Predictability of evoked activity governs the geometry of spontaneous neural manifolds

Abstract

Spontaneous neural activity reflects sensory experience yet occupies a lower-dimensional subspace than evoked responses. However, the principle governing which components of experience are incorporated into this intrinsic activity has remained unknown. Here, we propose that temporal predictability is one of the organizing principles that selects which evoked dimensions enter spontaneous neural manifolds. We show that local predictive synaptic plasticity provides a circuit mechanism that selectively embeds components of evoked activity that are predictable on the intrinsic timescale of recurrent dynamics, while excluding unpredictable fluctuations. As a consequence, the dimensionality of spontaneous activity is not fixed but depends on environmental timescales: rapidly fluctuating inputs are excluded, whereas slowly varying components are retained as contextual dimensions. This framework reproduces on- and off-manifold coding observed in visual cortex, and reconciles apparently conflicting developmental observations that spontaneous and evoked activity become both more similar and more geometrically distinct over maturation. Together, these results identify temporal predictability as a key principle linking environmental statistics to the geometry of intrinsic population dynamics.