Neural integrator and orchestrator communities shape spontaneous signaling in the human brain

Abstract

Understanding how intrinsic brain dynamics are organized is critical for explaining human cognition and sensory processing. Theoretical frameworks propose a hierarchical architecture in which some neural systems act as orchestrators, broadcasting information across the brain, whereas others serve as integrators, transforming incoming signals. Here, we quantitatively test whether this orchestration-integration framework is embedded in intrinsic brain activity, that is, in the absence of explicit cognitive/sensorial tasks. We adopt a multivariate fractional modeling framework originally developed in financial mathematics to characterize how volatility propagates across interacting markets, thereby identifying systems that act as orchestrators or integrators. We then test whether this integrator-orchestrator axis is related to human intelligence. To this end, using 7T resting-state functional magnetic resonance imaging data from 173 healthy young adults, we model spontaneous brain fluctuations with a multivariate fractional Ornstein-Uhlenbeck process to derive directional influence indices. Consistent with our predictions, we identified a bipartite organization, stable across modeling choices. At the subcortical level, the anterior thalamus, putamen, and caudate emerged as orchestrating transmitters, whereas the posterior thalamus, globus pallidus, hippocampus, amygdala, and nucleus accumbens acted as integrating receivers. At the cortical level, attentional and sensory networks functioned as orchestrating transmitters, while higher-order cognitive networks served as integrating receivers. These findings provide support for a theoretically grounded integration-orchestration framework, demonstrating that brain signaling is organized along this axis even at rest, relevant for intelligence scores. The proposed fractional framework offers a principled tool to investigate how disruptions of this balance may contribute to brain disorders. Competing Interest StatementNone.