Neural dynamics and architecture of the heading direction circuit in zebrafish

In this study, Petrucco, Lavian et al. identify a circuit in the hindbrain of larval zebrafish that persistently encodes heading direction. Neurons of this network, of stereotypical morphology, inhibit each other to support ring attractor dynamics. Animals generate neural representations of their heading direction. Notably, in insects, heading direction is topographically represented by the activity of neurons in the central complex. Although head direction cells have been found in vertebrates, the connectivity that endows them with their properties is unknown. Using volumetric lightsheet imaging, we find a topographical representation of heading direction in a neuronal network in the zebrafish anterior hindbrain, where a sinusoidal bump of activity rotates following directional swims of the fish and is otherwise stable over many seconds. Electron microscopy reconstructions show that, although the cell bodies are located in a dorsal region, these neurons arborize in the interpeduncular nucleus, where reciprocal inhibitory connectivity stabilizes the ring attractor network that encodes heading. These neurons resemble those found in the fly central complex, showing that similar circuit architecture principles may underlie the representation of heading direction across the animal kingdom and paving the way to an unprecedented mechanistic understanding of these networks in vertebrates.

Automated summary

In this study, the researchers discovered a circuit in the hindbrain of larval zebrafish that persistently encodes heading direction. This neuronal network supports ring attractor dynamics through inhibitory connections between neurons. The findings show a topographical representation of heading direction in the zebrafish anterior hindbrain, with a sinusoidal bump of activity rotating as the fish swims in different directions. The electron microscopy reconstructions revealed that these neurons arborize in the interpeduncular nucleus and exhibit similar architectural principles to those found in the fly central complex, suggesting a common mechanism for representing heading direction across different animal species.