Plastic landmark anchoring in zebrafish compass neurons

Vision can inform animals as they navigate their environment. Landmarks can be used to maintain heading, while optic flow can be integrated to estimate turning. Although it has been shown that head direction (HD) neurons in various species use these visual cues1,2, the circuit mechanisms underlying this process in vertebrates remain unknown. Here we asked whether and how the recently identified HD cells in the larval zebrafish3, 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 visual landmarks and optic flow cues. The mapping between landmark cues and heading estimates is idiosyncratic across fish and experience dependent. Furthermore, we show that landmark tracking requires the lateralized projection from the habenula to the interpeduncular nucleus4, a structure innervated by HD neuron processes3. The physiological and morphological parallels suggest that a Hebbian mechanism similar to the fly ring neurons5,6 is at work in the habenula axons. Overall, our observation that hindbrain HD cells of larval zebrafish can utilize the visual cues despite the lack of an elaborate visual telencephalon sheds new light on the evolution of navigation circuitry in vertebrates. Using two-photon microscopy with a panoramic virtual reality setup, how head direction cells in larval zebrafish integrate visual landmarks and optic flow to track orientation is revealed.