Sensory Inputs Drive Multi‑Scale Reorganization of Cortical Dynamics for Efficient Coding

Sensory inputs do more than activate individual neurons; they also reshape collective cortical dynamics. Using wide-field calcium imaging in mouse primary visual cortex (V1) during viewing factorial sets of shape, motion, and color stimuli, we simultaneously tracked thousands of neurons across the entire V1 and analyzed neural dynamics across thermodynamic, topological and geometric scales. While distributions of pairwise neuronal correlations remained unchanged, maximum-entropy models revealed that sensory inputs consistently lowered the network’s critical temperature, signifying a selective weakening of neuronal couplings and a departure from spontaneous near-criticality. This microscale decoupling dissolved modular subnetworks, integrating previously segregated neuronal communities. Consequently, neural population activity collapsed onto a lower-dimensional manifold aligned with stimulus-defined dimensions, thereby increasing linear decoding accuracy. Further formal proofs and computational modeling demonstrated a causal chain linking sensory-driven weakening of microscale couplings to reduced mesoscale modularity and enhanced macroscale manifold capacity. Thus, our study proposes microscale neuronal couplings as a mechanistic basis for cortical networks dynamically trading off exploratory variability for representational efficiency, thus unifying criticality and efficient coding, two classical signatures of cortical computation, within a coherent multiscale framework.