I Can't Hear You Both at the Same Time: A Temporal Dilemma During Inter-Regional Communication

Cognitive functioning depends on the brain's ability to process sensory information and simultaneously integrate contextual feedback from higher-order regions like the prefrontal cortex (PFC). This requires the sensory cortex (SC) to handle both processes simultaneously. Some phase-coupled oscillator models propose that the scaffolding of neuronal communication occurs via oscillatory coupling of low-frequency oscillations. However, it is often neglected that processing this bidirectional input poses serious temporal constraints on the system. Specifically, is it possible for SC to be coupled to PFC, while at the same time being coupled to the sensory input? In this article, we describe the temporal constraints required to simultaneously process feedforward and feedback information through oscillatory coupling. We adopt a dynamical systems perspective to suggest mechanisms by which phase-coupled oscillator models can achieve optimal temporal dynamics for neural communication while accounting for these temporal constraints. Although initially counterintuitive, our proposed framework indicates that any viable solution of bidirectional phase-based coupling inherently relies on the feedforward scaffolding of neuronal communication. The mechanisms proposed here may generalize to other situations in which brain areas need to cope with bidirectional feedforward and feedback interactions while maintaining phase coupling.