Two mechanisms facilitate regional independence between brain regions based on an examination of alpha-band activity in healthy control adult males.

BACKGROUND: At rest, 8 to 12 Hz alpha rhythms are the dominant rhythm in the brain, with a common peak alpha frequency (PAF = the frequency at which alpha generators show maximum power) observed across brain regions. Although a common PAF across brain regions should result in high between-region connectivity, especially connectivity measures assessing the phase-similarity between alpha generators, high inter-regional alpha connectivity has not been observed. The present study was conducted as an initial step toward identifying mechanisms that allow brain regions to maintain functional independence in the presence of a common PAF.

METHODS: MEG data were obtained from 16 healthy control male adults (mean age = 24 years; range 21 to 30 years). A task requiring participants to alternate between a 10 s eyes-closed condition and a 5 s eyes-open condition was used to drive parietal-occipital alpha generators, with the 10 s eyes-closed condition eliciting large-amplitude alpha activity and thus providing alpha measures with good signal-to-noise ratio for source localization. Alpha source-space measures were obtained using Vector-based Spatial-Temporal Analysis using L1-minimum-norm. In each participant, the four strongest parietal-occipital alpha generators were identified. Connectivity between sources was assessed via a measure of phase-based connectivity called inter-site phase clustering (ISPC).

RESULTS: Intra-class correlations (ICC) showed very high similarity in the average PAF (=computed using all eyes-closed data) between the four alpha sources (ICC single measure = 0.88, p < 0.001). Despite a common average PAF, across participants, significant ISPC was often observed no more than that expected by chance. Examination of the alpha time course data indicated that low ISPC was often due to instantaneous changes in alpha phase (phase slips). ISPC analyses removing data with phase slips indicated that low ISPC was also due to slight continuous changes in the alpha frequency, with frequency drift more likely in non-significant than significant ISPC trials.

CONCLUSIONS: The present exploratory effort suggested two processes underling the lack of observed inter-regional alpha phase coherence that may help maintain regional functional independence even in the presence of a common PAF. In particular, although the alpha generators were observed to oscillate at the same rate on average, across time each alpha generator oscillated a little slower or faster, and about every one and a half seconds an alpha generator abruptly lost the beat. Because of this, functional independence among alpha generators (and thus brain regions) was the rule rather than the exception. Studies replicating these processes that allow brain regions to maintain functional independence, using different source localization methods and in different conditions (e.g., a true resting state), are warranted.

IMPACT STATEMENT: Using source localization to measure parietal-occipital alpha generator activity, two properties that limit between-region alpha functional connectivity are proposed. In particular, a model of alpha generator activity is offered where via transient phase slips occurring approximately every 1.5 s, as well as slight non-stationarity in the alpha frequency, brain regions retain a common alpha frequency while also maintaining regional identity and presumably functionality. Findings also suggest novel markers for use in studies examining changes in alpha activity across maturation as well as in studies examining alpha activity in patient populations where alpha abnormalities have been reported.