Rotationally Stable Dynamics Over Long Timescales Emerge in Neuronal Development

Abstract

Neuronal networks must balance the need for stable yet flexible dynamics. This is evident during brain development, when synaptic plasticity during critical windows enables adaptability to changing environments whilst ensuring the stability of population dynamics. The emergence of population dynamics that balance stability and flexibility during development is poorly understood. Here, we investigated developmental brain dynamics in larval zebrafish, using in vivo 2-photon imaging to record single-cell activity across major brain regions from 3-8 days post-fertilisation, a highly plastic period in which hunting behaviours are established. Our findings revealed region-specific trajectories in the development of such dynamic regimes: the telencephalon exhibited increased neuronal excitability and long-range correlations, alongside the emergence of scale invariant avalanche dynamics indicative of enhanced flexibility. Conversely, while other regions showed increased state transitions over development, the telencephalon demonstrated a surprising rise in state stability, characterized by slightly longer dwell times and drastically reduced angular velocity in state space. Remarkably, such rotationally stable dynamics persisted up to 5 seconds into the future, indicating the emergence of strong attractors supporting stability over long timescales. Notably, we observed that telencephalon dynamics were maintained near to but not at a phase transition, thus allowing for robust responses while remaining adaptable to novel inputs. Our results highlight regionally-specific trajectories in the relationship between flexibility and stability, illustrating how developing neuronal populations can self-organize to balance these competing demands. Significance StatementBrain networks must balance the flexibility to adapt to new stimuli with the need for stability. This trade-off is particularly important during periods of high plasticity in brain development. Our study investigates this balance by recording single-cell activity across the entire brain of developing larval zebrafish. We discovered that brain dynamics become increasingly diverse, characterized by both short and long bursts of activity, reflecting increased flexibility. Simultaneously, we observed the emergence of stable dynamics, linked to consistent activity patterns over time. Using a modelling approach, we showed that this stability was driven by the formation of stable attractors that shape the dynamic trajectories. These findings highlight how population mechanisms can shape the dynamic interplay between flexibility and stability in regional networks in the developing brain.