a variety of social sound mimics. We determined that parts of the auditory pathway become successively more selective for the specific temporal structure of Danionella social sounds. In summary, this project established Danionella as the first adult vertebrate model organism with full optical access to its entire auditory processing chain and it provides insights into structure and function of the vertebrate auditory pathway at the population level.
Publications
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Blazed oblique plane microscopy reveals scale-invariant inference of brain-wide population activity. Nature Communications, 14(1).
Hoffmann, Maximilian; Henninger, Jörg; Veith, Johannes; Richter, Lars & Judkewitz, Benjamin
