Sequential neurogenesis in zebrafish habenula gives rise to distinct functional microcircuits

The Habenula (Hb), an evolutionarily conserved diencephalic nucleus crucial for adaptive behaviors, undergoes sequential neurogenesis in developing zebrafish, forming organized neuronal ensembles. Despite the increasing complexity of adaptive behaviors observed in developing zebrafish, the contribution of Hb neurogenesis to sensory and limbic integration remains unclear. Using in vivo birth-dating and functional brain imaging, we examined sensory-evoked activity in Hb neurons born at different developmental stages and their telencephalic input regions. Molecular markers identified distinct Hb subregions populated through different neurogenic waves, with later-born neurons displaying larger sensory responses. Notably, early-born neurons, initially exhibiting strong sensory preferences, demonstrated a capacity to reduce these preferences as the animal aged. Furthermore, we observed that later-born neurons exhibited enhanced functional connectivity with medial telencephalic regions, while early-born neurons preferred anterior regions. Our findings highlight that sequential Hb neurogenesis generates subpopulations integrating information diversely based on birthdate. Additionally, our findings challenge the notion that the sensory preference of Hb neurons is predetermined; rather, it can change as the animal ages.