The brain is an adaptive system that efficiently performs unique functions in complex and continuously changing environments. Through our brain we experience, learn, progress, adapt, and create memories that make each of us unique. In fact, although we all share the same brain architecture, each of us develops his own representation of objects and surrounding environments. Why is it so? How does our brain elaborate sensory inputs to produce responses and ultimately create our very own representation of the world? Questions of this sort puzzled philosophers and scientists for centuries, and still represent a major challenge for modern science. Recent studies suggest that our sensory experience is crucially shaped by the ongoing activity of the brain, which is thought to represent the brains internal state. However, such a state remains, to a large extent, an abstract entity, difficult to capture and quantify.
Empirical observations suggest that the brain self-organizes to operate near “criticality”, a peculiar state located at the border between order and disorder. An ordered state is rigid and the information flow among units of the system is low. Conversely, a disordered state is highly erratic with unbounded spreading of perturbations and noise that prevents effective information processing. Criticality interpolates between these two states, and is characterized by unique features that could be advantageous for brain function: long-range correlations, maximal variability of spatio-temporal patterns, and wide response range to external perturbations. With these properties, criticality would provide the brain with the ability to efficiently integrate information across spatial and temporal scales, and promptly and adequately respond to external stimuli by generating a rich variety of coordinated collective behaviors, thus optimizing brain function. This is the very core of the “critical brain hypothesis”. First proposed about 40 years ago, this hypothesis basically states that the brain “lives” at criticality. Theoretical arguments and models indicate that criticality could support optimal computational capabilities by providing a favorable trade-off between reliability and flexibility needed to support complex brain functions. Despite signatures of criticality in brain activity across species (including humans), the alleged role of criticality in brain functions currently lacks direct in vivo empirical confirmation.
This project aims to test the key assumptions of the critical brain hypothesis by investigating the relation between brain criticality and functions primarily in zebrafish larvae. Why zebrafish larvae? First, because the zebrafish is a vertebrate with a relatively high genetic homology to mammals and humans, and a nervous system that shares basic architecture with other vertebrates. This often allows to generalize discoveries in zebrafish to other vertebrates, including mammals. Second, in the larval stadium the zebrafish is small and transparent, and powerful imaging and genetic methods can be applied to follow whole-brain neural activity with cellular resolution during behavioral study. To assess the functional role of criticality in systems that are located at different stages of the vertebrate evolutionary phylogenetic tree, the analysis was extended to rats and humans. This does not only inform about the universal character of self-organization to criticality in neural networks of vertebrates, but also provides first insights into its evolutionary relevance.