How are opposite neurofeedback tasks represented at cortical and corticospinal tract levels?

The study objective was to characterise indices of learning and patterns of connectivity in two neurofeedback (NF) paradigms that modulate mu oscillations in opposite directions, and the relationship with change in excitability of the corticospinal tract (CST). Approach: Forty-three healthy volunteers participated in 3 NF sessions for upregulation (N=24) or downregulation (N=19) of individual alpha (IA) power at central location Cz. Brain signatures from multichannel electroencephalogram (EEG) were analysed, including oscillatory (power, spindles), non-oscillatory components (Hurst exponent), and effective connectivity (Directed Transfer Function) of participants who were successful at enhancing or suppressing IA power at Cz. CST excitability was studied through leg motor-evoked potential before and after the last NF session. We assessed whether participants modulated widespread alpha or central mu rhythm through the use of current source density derivation (CSD), and related the change in power in mu and upper half of mu band, to CST excitability change. Main results: In the last session, IA/mu power suppression was achieved by 79% of participants, while 63% enhanced IA. CSD-EEG revealed that mu power was upregulated through an increase in the incidence rate of bursts of alpha band activity, while downregulation involved changes in oscillation amplitude and temporal patterns. Neuromodulation also influenced frequencies adjacent to the targeted band, indicating the use of common mental strategies within groups. Directed transfer function analysis showed, for both groups, significant connectivity between structures associated with motor imagery tasks, known to modulate the excitability of the motor cortex, although most connections did not remain significant after correcting for multiple comparisons. CST excitability modulation was related to the absolute amplitude of upper mu modulation, rather than the modulation direction. Significance: The upregulation and downregulation of IA/mu power during NF, with respect to baseline were achieved via distinct mechanisms involving oscillatory and non-oscillatory EEG features. Mu enhancement and suppression post-NF and during the last NF block with respect to the baseline, respectively corresponded to opposite trends in motor-evoked potential changes post-NF. The ability of NF to modulate CST excitability could be a valuable rehabilitation tool for central nervous system disorders (stroke, spinal cord injury), where increased excitability and neural plasticity are desired. This work may inform future neuromodulation protocols and may improve NF training effectiveness by rewarding certain EEG signatures.