Abstract
BackgroundAnimals 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.ResultsHere, 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.ConclusionThese findings define distinct neuronal pathways for area-restricted and roaming search behaviors and clarify how internal drives promote goal-directed activity.
Highlights
Animals use sensory cues to efficiently locate resources, but when sensory information is insufficient, they may rely on internally coded search strategies
Search behavior requires the maintenance of an internal state that appropriately regulates motor activity, and potentially modulates sensory thresholds to facilitate the discovery of desirable resources [18, 19]
Our results reveal that retinal signaling and deep brain photoreceptors differentially trigger local and roaming search states; retinal signaling is required for local movement, whereas otpa-dependent sst1.1-expressing neurons and opn4a-expressing deepbrain photoreceptors sustain roaming search behavior
Summary
Animals use sensory cues to efficiently locate resources, but when sensory information is insufficient, they may rely on internally coded search strategies. Animals use a range of behavioral strategies to search for resource rich areas [1]. Sophisticated search behaviors under natural conditions have been catalogued in vertebrates, surprisingly few studies have exploited vertebrate models to probe genetic factors and neuronal connections that initiate and maintain active search states [8,9,10,11]. Larvae use sensory information in several modalities to actively navigate within the environment, initiating approach or avoidance behaviors as required. Search behavior requires the maintenance of an internal state that appropriately regulates motor activity, and potentially modulates sensory thresholds to facilitate the discovery of desirable resources [18, 19]. Short-term internal states such as arousal and hunger, and movement profiles consistent with exploratory behavior are present in larval stage
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