A many-to-one sensory circuit encodes oxygen levels and drives respiratory behaviour in Danio rerio
AbstractIn most animals, respiratory activity inversely correlates with environmental oxygen levels1,2. However, less is known about how the underlying neural circuitry encodes oxygen information and modifies behaviours. Here, we characterize the oxygen sensing circuit and reveal sensory coding principles in a Danio rerio larva, an optically accessible vertebrate that increases respiration and startle-related responses under hypoxia3. We observe that cranial sensory neurons receive input from multiple oxygen-sensing neuroendocrine cells, and then relay this information to hindbrain targets. Moreover, hypoxia evoked increase in cranial sensory dendrite calcium events indicates an oxygen-driven change in input dimensionality, which is also represented in their cytoplasm. Additionally, we estimate that a neural code using cytoplasmic calcium events requires most of the cranial sensory neurons, whereas one integrating input dimensionality needs only a third. Furthermore, we show that purinergic signalling at the neuroendocrine cell-sensory neuron synapses drives hypoxia-induced respiratory changes, independent of serotonin, which triggers startle-related responses. Collectively we demonstrate that oxygen coding employs a “many-to-one” sensory circuit that transforms ambient oxygen into neuronal activity and input dimensionality changes to impact behaviour. More broadly, we suggest that multi-dimensional coding might be a common feature of many-to-one circuit motifs, revealing a function for related circuits across species.