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

Abstract

1Theta-band (4-12 Hz) activities in the frontal cortex have been thought to be a key mechanism of 2 sustained attention and goal-related behaviors, forming a phase-coherent network with task-related 3 sensory cortices for integrated neuronal ensembles. However, recent visual task studies found that 4 selective attention attenuates stimulus-related theta power in the visual cortex, suggesting a 5 functional dissociation of cortical theta oscillations. To investigate this contradictory behavior of 6 cortical theta, a visual Go/No-Go task was performed with electroencephalogram recording in mice. 7 During the No-Go period, transient theta oscillations were observed in both the frontal and visual 8 cortices, but theta oscillations of the two areas were prominent in different trial epochs. By 9 separating trial epochs based on subjects' short-term performance, we found that frontal theta was 10 prominent in good-performance epochs, while visual theta was prominent in bad-performance 11 epochs, exhibiting a functional dissociation of cortical theta rhythms. Furthermore, the two theta 12 rhythms also showed a heterogeneous pattern of phase-amplitude coupling with fast oscillations, 13 reflecting their distinct architecture in underlying neuronal circuitry. Interestingly, in good-14 performance epochs, where visual theta was relatively weak, stronger fronto-visual long-range 15 synchrony and shorter posterior-to-anterior temporal delay were found. These findings highlight a 16 previously overlooked aspect of long-range synchrony between distinct oscillatory entities in the 17 cerebral cortex and provide empirical evidence of a functional dissociation of cortical theta rhythms. 18 19 KEYWORDS 20 Theta rhythms, frontal theta, visual theta, electroencephalogram (EEG), Go/No-Go task 21 22 42 bottom right indicate 500 ms and 300 µV. (D) Summary of behavioral results. From all subjects (five 43 mice), and all sessions (10 days), data of 8,390 trials were collected. In this study, only the trials from CR 44 (n = 2,411) were analyzed. (E and F) (E) Time-frequency representation of grand-averaged event-related 45 spectral perturbation (ERSP) of each cortical area. In both the frontal and visual cortices, prominent theta 46 (4-12 Hz) oscillations were observed during 4 s of stimulus presentation (No-Go period). (F) Temporal 47 average (0.5 to 4 s) of theta oscillations in each cortical area. Numbers denote peak frequency of each 48 channel. FA: false alarm, Fr: frontal cortex, Vis: visual cortex, Amptd: amplitude, Freq: frequency. 49 4 / 35 50 Figure 2. Task performance and theta amplitude 51 (A) Distribution of pc (proportion correct) in all CR trials (n = 2,411). pc was calculated across 10 previous 52 trials. With a threshold of chance level (pc = 0.5), each trial was classified as either attentive (pc > 0.5) or 53 inattentive (pc ≤ 0.5) state. (B) Change of mean RT as function of pc. The RT of Hit trials decreased as pc 54 increased (Pearson's r = -.051, p < .05), suggesting the change of attentional level within the ...

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