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Background  Animals use sensory cues to efficiently locate resources, but when sensory information is insufficient, they may rely on internally coded search strategies. Despite the importance of search behavior, there is limited understanding of the underlying neural mechanisms in vertebrates.    Results  Here, we report that loss of illumination initiates sophisticated light-search behavior in larval zebrafish. Using three-dimensional tracking, we show that at the onset of darkness larvae swim in a helical trajectory that is spatially restricted in the horizontal plane, before gradually transitioning to an outward movement profile. Local and outward swim patterns display characteristic features of area-restricted and roaming search strategies, differentially enhancing phototaxis to nearby and remote sources of light. Retinal signaling is only required to initiate area-restricted search, implying that photoreceptors within the brain drive the transition to the roaming search state. Supporting this,  orthopediaA  mutant larvae manifest impaired transition to roaming search, a phenotype which is recapitulated by loss of the non-visual opsin  opn4a  and somatostatin signaling.    Conclusion  These findings define distinct neuronal pathways for area-restricted and roaming search behaviors and clarify how internal drives promote goal-directed activity.    Electronic supplementary material  The online version of this article (doi:10.1186/s12915-016-0346-2) contains supplementary material, which is available to authorized users.

Search strategy is regulated by somatostatin signaling and deep brain photoreceptors in zebrafish