Mechanisms for plastic landmark anchoring in zebrafish compass neurons

Vision is a sensory modality particularly important for navigation, as it can inform animals of their current heading (i.e. visual landmarks) as well as its changes (i.e. optic flow). It has been shown that head direction (HD) neurons in various species incorporate the visual cues into their heading estimates. However, circuit mechanisms underlying this process remain still elusive in vertebrates. Here, we asked if and how the recently identified HD cells in the larval zebrafish – one of the smallest vertebrate models – incorporate visual information. By combining two-photon microscopy with a panoramic virtual reality setup, we demonstrate that the zebrafish HD cells can reliably track the orientation of multiple visual scenes, exploiting both landmark and optic flow cues. The mapping between landmark cues and the heading estimates is idiosyncratic across fish, and experience-dependent. Furthermore, we show that the landmark tracking requires the lateralized projection from the habenula to the interpeduncular nucleus (IPN), where the HD neuron processes innervate. The physiological and morphological parallels suggest that a Hebbian mechanism similar to the fly ring neuron is at work in the habenula axons. Overall, the observations that the hindbrain HD cells of the larval zebrafish lacking an elaborate visual telencephalon shed new light on the evolution of the navigation circuitry in vertebrates.