Motivated states allow plasticity of an animal’s behavior, facilitating adaptive responses to fluctuating homeostatic states and external challenges. A nearly universal motivated drive exists for finding resources. These goals are achieved by active modulation of sensory responsiveness and locomotor patterns. Despite the importance of these goal-directed behaviors for survival, the underlying neural mechanisms are still poorly understood. Here we report the identification of a novel light-search state in zebrafish that surprisingly includes an individual preference for left or right-ward movement. Using spatial analysis we found that after loss of illumination, larvae first show movement patterns consistent with a local light-search behavior that transitions to an outward exploratory phase. Each phase of the search exhibits distinct patterns of sensory responsiveness and movement trajectories that allow efficient navigation to local or remote sources of illumination respectively. Zebrafish otp mutants, null for the transcription factor Orthopedia, and previously demonstrated to have a reduced visual motor response, failed to transition out of local-search. Orthopedia is required for mid-brain dopaminergic (DA) neurons, neurosecretory neurons, and opn4a expressing deep-brain photoreceptors. Using mutants we found that the otp phenotype was not due to DA neuron loss, and was at least partially due to opn4a deep-brain photoreceptors. Next we sought to resolve the circuitry underlying the lateralized turning behavior. During local search, individuals show a robust preference for turning either left-ward or right-ward. Repeatedly testing individuals showed that an individual’s left/right turn bias persisted for at least 2 days. We have excluded genetic inheritance, sensory input, and retinal circuitry as the source of the bias. To locate circuitry establishing the bias we genetically ablated 40 different Gal4 enhancer trap labeled neuronal populations and tested for turn preference. Ablation of the xa170 enhancer trap abolished lateralized turning behavior. The xa170 expression pattern labels several populations of neurons including pineal projection neurons and hypothalamic neurons. Functional whole brain activity mapping confirmed increased pineal activity during lateralized turning implicating pineal output in the maintenance of lateralized behavior. Thus, loss of illumination initiates a behavioral state consistent with conserved search strategies observed in numerous species including C. elegans, Drosphila and mammals. This state is temporally regulated by Orthopedia specified neurons. In addition, the initial phase of the behavior exhibits a persistent left/right preference. Using this novel model we aim to dissect the circuitry of goal-mediated responses and motor asymmetry and how these impact behavioral choice.