A Hierarchy of Time-Scales and the Brain

TLDR

Brain function can be understood as a hierarchy of temporal scales, from fast sensory fluctuations to slow contextual changes, with cortical areas arranged along a rostro‑caudal gradient that reflects their engaged time‑scale, especially evident in prefrontal cortex where complex functions operate on slowly changing representations. The paper proposes that cortical anatomy mirrors this temporal hierarchy inherent in environmental dynamics. The authors present a mathematical model that uses fast sensory input to track slower underlying causes, and review empirical evidence showing that the macroscopic cortical organization recapitulates this temporal hierarchy. The model demonstrates that slowly changing neuronal states can encode the trajectories of faster sensory states, and the resulting anatomic‑temporal framework predicts structure‑function relationships that can be tested by manipulating sensory time‑scales.

Abstract

In this paper, we suggest that cortical anatomy recapitulates the temporal hierarchy that is inherent in the dynamics of environmental states. Many aspects of brain function can be understood in terms of a hierarchy of temporal scales at which representations of the environment evolve. The lowest level of this hierarchy corresponds to fast fluctuations associated with sensory processing, whereas the highest levels encode slow contextual changes in the environment, under which faster representations unfold. First, we describe a mathematical model that exploits the temporal structure of fast sensory input to track the slower trajectories of their underlying causes. This model of sensory encoding or perceptual inference establishes a proof of concept that slowly changing neuronal states can encode the paths or trajectories of faster sensory states. We then review empirical evidence that suggests that a temporal hierarchy is recapitulated in the macroscopic organization of the cortex. This anatomic-temporal hierarchy provides a comprehensive framework for understanding cortical function: the specific time-scale that engages a cortical area can be inferred by its location along a rostro-caudal gradient, which reflects the anatomical distance from primary sensory areas. This is most evident in the prefrontal cortex, where complex functions can be explained as operations on representations of the environment that change slowly. The framework provides predictions about, and principled constraints on, cortical structure-function relationships, which can be tested by manipulating the time-scales of sensory input.