Spontaneous neuronal activity in sensory brain regions is spatiotemporally structured, suggesting that this ongoing activity may have a functional role. Nevertheless, the neuronal interactions underlying these spontaneous activity patterns, and their biological relevance, remain elusive. We addressed these questions using two-photon and light-sheet Ca2+ imaging of intact zebrafish larvae to monitor the fine structure of the spontaneous activity in the zebrafish optic tectum (the fish’s main visual center. We observed that the spontaneous activity was organized in topographically compact assemblies, grouping functionally similar neurons rather than merely neighboring ones, reflecting the tectal retinotopic map. Assemblies represent all-or-none-like sub-networks shaped by competitive dynamics, mechanisms advantageous for visual detection in noisy natural environments. Furthermore, the spontaneous activity structure also emerged in “naive” tecta (tecta of enucleated larvae before the retina connected to the tectum). We thus suggest that the formation of the tectal network circuitry is genetically prone for its functional role. This capability is an advantageous developmental strategy for the prompt execution of vital behaviors, such as escaping predators or catching prey, without requiring prior visual experience.
Mutant zebrafish larvae for the mecp2 gene display an abnormal spontaneous tectal activity, thus representing an ideal control to shed light on the biological relevance of the tectal functional connectivity. We found that the tectal assemblies limit the span of the visual responses, probably improving visual spatial resolution.