Spontaneous network coupling enables efficient task performance without local task-induced activations.

Neurobehavioral studies in humans have long concentrated on changes in local activity levels during repetitive executions of a task. Spontaneous neural coupling within extended networks has latterly been found to also influence performance. Here, we intend to uncover the underlying mechanisms, the relative importance and the interaction between spontaneous coupling and task-induced activations. To do so, we recorded two groups of healthy participants (male and female) during rest and while they performed either a visual perception or a motor sequence task. We demonstrate that for both tasks, stronger activations during the task as well as greater network coupling through spontaneous alpha rhythms at rest predict performance. However, high performers present an absence of classical task-induced activations, and, instead, stronger spontaneous network coupling. Activations were thus a compensation mechanism needed only in subjects with lower spontaneous network interactions. This challenges classical models of neural processing and calls for new strategies in attempts to train and enhance performance.SIGNIFICANCE STATEMENTOur findings challenge the widely accepted notion that task-induced activations are of paramount importance for behavior. This will have an important impact on interpretations of human neurobehavioral research. They further link the widely used techniques of quantifying network communication in the brain with classical neuroscience methods and demonstrate possible ways of how network communication influences human behavior. Traditional training methods attempt to enhance neural activations through task repetitions. Our findings suggest a more efficient neural target for learning: enhancing spontaneous neural interactions. This will be of major interest for a large variety of scientific fields with very broad applications in schools, work and others.