Changes in functional neuroimaging measures as novices gain proficiency on the fundamentals of laparoscopic surgery suturing task.

Significance: As trainees practice fundamental surgical skills, they typically rely on performance measures such as time and errors, which are limited in their sensitivity. Aim: The goal of our study was to evaluate the use of portable neuroimaging measures to map the neural processes associated with learning basic surgical skills. Approach: Twenty-one subjects completed 15 sessions of training on the fundamentals of laparoscopic surgery (FLS) suture with intracorporeal knot-tying task in a box trainer. Functional near infrared spectroscopy data were recorded using an optode montage that covered the prefrontal and sensorimotor brain areas throughout the task. Average oxy-hemoglobin (HbO) changes were determined for repetitions performed during the first week of training compared with the third week of training. Statistical differences between the time periods were evaluated using a general linear model of the HbO changes. Results: Average performance scores across task repetitions increased significantly from the first day to the last day of training ( p < 0.01 ). During the first day of training, there was significant lateral prefrontal cortex (PFC) activation. On the final day, significant activation was observed in the PFC, as well as the sensorimotor areas. When comparing the two periods, significant differences in activation ( p < 0.05 ) were found for the right medial PFC and the right inferior parietal gyrus. While gaining proficiency, trainees activated the perception-action cycle to build a perceptual model and then apply the model to improve task execution. Conclusions: Learners engaged the sensorimotor areas more substantially as they developed skill on the FLS suturing task. These findings are consistent with findings for the FLS pattern cutting task and contribute to the development of objective metrics for skill evaluation.

Portable neuroimaging differentiates novices from those with experience for the Fundamentals of Laparoscopic Surgery (FLS) suturing with intracorporeal knot tying task.

BACKGROUND: The goal of this study was to compare the brain activation patterns of experienced and novice individuals when performing the Fundamentals of Laparoscopic Surgery (FLS) suture with intracorporeal knot tying task, which requires bimanual motor control. METHODS: Twelve experienced and fourteen novice participants completed this cross-sectional observational study. Participants performed three repetitions of the FLS suture with intracorporeal knot tying task in a standard box trainer. Functional near infrared spectroscopy (fNIRS) data was recorded using an optode montage that covered the prefrontal and sensorimotor brain areas throughout the task. Data processing was conducted using the HOMER3 and AtlasViewer toolboxes to determine the oxy-hemoglobin (HbO) and deoxyhemoglobin (HbR) concentrations. The hemodynamic response function based on HbO changes during the task relative to the resting state was averaged for each repetition and by participant. Group-level differences were evaluated using a general linear model of the HbO changes with significance set at p < 0.05. RESULTS: The average performance score for the experienced group was significantly higher than the novice group (p < 0.01). There were significant cortical activations (p < 0.05) in the prefrontal and sensorimotor areas for the experienced and novice groups. Areas of statistically significant differences in activation included the right dorsolateral prefrontal cortex (PFC), the right precentral gyrus, and the right postcentral gyrus. CONCLUSIONS: Portable neuroimaging allowed for the differentiation of brain regions activated by experienced and novice participants for a complex surgical motor task. This information can be used to support the objective evaluation of expertise during surgical skills training and assessment.

Brain-behavior analysis of transcranial direct current stimulation effects on a complex surgical motor task.

Transcranial Direct Current Stimulation (tDCS) has demonstrated its potential in enhancing surgical training and performance compared to sham tDCS. However, optimizing its efficacy requires the selection of appropriate brain targets informed by neuroimaging and mechanistic understanding. Previous studies have established the feasibility of using portable brain imaging, combining functional near-infrared spectroscopy (fNIRS) with tDCS during Fundamentals of Laparoscopic Surgery (FLS) tasks. This allows concurrent monitoring of cortical activations. Building on these foundations, our study aimed to explore the multi-modal imaging of the brain response using fNIRS and electroencephalogram (EEG) to tDCS targeting the right cerebellar (CER) and left ventrolateral prefrontal cortex (PFC) during a challenging FLS suturing with intracorporeal knot tying task. Involving twelve novices with a medical/premedical background (age: 22-28 years, two males, 10 females with one female with left-hand dominance), our investigation sought mechanistic insights into tDCS effects on brain areas related to error-based learning, a fundamental skill acquisition mechanism. The results revealed that right CER tDCS applied to the posterior lobe elicited a statistically significant (q < 0.05) brain response in bilateral prefrontal areas at the onset of the FLS task, surpassing the response seen with sham tDCS. Additionally, right CER tDCS led to a significant (p < 0.05) improvement in FLS scores compared to sham tDCS. Conversely, the left PFC tDCS did not yield a statistically significant brain response or improvement in FLS performance. In conclusion, right CER tDCS demonstrated the activation of bilateral prefrontal brain areas, providing valuable mechanistic insights into the effects of CER tDCS on FLS peformance. These insights motivate future investigations into the effects of CER tDCS on error-related perception-action coupling through directed functional connectivity studies.

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

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.

Error related fNIRS-EEG microstate analysis during a complex surgical motor task.

Fundamentals of Laparoscopic Surgery (FLS) is a standard education and training module with a set of basic surgical skills. During surgical skill acquisition, novices need to learn from errors due to perturbations in their performance which is one of the basic principles of motor skill acquisition. This study on thirteen healthy novice medical students and nine expert surgeons aimed to capture the brain state during error epochs using multimodal brain imaging by combining functional near-infrared spectroscopy (fNIRS) and electroencephalography (EEG). We performed error-related microstate analysis in the latent space that was found using regularized temporally embedded Canonical Correlation Analysis from fNIRS-EEG recordings during the performance of FLS "suturing and intracorporeal knot-tying" task - the most difficult among the five psychomotor FLS tasks. We found from two-way analysis of variance (ANDVA) with factors, skill level (expert, novice), and microstate type (1-6) that the proportion of the total time spent in microstates in the error epochs was significantly affected by the skill level ( ), microstate type ( ), and the interaction between the skill level and the microstate type ( ). Therefore, our study highlighted the relevance of portable brain imaging to capture error behavior when comparing the skill level during a complex surgical task. Clinical Relevance-This establishes the brain-behavior relationship for monitoring complex surgical motor task errors that differentiated experts from novices.

Portable Neuroimaging-Guided Noninvasive Brain Stimulation of the Cortico-Cerebello-Thalamo-Cortical Loop-Hypothesis and Theory in Cannabis Use Disorder.

BACKGROUND: Maladaptive neuroplasticity-related learned response in substance use disorder (SUD) can be ameliorated using noninvasive brain stimulation (NIBS); however, inter-individual variability needs to be addressed for clinical translation. OBJECTIVE: Our first objective was to develop a hypothesis for NIBS for learned response in SUD based on a competing neurobehavioral decision systems model. The next objective was to develop the theory by conducting a computational simulation of NIBS of the cortico-cerebello-thalamo-cortical (CCTC) loop in cannabis use disorder (CUD)-related dysfunctional "cue-reactivity"-a construct closely related to "craving"-that is a core symptom. Our third objective was to test the feasibility of a neuroimaging-guided rational NIBS approach in healthy humans. METHODS: "Cue-reactivity" can be measured using behavioral paradigms and portable neuroimaging, including functional near-infrared spectroscopy (fNIRS) and electroencephalogram (EEG) metrics of sensorimotor gating. Therefore, we conducted a computational simulation of NIBS, including transcranial direct current stimulation (tDCS) and transcranial alternating current stimulation (tACS) of the cerebellar cortex and deep cerebellar nuclei (DCN) of the CCTC loop for its postulated effects on fNIRS and EEG metrics. We also developed a rational neuroimaging-guided NIBS approach for the cerebellar lobule (VII) and prefrontal cortex based on a healthy human study. RESULTS: Simulation of cerebellar tDCS induced gamma oscillations in the cerebral cortex, while transcranial temporal interference stimulation induced a gamma-to-beta frequency shift. A preliminary healthy human study (N = 10) found that 2 mA cerebellar tDCS evoked similar oxyhemoglobin (HbO) response in the range of 5 × 10-6 M across the cerebellum and PFC brain regions (α = 0.01); however, infra-slow (0.01-0.10 Hz) prefrontal cortex HbO-driven phase-amplitude-coupled (PAC; 4 Hz, ±2 mA (max)) cerebellar tACS evoked HbO levels in the range of 10-7 M that were statistically different (α = 0.01) across these brain regions. CONCLUSION: Our healthy human study showed the feasibility of fNIRS of cerebellum and PFC and closed-loop fNIRS-driven ctACS at 4 Hz, which may facilitate cerebellar cognitive function via the frontoparietal network. Future work needs to combine fNIRS with EEG for multi-modal imaging for closed-loop NIBS during operant conditioning.

Correction: Grey-box modeling and hypothesis testing of functional near-infrared spectroscopy-based cerebrovascular reactivity to anodal high-definition tDCS in healthy humans.

[This corrects the article DOI: 10.1371/journal.pcbi.1009386.].

Neuroimaging guided tES to facilitate complex laparoscopic surgical tasks - insights from functional near-infrared spectroscopy.

Fundamentals of Laparoscopic Surgery (FLS) is a prerequisite for board certification in general surgery in the USA. In FLS, the suturing task with intracorporeal knot tying is considered the most complex task. Transcranial direct current stimulation (tDCS) of the dorsolateral prefrontal cortex (PFC) has been shown to facilitate FLS surgical skill acquisition where 2mA tDCS for 15min with the anode over F3 (10/10 EEG montage) and cathode over F4 has improved performance score in an open knot-tying task. Since PFC has a functional organization related to the hierarchy of cognitive control, we performed functional near-infrared spectroscopy (fNIRS) to investigate PFC sub-domain activation during a more complex FLS suturing task with intracorporeal knot tying. We performed fNIRS-based analysis using AtlasViewer software on two expert surgeons and four novice medical students. We found an average cortical activation mainly at the left frontopolar PFC across the experts, while the average cortical activation across the novices was primarily at the left pars opercularis of the inferior frontal gyrus and ventral premotor cortex, inferior parietal lobule, and supramarginal gyrus. Here, the average cortical activation across the novices included not only the cognitive control related brain regions but also motor control complexity related brain regions. Therefore, we present a computational pipeline to identify a 4x1 high-definition (HD) tDCS montage of motor complexity related PFC sub-regions using ROAST software.Clinical Relevance-A computational pipeline for fNIRS-guided tES to individualize electrode montage that may facilitate FLS surgical training in our future studies.

Grey-box modeling and hypothesis testing of functional near-infrared spectroscopy-based cerebrovascular reactivity to anodal high-definition tDCS in healthy humans.

Transcranial direct current stimulation (tDCS) has been shown to evoke hemodynamics response; however, the mechanisms have not been investigated systematically using systems biology approaches. Our study presents a grey-box linear model that was developed from a physiologically detailed multi-compartmental neurovascular unit model consisting of the vascular smooth muscle, perivascular space, synaptic space, and astrocyte glial cell. Then, model linearization was performed on the physiologically detailed nonlinear model to find appropriate complexity (Akaike information criterion) to fit functional near-infrared spectroscopy (fNIRS) based measure of blood volume changes, called cerebrovascular reactivity (CVR), to high-definition (HD) tDCS. The grey-box linear model was applied on the fNIRS-based CVR during the first 150 seconds of anodal HD-tDCS in eleven healthy humans. The grey-box linear models for each of the four nested pathways starting from tDCS scalp current density that perturbed synaptic potassium released from active neurons for Pathway 1, astrocytic transmembrane current for Pathway 2, perivascular potassium concentration for Pathway 3, and voltage-gated ion channel current on the smooth muscle cell for Pathway 4 were fitted to the total hemoglobin concentration (tHb) changes from optodes in the vicinity of 4x1 HD-tDCS electrodes as well as on the contralateral sensorimotor cortex. We found that the tDCS perturbation Pathway 3 presented the least mean square error (MSE, median <2.5%) and the lowest Akaike information criterion (AIC, median -1.726) from the individual grey-box linear model fitting at the targeted-region. Then, minimal realization transfer function with reduced-order approximations of the grey-box model pathways was fitted to the ensemble average tHb time series. Again, Pathway 3 with nine poles and two zeros (all free parameters), provided the best Goodness of Fit of 0.0078 for Chi-Square difference test of nested pathways. Therefore, our study provided a systems biology approach to investigate the initial transient hemodynamic response to tDCS based on fNIRS tHb data. Future studies need to investigate the steady-state responses, including steady-state oscillations found to be driven by calcium dynamics, where transcranial alternating current stimulation may provide frequency-dependent physiological entrainment for system identification. We postulate that such a mechanistic understanding from system identification of the hemodynamics response to transcranial electrical stimulation can facilitate adequate delivery of the current density to the neurovascular tissue under simultaneous portable imaging in various cerebrovascular diseases.

Neuroimaging Guided Transcranial Electrical Stimulation in Enhancing Surgical Skill Acquisition. Comment on Hung et al. The Efficacy of Transcranial Direct Current Stimulation in Enhancing Surgical Skill Acquisition: A Preliminary Meta-Analysis of Randomized Controlled Trials. Brain Sci. 2021, 11, 707.

Surgical skill acquisition may be facilitated with a safe application of transcranial direct current stimulation (tDCS). A preliminary meta-analysis of randomized control trials showed that tDCS was associated with significantly better improvement in surgical performance than the sham control; however, meta-analysis does not address the mechanistic understanding. It is known from skill learning studies that the hierarchy of cognitive control shows a rostrocaudal axis in the frontal lobe where a shift from posterior to anterior is postulated to mediate progressively abstract, higher-order control. Therefore, optimizing the transcranial electrical stimulation to target surgical task-related brain activation at different stages of motor learning may provide the causal link to the learning behavior. This comment paper presents the computational approach for neuroimaging guided tDCS based on open-source software pipelines and an open-data of functional near-infrared spectroscopy (fNIRS) for complex motor tasks. We performed an fNIRS-based cortical activation analysis using AtlasViewer software that was used as the target for tDCS of the motor complexity-related brain regions using ROAST software. For future studies on surgical skill training, it is postulated that the higher complexity laparoscopic suturing with intracorporeal knot tying task may result in more robust activation of the motor complexity-related brain areas when compared to the lower complexity laparoscopic tasks.