A distributed theta network of error generation and processing in aging

Based on previous concepts that a distributed theta network with a central "hub" in the medial frontal cortex is critically involved in movement regulation, monitoring, and control, the present study explored the involvement of this network in error processing with advancing age in humans. For that aim, the oscillatory neurodynamics of motor theta oscillations was analyzed at multiple cortical regions during correct and error responses in a sample of older adults. Response-related potentials (RRPs) of correct and incorrect reactions were recorded in a four-choice reaction task. RRPs were decomposed in the time-frequency domain to extract oscillatory theta activity. Motor theta oscillations at extended motor regions were analyzed with respect to power, temporal synchronization, and functional connectivity. Major results demonstrated that errors had pronounced effects on motor theta oscillations at cortical regions beyond the medial frontal cortex by being associated with (1) theta power increase in the hemisphere contra-lateral to the movement, (2) suppressed spatial and temporal synchronization at pre-motor areas contra-lateral to the responding hand, (2) inhibited connections between the medial frontal cortex and sensorimotor areas, and (3) suppressed connectivity and temporal phase-synchronization of motor theta networks in the posterior left hemisphere, irrespective of the hand, left, or right, with which the error was made. These findings reveal distributed effects of errors on motor theta oscillations in older subjects and support the hypothesis that error processing operates on a network level. They confirm the presence of aging-dependent functional disengagement of the medial frontal region and suggest that difficulties in controlling the focus of motor attention and response selection contribute to performance impairment in old individuals.