Propagation of Prediction Signals Revealed by Synchronous Oscillations in the Frontotemporal Network During Tone Omission in Macaque Monkeys

Proactive sensory processing based on prediction is a fundamental ability that enables humans to respond appropriately to external events. The brain forms predictions based on sensory context and generates prediction error signals by comparing these predictions with actual sensory events, suggesting a mutually active exchange of information between prefrontal areas that generate predictions and sensory areas that represent incoming information. To elucidate the neural circuits involved in prediction and prediction error, we investigated functional coupling between prefrontal and temporal cortices using electrocorticography recordings from 256 electrodes implanted in two macaque monkeys. We employed an omission paradigm, which examines responses to omitted tones embedded within repetitive tone sequences. Monkeys were presented with tone stimuli under two conditions: one in which the timing of omission could be predicted and one in which it could not. We found differences in event-related potentials before omission onset mainly at the frontal pole, dorsolateral prefrontal cortex, and peri-arcuate electrodes, although differences after omission onset were observed primarily in the ventrolateral prefrontal cortex and peri-arcuate electrodes. Theta- and alpha-band phase synchrony between the superior temporal gyrus and prefrontal cortices increased for Predicted omissions compared with Unpredicted omissions before omission onset, whereas alpha- and beta-band synchrony increased after omission onset. Phase directionality analysis suggested that omission-related information is propagated between frontotemporal cortices, with bottom-up signals conveyed through theta-band synchrony and top-down signals through alpha- and beta-band synchrony. Considering their temporal profiles, theta-band synchrony may be involved in generating prediction itself, beta-band in generating prediction error, and alpha-band in both processes.