Error-related brain state analysis using electroencephalography in conjunction with functional near-infrared spectroscopy during a complex surgical motor task.

ABSTRACT

Error-based learning is one of the basic skill acquisition mechanisms that can be modeled as a perception-action system and investigated based on brain-behavior analysis during skill training. Here, the error-related chain of mental processes is postulated to depend on the skill level leading to a difference in the contextual switching of the brain states on error commission. Therefore, the objective of this paper was to compare error-related brain states, measured with multi-modal portable brain imaging, between experts and novices during the Fundamentals of Laparoscopic Surgery (FLS) "suturing and intracorporeal knot-tying" task (FLS complex task)-the most difficult among the five psychomotor FLS tasks. The multi-modal portable brain imaging combined functional near-infrared spectroscopy (fNIRS) and electroencephalography (EEG) for brain-behavior analysis in thirteen right-handed novice medical students and nine expert surgeons. The brain state changes were defined by quasi-stable EEG scalp topography (called microstates) changes using 32-channel EEG data acquired at 250 Hz. Six microstate prototypes were identified from the combined EEG data from experts and novices during the FLS complex task that explained 77.14% of the global variance. Analysis of variance (ANOVA) found that the proportion of the total time spent in different microstates during the 10-s error epoch was significantly affected by the skill level (p < 0.01), the microstate type (p < 0.01), and the interaction between the skill level and the microstate type (p < 0.01). Brain activation based on the slower oxyhemoglobin (HbO) changes corresponding to the EEG band power (1-40 Hz) changes were found using the regularized temporally embedded Canonical Correlation Analysis of the simultaneously acquired fNIRS-EEG signals. The HbO signal from the overlying the left inferior frontal gyrus-opercular part, left superior frontal gyrus-medial orbital, left postcentral gyrus, left superior temporal gyrus, right superior frontal gyrus-medial orbital cortical areas showed significant (p < 0.05) difference between experts and novices in the 10-s error epoch. We conclude that the difference in the error-related chain of mental processes was the activation of cognitive top-down attention-related brain areas, including left dorsolateral prefrontal/frontal eye field and left frontopolar brain regions, along with a 'focusing' effect of global suppression of hemodynamic activation in the experts, while the novices had a widespread stimulus(error)-driven hemodynamic activation without the 'focusing' effect.