The etiology of time-varying functional connectivity (dFC) during rest is unclear. Those who hypothesize it to be neuronally relevant explore the phenomena in the context of consciousness, development and psychopathology. Yet, others have raised valid concerns regarding methodology or its significance beyond fluctuations in arousal and sleep. Here, we demonstrate how decodable covert on-going cognition contributes to dFC estimates during awake rest, suggesting that several meaningful FC configurations may be observable during rest. We also demonstrate how FC states—a common model for dFC—robustly capture periods of distinct cognition only when externally imposed, but not during rest.