Functional dissociation of theta oscillations in the frontal and visual cortices and their long-range network during sustained attention

ABSTRACT Theta-band (4–12 Hz) activities in the frontal cortex have been thought to be a key mechanism of sustained attention and goal-related behaviors, forming a phase-coherent network with task-related sensory cortices for integrated neuronal ensembles. However, recent visual task studies found that selective attention attenuates stimulus-related theta power in the visual cortex, suggesting a functional dissociation of cortical theta oscillations. To investigate this contradictory behavior of cortical theta, a visual Go/No-Go task was performed with electroencephalogram recording in mice. During the No-Go period, transient theta oscillations were observed in both the frontal and visual cortices, but theta oscillations of the two areas were prominent in different trial epochs. By separating trial epochs based on subjects’ short-term performance, we found that frontal theta was prominent in good-performance epochs, while visual theta was prominent in bad-performance epochs, exhibiting a functional dissociation of cortical theta rhythms. Furthermore, the two theta rhythms also showed a heterogeneous pattern of phase-amplitude coupling with fast oscillations, reflecting their distinct architecture in underlying neuronal circuitry. Interestingly, in good-performance epochs, where visual theta was relatively weak, stronger fronto-visual long-range synchrony and shorter posterior-to-anterior temporal delay were found. These findings highlight a previously overlooked aspect of long-range synchrony between distinct oscillatory entities in the cerebral cortex and provide empirical evidence of a functional dissociation of cortical theta rhythms. IN BRIEF Previous literature emphasized the pro-cognitive role of coherent oscillatory networks between distal brain regions, such as the fronto-visual theta synchrony. However, such a conceptual framework has been challenged as recent findings revealed distinct behavioral correlates of theta oscillations found in different cortical regions, especially in the frontal and visual cortices. Here, we show that frontal and visual theta represent distinct cortical processes and that the functional connectivity between them increases during sustained attention, especially when one of the two theta rhythms is relatively suppressed. The data presented here highlight a novel aspect of neural long-range synchrony between distinct cortical oscillators with distinct functional significance in task performance.